Bonn zoological Bulletin 69 (2): 157-164

2020 - Ambekar M. et al.

https://do1.org/10.20363/BZB-2020.69.2.157

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:9202B 13C-4294-4049-8 DEB-42534205BDF5

A new Species of fan-throated lizard of the genus Sitana Cuvier, 1829

(Squamata: Agamidae) from northern Karnataka, India

Mayuresh Ambekar', Arya Murthy” & Zeeshan A. Mirza**

!3 National Centre for Biological Sciences, Tata Institute for Fundamental Research, Bangalore, Karnataka 560065, India

?Inventure Academy, Whitefield, Sarjapur Road, Bangalore, Karnataka 562125, India

* Corresponding author: Email: snakeszeeshan@gmail.com

'urn:lsid:zoobank.org:author:37 14B65D-DEOA-4C38-A054-BOB7EFECCF8B

7 urn:Isid:zoobank.org:author:25 DD6BF3-5EC4-40A3-ACD4-915638D4BF47

3urn:lsid:zoobank.org:author:25F673FO-3FB9-4A4F-8 1 CE-997748CC26E6

Abstract. A new species of fan-throated lizard of the genus Sitana Cuvier, 1829 is described from northern Karnataka,

India. The new species is similar to members of the clade of Sitana spinaecephalus Deepak et al., 2016, however, can

be distinguished based on morphological as well as molecular data. Sitana dharwarensis sp. nov. differs from its sister

species, S. laticeps Deepak & Giri, 2016 in bearing a much larger dewlap. Data from micro-CT scan of the cranium and

jaws further add support to the distinctness of the new species. The rivers, namely Krishna and Tungabhadra, likely act as

a biogeographic barrier for terrestrial lizard species.

Key words. Reptilia, mtDNA, molecular phylogeny, micro-CT scan, taxonomy.

INTRODUCTION

Members of the genus Sitana Cuvier, 1829 have received

considerable attention from the view of systematics, ev-

ident from the recent surge in species descriptions in the

last five years (Amarasinghe et al. 2015; Deepak et al.

2016a; b; Deepak & Karanth 2017; Sadasivan et al. 2018).

The genus currently contains eleven species, however, a

recent molecular investigation hints at the presence of ad-

ditional undescribed species (Deepak & Karanth 2017).

During the course of a herpetological investigation trip

to northern Karnataka, a state in south India, we collected

specimens of Sitana, which resembled S. laticeps Deep-

ak & Giri, 2016, and S. spinaecephalus Deepak, Vyas &

Giri, 2016 based on the dewlap coloration (Deepak et al.

2016a). Molecular data for a specimen was generated

which shows that the specimen was genetically related

to S. laticeps, however, it differed in several aspects with

regard to its morphology. Phylogenetic analysis based

on existing sequences generated by Deepak & Karanth

(Deepak & Karanth 2017) and the sequence generated in

the present work recovered two well supported clades;

one representing S. /aticeps sensu stricto occurring north

of Krishna river, and a second clade representing spec-

imens from south of the river. The clade containing se-

quences from south of Krishna river is divergent and

exhibits unique set of morphological characters which

enables us to describe it as a new species herein based on

Received: 14.11.2019

Accepted: 04.06.2020

molecular as well as morphological data, further support-

ed by its allopatric range.

MATERIALS AND METHODS

Morphology. Specimens were collected by hand, eutha-

nized and fixed in 6% formalin. They were later washed

and stored in 70% ethanol. Muscle tissue was taken pri-

or to fixation and stored for molecular work. The type

specimens are deposited in the collection of the Bom-

bay National History Society, Mumbai (BNHS) and the

collection facility of the National Centre for Biological

Sciences, Bangalore (NCBS). Specimens were measured

using a Mitutoyo™ digital caliper. Descriptive style and

morphometric/morphological characteristics were re-

corded as follows (Sadasivan et al. 2018). The following

measurements were taken: snout-vent length (SVL, from

tip of snout to anterior border of cloaca), head length

(HL, from snout tip to posterior border of tympanum),

head width (HW, distance from left to right outer edge

of the head at its widest point), head height (HH, dor-

soventral distance from top of head to underside of jaw

at transverse plane intersecting angle of jaws), snout-eye

length (SE, from snout tip to anterior border of orbit),

eye to tympanum (ET, from posterior border of orbit to

anterior border of tympanum), jaw length (JL, from ros-

trum to corner of jaw), interorbital width (IO, transverse

distance between anterodorsal corners of left and right

Corresponding editor: W. Bohme

Published: 01.07.2020

158 Mayuresh Ambekar et al.

orbits), nares to eye (NE, distance from the anterior edge

of orbit to posterior edge of naris), snout width/internasal

distance (IN, transverse distance between left and right

nares), tympanum diameter (TD, greatest diameter of

tympanum), orbit diameter (OD, distance between an-

terior and posterior margins of orbit), lower arm length

(LAL, distance from elbow to distal end of wrist, or just

underside of forefoot when the limb is flexed), upper arm

length (UAL, distance from anterior insertion of forelimb

to elbow when the limb is flexed), finger lengths (F1, F2,

F3, F4, F5) (e.g., F4 = Distance from juncture of 3rd and

Ath digits to distalmost extent of 4th finger including the

claw), femur length (FEL, length of femur from groin to

knee), crus length (CL, length of crus (tibia) from knee

to heel), hind foot length (HFL, distance from proximal

end (heel) of hind foot to distal most point of fourth toe),

hind limb length (HLL, from groin to tip of fourth toe),

toe lengths (T1, T2, T3, T4) (e.g., T4 = Distance from

juncture of 3rd and 4th digits to distal end of 4th digit on

hind foot), trunk length (TrL, from forelimb insertion to

hind limb insertion), trunk height (TrH, depth midway

between the fore and hind limb insertions), trunk width

(TrW, width midway between the fore and hind limb in-

sertions), tail length (TL, from posterior border of cloa-

cal opening to tip of tail), tail height (TH) and tail width

(TW, at tail base),dewlap length (DWL, distance between

posterior end of dewlap and tip of lower jaw), and extent

of dewlap in trunk (DWLT, measured from the axilla till

the end of the dewlap). Meristic characters were counted

for multiple individuals per species. The following char-

acters were scored: mid-body scale rows (MBS, number

of scale rows around the trunk at midbody), ventral scales

(VEN, number of scales from below mental around the

base of the dewlap to anterior border of cloaca), fourth

toe lamellae (LAM4, number of 4th toe lamellae, from

lst lamella at the digit’s cleft to the most distal lamel-

la), dewlap scales (ESD, number of enlarged scale rows

on the dewlap), supralabials (SL, posterior end defined

by the last enlarged scale that contacts the infralabials

at the corner of mouth), infralabials (IL, posterior end

defined by the posterior most enlarged scales that contact

the supralabials at the corner of the mouth), ventral scales

on the belly (VENB, number of scales posterior to the

dewlap to the anterior border of cloaca), and vertebral

scales (VS, number of scales above the vertebral column

counted from the mid-dorsal first nuchal spine to a level

directly above the cloacal opening).

Institutional abbreviations

NCBS = National Centre for Biological Sciences,

Bangalore

BNHS = Bombay Natural History Society, Mumbai

CES =Centre for Ecological Sciences, Bangalore

Bonn zoological Bulletin 69 (2): 157-164

Micro-CT scans were generated for three male spec-

imens using a Bruker® Skyscan 1272 (Bruker BioSpin

Corporation, Billerica, Massachusetts, USA). Head of

the specimens were scanned from 16 to 20 minutes at

15um. Volume rendering was performed with CTVox

(Bruker BioSpin Corporation, Billerica, Massachusetts,

USA) and images were edited in Adobe Photoshop CS6.

Osteological description is based on volume renders re-

trieved from CTVox following terminology of the skull

described by Evans (Evans 2008).

Molecular analysis. Genomic DNA was extracted

from liver tissue following Qiagen DNeasy™ Tissue kits

following protocols specified by manufacturers. We am-

plified partial segment of mitochondrial Nicotinamide

Adenine Dinucleotide Dehydrogenase Subunit 2 (VADH

2) gene with published primers L4437 5’-AAGCTTTC-

GGGCCCATACC-3’ and H5540 5’-TTTAGGGCTTT-

GAAGGC-3’ (Macey et al. 1997). A 12ul reaction was

set containing 5ul of Qiagen Taq PCR Master Mix, 4ul of

water, 0.5ul of each primer and 2ul template DNA, car-

ried out with an Eppendorf Mastercycler Nexus GSX1.

Thermo-cycle profile used for amplification were as fol-

lows: 94°C for 15 minutes, (denaturation temperature

94°C for 50 seconds, annealing temperature 59°C for 50

seconds, elongation temperature 72°C for 1 minutes) x

35 cycles, 72°C for 12 minutes, hold at 4°C. PCR product

was cleaned using QIAquick PCR Purification Kit and

sequenced with a 3730 DNA Analyzer. Sequences were

cleaned and edited in Geneious R6 v.6.18. (Kearse et al.

2012) and were also manually checked in MEGAG6. Tax-

on selection for phylogenetic analysis and additional se-

quences for the nuclear gene G protein-coupled receptor

149 (R35) were taken from Deepak et al. (2017, 2018).

Sequences were aligned with ClustalW (Thompson &

Gibson 2002) in MEGA6 (Tamura et al. 2013). Aligned

data comprised of 856 bp of ND2 and 649 bp of R35

gene which was analyzed with PartitionFinder (Lanfear

et al. 2012) for optimal partitioning strategy and evolu-

tionary substitution model. Maximum Likelihood (ML)

and Bayesian Inference (BI) analyses were employed to

infer phylogenetic relationships in RAXML (Stamatakis

2014) and MrBayes 3.2.2. (Ronquist & Huelsenbeck

2003) respectively with data partitioned by codon posi-

tions. ML analysis was run for 1000 bootstrap replicates

under GTR + G model to assess clade support. BI was

run for 10 million generations with a sampling rate of

1000 under GTR + G. The analysis was terminated after

the standard split frequency reached below 0.05. Gen-

Bank accession numbers for the sequence generated of

the holotype is MH399850. GenBank accession numbers

for sequences used in the present study are listed in sup-

porting material.

©ZFMK

A new species of fan-throated lizard of the genus Sitana Cuvier, 1829 from northern Karnataka, India [59

RESULTS

Molecular phylogenetics based on a fragment of mito-

chondrial ND2 and nuclear R35 gene recovered Sitana

specimens from northern Karnataka embedded within a

clade containing S. /aticeps and S. spinaecephalus and as

the sister taxon to S. /aticeps with high support from ML

(bootstrap 100) & BI (posterior probability 1.0). Among

the 856 sites of ND2 gene, 750 sites are conserved, 106

are variable and 40 parsimony informative sites. Mor-

phological data (see diagnosis below) and molecular

data support recognition of the population of Sitana from

northern Karnataka as a distinct species, which is de-

scried here.

Sitana dharwarensis sp. nov.

Sitana laticeps Deepak & Karanth 2018: 56—57 (in part)

Figs 1-4, Table 1

urn: lsid:zoobank. org: act:89C261E1-7E11-4SAB-9D91-927997D7A4AC

Holotype. 3 adult (NCBS-AL142); India, Karnata-

ka, Bagalkot; 16.139744° N, 75.672671° E; alt. 590 m;

14Apr. 2018; M. Ambekar, A. Murthy & Z. Mirza leg.

Paratypes. 2 299 adult (BNHS 2510, NCBS-AL143);

1 3 adult (BNHS 2509); same data as for holotype.

Diagnosis. Sitana dharwarensis sp. nov. is a large sized

species in relation to members of the Sitana spinaeceph-

alus clade, males reaching SVL of 52 mm. Dewlap large,

coloration in breeding males cream to off-white, extend-

ing up to 47% of the trunk. Parietal bone with a subtle

indentation on the anterior border, maxillary bone short

in its length and covers a smaller area of the snout, squa-

mosal long and slender gradually tapering at both ends in

a sharp tip and, quadrate robust and stout.

Sitana dharwarensis sp. nov. differs from most known

species within the genera Sitana and Sarada Deepak

et al., 2016 in bearing a white colored moderately large

dewlap (vs. dewlap in shades of red, blue and black in

Sarada spp., Sitana visiri Deepak, 2016, S. attenbor-

oughii Sadasivan et al., 2018, S. marudhamneydhal

Deepak et al., 2016, S. bahiri Amarasinghem et al. 2015,

S. devakai Amarasinghe et al., 2015). The new species

is similar to S. /aticeps and S. spinaecephalus in sharing

a white dewlap. It differs from S. /aticeps in bearing a

much larger dewlap, dewlap extending to about 47% of

Fig. 1. Sitana dharwarensis sp. nov., holotype, 6 (NCBS-AL142). a. Dorsal view of the specimen. b. Dorsal view of head. ec. Lat-

eral view of head. Scale bar: 10 mm.

Bonn zoological Bulletin 69 (2): 157-164

©ZFMK

160 Mayuresh Ambekar et al.

Table 1. Measurements and morphological details of type spec-

imens of Sitana dharwarensis sp. nov. in millimeters

Holotype Paratype Paratype Paratype

NCBS- BNHS NCBS- BNHS

AL142 2509 AL143 2510

Sex Male Male Female Female

SVL SZul 44.8 42.0 39.8

HL 14.1 132 12.4 22

HW 10.2 9.3 9.1 8.9

HH 9.5 8.2 6.7 7.0

SE aD B.2 5.0 48

ET 3.6 3.3 Bek 3.0

JL 15.4 13.9 12.6 1285

IO 8.0 as, 6.8 6.6

NE 3.5 2.8 2.6 2:5

IN 2.9 1.9 2.4 2.4

TD 2] i Be) 1.6 145

OD B03 28 2.9 2.6

LAL 8.5 6.7 6:7 6.4

UAL 10.7 6.6 6.4 6.3

F1 2.0 LS ie 1.5

F2 aa 2.9 25 D5

F3 48 4.0 4.0 3.6

F4 4.5 3.8 3.6 Bx

F5 2.9 2-6 pre 212

FEL 1a 13:0 12.5 11.7

CL 19.6 15.8 16.6 14.6

HFL 21.9 19.5 19.2 18.0

T1 2.0 LF 1.6 1.4

T2 3:0) 2.8 2.8 2.6

T3 6.0 5.0 49 49

T4 12.2 10.0 9.2 9.1

TrL Dalai 19.4 19.0 18.8

TrH 9.7 Fis) 6.9 6.0

TrWw 14.2 12.9 1256 10.6

TL - 118.5 112.4 -

TH 40 3.1 2h Diy.

TW 5.4 3.8 3.4 2.9

DWL 33 27.9 — —

DWLT 9.9 6.9 — —

the trunk (vs. 29% in S. laticeps, 45% in S. spinaeceph-

alus). Sitana dharwarensis sp. nov. further differs from

Bonn zoological Bulletin 69 (2): 157-164

S. laticeps in bearing a subtle indentation on the anterior

border of parietal (vs. a deep indentation in S. Jaticeps,

Fig. 2), the maxillary bone is short and covers a smaller

area of the snout (vs. much longer and covering a larger

area of the snout in S. /aticeps), the squamosal is long

and slender gradually tapering at both ends in a sharp

tip (vs. squamosal short, abruptly ending in a blunt tip

at both ends), quadrate 1s robust and stout (vs. slender in

S. laticeps, Fig. 2).

Genetic divergence. Genetic divergence (un-correct-

ed p-distance) between populations of S. dharwarensis

Sp. nov. was 1—2% whereas it was 34% from S. /aticeps.

Description. The holotype male (NCBS-AL142) is in

generally good condition, with an incision on the thigh

made to remove muscle tissue. The entire tail is broken

from its base and is preserved separately.

Adult male SVL 52.8 mm. Head relatively long (HL/

SVL ratio 0.27), wide (HW/HL ratio 0.72), not depressed

(HH/HL ratio 0.67), distinct from neck (Fig. la). Snout

moderately long (SE/HL ratio 0.39) bluntly conical; lon-

ger than eye diameter (OD/SE ratio 0.45) (Fig. Ic). Eye

large (OD/HL ratio 0.56); pupil round, eyelids covered

with small pentagonal and hexagonal scales, supracili-

aries short. Snout obtusely pointed when viewed dorsal-

ly, rostral much wider than deep, bordered posteriorly by

two supralabials, prenasal and dorsally by three small

scales. Canthus rostralis and supraciliary edge moder-

ately sharp consisting of nine scales. Nostrils positioned

in the centre of a large, undivided nasal plate, bordered

by eight scales (right side), including one prenasal, two

postnasals and one supranasal, and separated from ros-

tral by prenasal and supralabials. Ten rectangular, weakly

keeled supralabials, bordered above by a single row of

slightly smaller, rectangular, keeled scales. Loreal re-

gion concave, scales of the loreal region heterogeneous

in size, flat, keeled, some roughly hexagonal. Scales on

postorbital and temporal region homogenous, imbricate,

strongly keeled, and directed posteriorly and dorsally.

Orbital scales small but not granular. Tympanum naked.

Canthals enlarged, overlapping, becoming slightly small-

er along subimbricate supraciliaries, protruding slightly

laterally on supraorbital ridge. Scales on dorsal surface of

snout, forehead, interorbital, and occipital region hetero-

geneous in size, and shape; mostly elongate, imbricate,

strongly keeled longitudinally; those on snout smaller,

rhomboidal, those on forehead largest, greatly elongate:

supraorbital scales increase in size becoming more elon-

gate from supraciliaries to inner edges of orbits, of which

the enlarged scales follow the curvature of the orbit pos-

terolaterally; occipital region with slightly smaller, less

elongate; imbricate, and keeled scales. Parietal plate with

pineal eye, the plate slightly larger than adjacent scales.

Mental shield narrower than rostral; gular scales keeled.

Dewlap moderately large, extends posteriorly over 47%

©ZFMK

A new species of fan-throated lizard of the genus Sitana Cuvier, 1829 from northern Karnataka, India 161

Fig. 2. Micro-CT scan image of the cranium and jaws of Sitana dharwarensis sp. nov. (a—b) and Sitana laticeps (c—d). a, c. Dorsal

view of skull. b, d. Lateral view. Scale bar: 1 mm. Abbreviations: D = dentary, F = frontal, J = jugal, Mx = maxilla, N = nasal,

parietal, Po = postorbital, prf = prefrontal, Px = premaxilla, Q = quadrate, Sq = squamosal (Evans 2008).

of trunk length, with posterior scales extending slight-

ly beyond axila, not extending to mid-venter, approxi-

mately four to five rows of anteriodorsal dewlap scales

smaller, elongate, pointed, keeled, remainder of scales

much larger, keeled, lanceolate, bluntly pointed, gradu-

ally increasing in size towards margin, single marginal

row largest with many more pointed scales. 17 enlarged

rows of scales on dewlap. Nuchal and dorsal crest ab-

sent. Scales on nuchal region smaller, less than half the

size of those on interorbital region, imbricate, strongly

keeled. Body slender, 59 rows of scales around midbody,

of these 10—12 rows of scales on back, from occiput to

pectoral region homogenous in size, shape, slightly larg-

er than those on neck, imbricate, pointed, keeled, and

directed posteriorly forming regularly arranged longitu-

dinal rows; those on flanks heterogeneous in size, shape,

Bonn zoological Bulletin 69 (2): 157-164

smaller than those on back, obtusely pointed, keeled,

with irregularly scattered, slightly larger, pointed, keeled

scales; scales of upper rows directed backwards and up-

wards; ventral rows backwards and downwards; ventral

scales subimbricate, keeled, homogenous in size, shape,

arranged in 65 rows; no precloacal or femoral pores. 48

scales in a row from nape to the cloaca. Fore and hind

limbs relatively slender, tibia short (CL/SVL ratio 0.37);

digits moderately long, ending in strong, elongate, slight-

ly recurved claw; inter-digital webbing absent; subdigi-

tal lamellae entire, tri-mucronate, 22 subdigital lamellae

on toe IV; relative length of fingers 4>3>2>5>1, toes

4>3>2>1. Fore and hind limbs covered above and be-

low with regularly arranged, enlarged, pointed, strongly

keeled scales. Enlarged projecting scale on thigh pres-

ent. Tail entire; tail base swollen; tail uniformly covered

©ZFMK

162 Mayuresh Ambekar et al.

Fig. 3. Sitana dharwarensis sp. nov., holotype, 4 (NCBS-AL142) in life.

Fig. 4. Sitana dharwarensis sp. nov., holotype, @ (NCBS-

AL142) dewlap in life.

with similar sized, keeled, weakly pointed, regularly ar-

ranged, posteriorly directed imbricate scales, no enlarged

subcaudal row.

Coloration in preservative (Fig. 1). Coloration much

more faded, overall background coloration more yellow-

ish. Rhomboidal marks turn much paler and are almost

diffused towards the flank. Blue coloration on the lower

chin turns black.

Bonn zoological Bulletin 69 (2): 157-164

Coloration in life (Figs 3-4). Dark-brown above with

five dark rhomboidal markings on the trunk, first mark

present just posterior to the neck and the last one on the

flank. Each rhomboidal blotch has a light colored line

running through it along the vertebral column. Limbs

brown, banded with alternating dark and light bands.

Head coloration same as the body, labials banded with

light and dark bands. Dewlap yellowish white throughout

with a steel-grey to blue line running from mental to a

few scales below it. The colored line does not enter the

dewlap and terminates just before the enlarged dewlap

scales. Ventrally white.

Etymology. The specific epithet refers to the Dharwar

Craton where the species is distributed.

Variation. The paratypes resemble the holotype in most

aspects except for ventral belly scale number. The para-

type male possesses 31—32 scales. Other morphometric

and meristic characteristics are presented in Table 1.

Natural history. A species inhibiting open dry scrub and

rock terrain in northern Karnataka. The type locality is

a barren hillock adjacent to a seasonal river. The local-

ity is heavily disturbed from activities relating to stone

quarrying. The species is common at the type locality

and is found in gardens in the town. Other sympatric

reptiles observed are Eutropis cf. carinata, Hemidactylus

parvimaculatus Deraniyagala, 1953 and Hemidactylus

©ZFMK

A new species of fan-throated lizard of the genus Sitana Cuvier, 1829 from northern Karnataka, India 163

7 3/0.91

S. spinaecephalus CES 518

S. spinaecephalus NCBS AQ055

S. dharwarensis sp. nov. CES 141134

S. dharwarensis sp. nov. NCBS AL142

S. laticeps BNHS 2323

S. laticeps CES 13517

Sitana sp. CES 245

Sitana sp. CES 141114

0.02

Fig. 5. Maximum Likelihood phylogeny based on 1011bp of ND2 and 649np of R35 gene for selected Sitana species. Numbers at

nodes indicate ML/BI support.

Fig. 6. Map of south western India showing distribution of Si-

tana laticeps (black circle) and S. dharwarensis sp. nov. (aster-

isk). Inset map shows main map highlighted by the red square.

vijayraghavani Mirza, 2018. Based on available mtDNA

ND2 gene sequences, the species appears to be distrib-

Bonn zoological Bulletin 69 (2): 157-164

uted south of a tributary (Panchgana) of Krishna River

at the following localities: Bagalkot, Tumarguddi and

Koppal.

DISCUSSION

Molecular phylogenetics based on a fragment of mito-

chondrial ND2 and nuclear R35 gene recovered Sitana

dharwarensis sp. nov. embedded within a clade contain-

ing S. laticeps and S. spinaecephalus and was recovered

as sister taxon to S. /aticeps with high support from ML

(bootstrap 100) & BI (posterior probability 1.0) (Fig. 5).

The new species is 3—4% (un-corrected p-distance for

ND2 gene) divergent from available sequences of S. /ati-

ceps. Additionally, the new species is distributed south of

Panchganga River, a tributary of Krishna River, where-

as S. laticeps is distributed north of the river (Fig. 6).

The new species appears to be restricted to the area en-

compassed by the two major rivers Krishna and Tung-

abhadra. A parallel case appears to be that of the newly

described Hemidactylus vijayraghavani (Mirza, 2018)

from the same locality. These rivers likely act as biogeo-

graphic barriers for terrestrial lizards as seen in species of

the genus Sitana (Deepak et al. 2016; Deepak & Karanth

2017). The sequences of specimens CES 245 and CES

©ZFMK

164 Mayuresh Ambekar et al.

141114 used in the phylogenetic analysis potentially rep-

resent a new species.

Description of yet another species of the genus Sitana

is not surprising as recent studies provided hints on the

presence of immense genetic diversity across sampled

populations (Deepak & Karanth 2017). With additional

sampling, the number of Sitana species in the subconti-

nent will certainly rise. Morphologically cryptic species

currently considered conspecific with broadly distrib-

uted species, a common case with most lizard species

recorded from India (Agarwal et al. 2014; Agarwal &

Ramakrishnan 2017; Deepak & Karanth 2017; Mirza

et al. 2018), represent a major subset of the reptilian di-

versity of the country and hence dedicated efforts must

be made to document and describe these. Many of these

newly described species occur outside of protected areas

and in most localities, local populations are at risk from

being wiped out. A management plan for non-protected

area, especially open and scrublands that are otherwise

termed wasteland and considered less biodiverse must be

devised to ensure protection of species and habitats.

Acknowledgments. ZM acknowledges K. VijayRaghavan for

help and support at the National Centre for Biological Scienc-

es. We thank a lot a people who request anonymity for all the

help we received for work on Sitana species. Micro-CT scan

would not have been possible without the support of Sunil Pra-

bhakar and the CT scan facility team at NCBS and the NCBS

sequencing facility. Vivek Ramachandran (NCBS) and Rahul

Khot (BNHS) helped with registration of the types.

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Bonn zoological Bulletin 69 (2): 165-183

2020 - Caballero A. et al.

https://do1.org/10.20363/BZB-2020.69.2.165

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:F30B3548-7A D0-4A8C-8 1 EF-B6E2028FBE4F

The scale insect (Hemiptera: Coccomorpha) collection

of the entomological museum “Universidad Nacional Agronomia Bogota”,

and its impact on Colombian coccidology

Alejandro Caballero'*, Andrea Amalia Ramos-Portilla’, Diana Rueda-Ramirez’,

Erika Valentina Vergara-Navarro‘ & Francisco Serna®

"4° Entomological Museum UNAB, Faculty of Agricultural Science, Cra 30 N° 45-03 Ed. 500,

Universidad Nacional de Colombia, Bogota, Colombia

? Instituto Colombiano Agropecuario, Subgerencia de Proteccion Vegetal, Av. Calle 26 N° 85 B-09, Bogota, Colombia

> Research group “Manejo Integrado de Plagas”’, Faculty of Agricultural Science, Cra 30 # 45-03 Ed. 500,

Universidad Nacional de Colombia, Bogota, Colombia

*Corporacion Colombiana de Investigacién Agropecuaria AGROSAVIA, Research Center Tibaitata, Km 14,

via Mosquera-Bogota, Cundinamarca, Colombia

* Corresponding author: Email: lacaballeror@unal.edu.co; fisernac@unal.edu.co

'urn:|sid:zoobank.org:author:A4A B613B-930D-4823-B5A6-45E846FDB89B

2urn:Isid:zoobank.org:author: B7F6B826-2C68-4169-B965-1EB57AF0552B

3urn:Isid:zoobank.org:author: ECFA677D-3770-43 14-A73B-BF735123996E

4urn:Isid:zoobank.org:author: AA36E009-D7CE-44B6-8480-A FF74753B33B

>urn:|sid:zoobank.org:author: EOSAE2CA-8C85-4069-A556-7BDB45978496

Abstract. Acquisition of local and global biodiversity knowledge demands immediate and long-term efforts, both tutoring

new generations of taxonomists and establishing, maintaining and improving research collections. Through biodiversity

studies, the entomological museum “Universidad Nacional Agronomia Bogota” (Bogota, Colombia) has been developed

and has built up a substantial collection of scale insects (Hemiptera: Coccomorpha), with 7,052 slide-mounted specimens

and close to 800 alcohol-preserved samples representing 115 species belonging to 59 genera and nine families. This insect

group is exclusively phytophagous, and many species are pests on economically important crops in Colombia. Curation

of scale insect specimens includes slide mounting, identification, cataloging and databasing. Ecological and geospatial

analyses of field data have identified tnsect-host interactions, and areas of the country where new field collections should

be made. Host-insect interaction analysis has shown that coffee is the host-plant with the largest number of associated

scales, Rhizoecus cacticans (Hambleton, 1946) and Rh. colombiensis Ramos & Caballero, 2016 are the scale species with

the largest host-plant range; and Geococcus coffeae Green, 1933 and Puto barberi (Cockerell, 1895) are the commonest

scale species. Altitudinal and geographic distribution analysis have shown that sampling efforts have been concentrated

in the central region, while the northern and southeastern regions of Colombia have been poorly collected. These ana-

lyses provide a guideline for future studies, such as which zones should be sampled and which host-plant species have

information gaps in their documented distributions and scale insect-host interactions. The museum’s large number of spe-

cimens, species diversity representation and rich associated biological data indicate that the scale insect collection of the

“Universidad Nacional Agronomia Bogota” entomological museum is the most important in Colombia.

Key words. Alpha taxonomy, biodiversity conservation, Neotropical, South America, Sternorrhyncha.

INTRODUCTION

The scale insects (Hemiptera: Sternorrhyncha: Cocco-

morpha) are comprised of 55 families (20 of them ex-

tinct) and more than 8,000 extant species worldwide

(Garcia Morales et al. 2016). In Colombia, 252 species

have been recorded, representing 13 families, with hosts

in more than 40 plant families. The scale insect families

with the greatest diversity are Diaspididae (with 32% of

recorded species), followed by Pseudococcidae (26%),

Received: 09.03.2020

Accepted: 17.06.2020

Coccidae (17%) and Rhizoecidae (10%) (Garcia Morales

et al. 2016).

The Coccomorpha is an important group due to its eco-

nomic impact on agriculture worldwide (Kondo 2001;

Gullan & Martin 2003). In Colombia, over 100 species

have been recorded attacking crops such as avocado

(Persea americana Mill., 1768 ), banana (Musa paradisi-

aca L., 1753), cacao (Theobroma cacao L., 1753), coffee

(Coffea arabica L., 1753), sugarcane (Saccharum offi-

cinarum L., 1753), citrus (Citrus sp..), oil palm (Elaeis

guineensis Jacq., 1763), mango (Mangifera indica L.,

Corresponding editor: R. Peters

Published: 15.07.2020

166 Alejandro Caballero et al.

1753) and cassava (Manihot esculenta Crantz, 1766)

(Figueroa 1977; Castillo & Bellotti 1990; Gallego &

Vélez 1992; Kondo 2001; Kondo et al. 2008; Caballe-

ro et al. 2017, 2019; Ramos-Portilla & Caballero 2017).

At the international level, several scale insect species are

considered to be quarantine pest risks by the Colombian

phytosanitary protection organization, Instituto Colom-

biano Agropecuario (ICA). Its Resolution 3593 (Instituto

Colombiano Agropecuario 2015) includes scale insects

such as Aonidiella aurantii (Maskell, 1879), Comstock-

aspis perniciosa (Comstock, 1881) and Aulacaspis rosae

(Bouché, 1833) (Diaspididae), Eulecanium tiliae (L.,

1758) (Coccidae), Icerya aegyptiaca (Douglas, 1890) and

I. seychellarum (Westwood, 1855) (Monophlebidae), and

Maconellicoccus hirsutus (Green, 1908) and Pseudococ-

cus calceolariae (Maskell, 1879) (Pseudococcidae). As

endemic quarantine pest risks, the following scale insects

were mentioned: Coccus hesperidum L., 1758, Saissetia

coffeae (Walker, 1852), Icerya purchasi Maskell, 1879

and Selenaspidus articulatus (Morgan, 1889) (Instituto

Colombiano Agropecuario 2015).

The chronology of coccidology in Colombia

The first scale insect species described from Colombia

was Coccus caudatus by F. Walker in 1852, based on a

male specimen. It came from a personal collection with-

out information on its host or locality and is conserved in

the British Museum (Natural History) in London, U.K.

(Walker 1852). Coccomorpha studies in Colombia began

in 1929, when F. Laing described Crenulaspidiotus mau-

rellae and Acanthococcus tucurincae from samples col-

lected in Magdalena department (Laing 1929). The ento-

mologist L. Murillo was the first Colombian to describe

a scale insect species, Puto antioquensis from samples

taken on roots of Coffea arabica in the department of

Antioquia (Murillo 1931). Over the next two decades, 23

new species from various departments of Colombia were

described by F. Laing, E. Hambleton, N. S. Borchsentus,

R. Mamet and A. S. Balachowsky (Laing 1929; Ham-

bleton 1946; Mamet 1954; Balachowsky 1957, 1959a, b:

Beardsley 1986; Williams & Granara de Willink 1992:

Gimpel & Miller 1996;).

The Russian-born French entomologist A. S. Bala-

chowsky was one of the most important contributors to

the coccidology of Colombia. He published descriptions

of 16 species of Diaspididae, Eriococcidae, Pseudococ-

cidae and Rhizoecidae. He also provided information

from samples he collected when visiting Colombia in the

1950s and his slide-mounted specimens are conserved

in the Muséum National d‘Histoire Naturelle in France

(Balachowsky 1957, 1959a, b). The first Colombian en-

tomologist to conduct pioneering scale insect inventories

for the country was A. Figueroa: he listed five families,

34 genera and 53 species, including new records and lists

of host plants (Figueroa 1946, 1952, 1977). So far, there

Bonn zoological Bulletin 69 (2): 165-183

is no information regarding the whereabouts of his col-

lection (Caballero et al. 2017). Figueroa was followed

by F. Mosquera, who published two important papers

about the genus Ceroplastes (Coccidae) in Colombia, in

which he listed seven species, six of them presented as

new (Mosquera 1979, 1984). Slide-mounted specimens

representing those species are currently preserved in the

Coleccion Taxonomica Nacional de Insectos “Luis Maria

Murillo” (Colombia).

The last part of the 20" century was characterized by

important efforts on the recognition of species in Co-

lombia, carried out by several national and international

researchers. Castillo & Bellotti (1990) listed mealybugs

(Pseudococcidae) associated with cassava, from which

slide-mounted specimens are preserved in the Interna-

tional Center of Tropical Agricultural (CIAT) collection.

Likewise, Gallego & Vélez (1992) increased the number

of families, genera and species of Coccoidea recorded,

particularly for the families Diaspididae, Pseudococci-

dae and Coccidae. In the same year, Williams & Granara

de Willink (1992) listed and described eight species of

mealybugs (Pseudococcidae, Putoidae and Rhizoecidae)

from Colombia. Posada (1989), in his treatise on insects

in agriculture, updated the species list of Coccoidea for

Colombia to 114 taxa (93 of them to species level), asso-

ciated with more than 60 economically important crops.

In the 21% century, Colombian coccidology has been

characterized by a new insight. Through reviewing pre-

vious contributions, the coccidologist Dr. Takumasa

Kondo has led the investigation in Colombia and in the

world, publishing more than 120 peer-reviewed papers.

He has been working constantly to update the list of scale

insects in the country, and has described more than 50

new species, 14 of them from specimens collected in Co-

lombia: Akermes colombiensis Kondo & Williams, 2004,

Austrotachardiella colombiana Kondo & Gullan, 2005,

Leptococcus rodmani Kondo, 2008, Neotoumeyella cali-

ensis Kondo & Williams, 2009, Crypticerya multicica-

trices Kondo & Unruh, 2009, Bombacoccus aguacatae

Kondo, 2010, Cryptostigma philwardi Kondo, 2010,

Foldilecanium multisetosum Kondo, 2011, Hemileca-

nium guanabana Kondo & Hodgson, 2013, Toumeye-

lla coffeae Kondo, 2013, Pulvinaria caballeroramosae

Tanaka & Kondo, 2015, Capulinia linarosae Kondo &

Gullan, 2016, Cryptinglisia corpoica Kondo & Montes,

2018, Cryptinglisia ica Montes & Kondo, 2018 (Kon-

do & Williams 2004, 2009; Kondo & Gullan 2005, 2008;

Kondo & Unruh 2009; Kondo 2010a, b, 2011, 2013;

Kondo & Hodgson 2013; Tanaka & Kondo 2015; Kondo

et al. 2016a, 2018).

The Entomological Museum UNAB and its scale

insect collection

The northernmost region of South America, the so-called

Tropical Andes Hotspot, is considered to be the most

©ZFMK

Scale insects of the UNAB museum 167

biodiverse region on Earth (Conservation International

2005), and this richly biodiverse realm is under persistent

threat from human activities such as mining, timber ex-

traction, oil exploration, extensive monocrop cultivation,

and illegal trafficking of fauna and flora (FAO 2019). In

order to preserve and study that biodiversity, specialized

insect collections in universities play an essential role

in training new generations of entomologists. In 2001,

the Faculty of Agronomy (FA) at the Universidad Na-

cional de Colombia, Bogota, designated the “Universi-

dad Nacional Agronomia Bogota” (UNAB) museum as

a “Scientific Center for research and student learning

of Insect Systematics” related to agriculture (Sistema de

Patrimonio Cultural y Museos 2008). One of the great-

est achievements at the UNAB museum is the collection

and curation of close to 180,000 dry-mounted specimens,

18,400 larvae and adults preserved in alcohol, and 10,430

slide-mounted specimens as follows (rounded numbers):

Coccomorpha (7000 slides), Collembola (1700), Aphi-

domorpha (1400), Aleyrodomorpha (500), Thysanoptera

(90), Acari (90) and Psyllomorpha (50 slides). Overall,

the museum’s collections represent 4,000 species, 150

families, and 19 insect orders (Serna et al. 2017).

In the last five years there has been a notable effort

to build the Scale Insect Collection at UNAB (hereafter

referred SIC-UNAB) to become the most important col-

lection of this insect group in the country and one of the

most important in South America. This development is

derived from undergraduate and graduate theses and stud-

ies and has contributed to the knowledge of Colombian

scale insect biodiversity with descriptions of new species

and new collection records. Moreover, the SIC-UNAB

has received contributions by recognized coccidologists

like Douglass Miller (USDA Animal and Plant Health In-

spection Service, U.S.A.), Pennelope Gullan (Australian

National University, Australia), Takumasa Kondo (Cor-

poracion Colombiana de Investigacion Agropecuaria,

Colombia), Lucia Claps and Patricia Gonzalez (Univer-

sidad Nacional de Tucuman, Argentina), Bora Kaydan

(Cukurova University, Turkey) and Ana Lucia Peronti

(Sao Paulo State University, Brazil).

collection data label ~~

In view of the economic impact of scale insects and

the lack of knowledge about their diversity in Colom-

bia, our aim is to present the status of the SIC-UNAB

and acquaint the coccidologist community with the most

important scale insect collection in Colombia and one of

the most important in South America. Furthermore, our

intention is to encourage coccidologists to consider the

SIC-UNAB as a partner to develop new taxonomic stud-

ies and specimen exchanges.

MATERIALS AND METHODS

The specimens deposited in the SIC-UNAB are com-

posed mainly of insect samples collected by students

and specialists from the Universidad Nacional de Co-

lombia. The two most significant sources of samples

are from (1) Dr. Andrea Ramos working in partnership

with Instituto Colombiano Agropecuario (ICA), and (2)

the sampling conducted by the Centro de Investigacion

del Café (Cenicafé). The first covered 12 departments

of Colombia focused on the main economically import-

ant crops (1.e., Musa sp., Theobroma cacao, Coffea sp.,

Citrus sp. and Saccharum officinarum). The second was

carried out in seven departments and aimed to record the

scale insects associated with coffee roots. Other sources

of samples include the Corporacion Colombiana de In-

vestigacion Agropecuaria (Agrosavia), the Banana Asso-

ciation of Colombia (AUGURA), Bogota Botanical Gar-

den “Jose Celestino Mutis”, and exchanges with national

and international entomological museums.

The first scale insect slides were made using differ-

ent protocols, such as those standardized by Williams &

Granara de Willink (1992) and the Systematic Entomol-

ogy Laboratory (2015), U.S. Department of Agriculture,

Beltsville, MD, U.S.A. Since 2016, SIC-UNAB has

switched to a modification of the method established by

Sirisena et al. (2013), as the process is faster and avoids

the use of some carcinogenic compounds (xylene and

phenol). All samples are preserved as permanent slide-

mounts in Canada balsam.

_ identification data label |

Fig. 1. A. Slide holder with samples curated. B. Slide of a curated sample, showing the arrangement of collection and identification

data labels and specimen.

Bonn zoological Bulletin 69 (2): 165—183

©ZFMK

168 Alejandro Caballero et al.

Identifications and imaging have been carried out us-

ing a Nikon Eclipse E600 and Zeiss Axio Lab.A1 phase

contrast compound microscopes, a Lumenera Infinity

1-5C and Axiocam ERc 5s microscope cameras, and the

photograph editing software Image-Pro Insight version

8.0. Taxonomic determinations are supported by publi-

cations, comparisons with voucher specimens and spe-

cialist corroborations. The data systematization is made

using Microsoft Excel 2017® software.

Curatorship is based on the protocol given by

Martinez-Alava & Serna (2015). The scale insect da-

tabase is composed of field data and taxonomic infor-

mation, 1.e., genus, family, order, identifier, identifier

institution, identification date (dd-mmm-yyyy), curator

observations, number of specimens, sex, development

stage of specimens, and voucher specimens conserved in

ethanol. The liquid voucher specimens are preserved in

75% ethanol with the same labels inside the vials (Fig. 1).

A simple scale insect-host interaction network analy-

sis was performed with the information available in the

collection. The matrix used for the analyses comprised

quantitative data of the number of associations recorded

in the SIC-UNAB database between scale insect species

(rows) and plant hosts (columns). Network metrics were

calculated as follows: 1) number of nodes or total number

of species of the network as the sum of the number of

scale insect species with host record and the number of

host-plant species, 11) linkage density as total number of

interactions divided by the total number of plant and in-

sects species in the network, 111) connectance as the pro-

portion of actually observed interactions to all possible

interactions, being 0 when there are no interactions and 1

when all species interact, and iv) H, as the network-lev-

el specialization measure, based on the deviation of the

number of interactions of a species and the expected

number of interactions of each species (Blithgen et al.

2006; Dormann et al. 2009; Delmas et al. 2019). Also,

bipartite graphs representing the linkage between spe-

cies were constructed. Interaction analysis and figures

were performed with a bipartite package (Dormann

et al. 2008) in the open-license software R version 3.5.2

(R Development Core Team 2019).

Available data about altitude (m a.s.l.) and location

(decimal degree coordinates) were used to plot the pat-

tern of altitudinal and geographical distribution. The al-

timetry graphic was built in the console RWizard (Gui-

sande et al. 2014), based on the free statistical software

R version 3.5.2 (R Development Core Team 2019).The

geographic distribution map was developed with the soft-

ware DIVA-GIS version 7.5.0, with a physical map layer

2009).

Bonn zoological Bulletin 69 (2): 165-183

RESULTS AND DISCUSSION

To date, the SIC-UNAB preserves 7,052 curated spec-

imens, resulting from more than 1,000 samples. The

collection has records of 131 taxa, of which 115 are

identified to species level, 3 are identified as species

complexes and 13 identified to genus level (see Appendix

I: Table 1). The 115 species belong to 57 genera and nine

families. The highest diversity is represented by species

of Pseudococcidae (34.1%), followed by Rhizoecidae

(23.2%). The remainder of the species are divided be-

tween Diaspididae (18.8%), Coccidae (10.9%), Orthe-

ziidae (2.9%), Monophlebidae (2.9%), Asterolecaniidae

(2.2%), Putoidae (2.2%), Eriococcidae (1.4%), Dacty-

lopiidae (0.7%) and Margarodidae (0.7%). Worldwide,

the most diverse scale insects families are Diaspididae (>

2,600 spp.), Pseudococcidae (> 2,000 spp.) and Coccidae

(> 1,100 spp.), but SIC-UNAB conserves a rich on rep-

resentation of Pseudococcidae and Rhizoecidae because

the research projects that have provided samples to the

collection were focused on the diversity of mealybugs in

the broad sense, i1.e., Pseudococcidae, Rhizoecidae and

Putoidae.

The scale insects-host interaction network based on

samples deposited in the SIC-UNAB 1s shown in Fig-

ure 2. The interaction network based on the information

available at the SIC-UNAB consisted of 222 nodes, cor-

responding to a total of the scale insect species and their

host-plant species. Of the 131 taxa, 120 have host data,

with 102 plant species. In the network, 227 interactions

or links were recorded, with a density of 1.023 links

per species. Around 70% of the scale insect species are

recorded with only one host-plant species.

The network metrics of the data were low, with a con-

nectance value of 0.019 and H, of 0.604. Connectance

values close to zero indicate little interaction between

the species, and the low H, index indicates a high lev-

el of specialization of the species in the network. These

metrics provide preliminary knowledge of the associa-

tion between scale insects and their hosts in Colombia.

The scale insect species with the highest number of

interaction records (grade) with host plants are Rhizoe-

cus cacticans (Hambleton, 1946) and Rhizoecus colom-

biensis Ramos & Caballero, 2016. The polyphagous

habit of R. cacticans is confirmed and its range of host

records is increased. The SIC-UNAB conserves samples

of this species associated with 34 hosts, of which 23 are

new records (Appendix I: Table 1). This new informa-

tion broadens its host-range from 32 to 53 plant species.

Rhizoecus colombiensis was described from specimens

collected and preserved in SIC-UNAB, hence most of

the hosts that have been recorded for this species are

the same as are presented in this paper, except for four

plant species recorded here for the first time (See under-

lined names of hosts in Appendix I: Table 1).

©ZFMK

® Saccharicoccus sacchari

e Dystaicoccus boninsis

Pulvinaria elongata

®@ Duplachionaspis divergens

® Pinnaspis strachani

® Macrocepicoccus loranthi

® Planococcus halli

@ Maconellicoccus hirsutus

@Unaspis citri

® Lepidosaphes beckii

® Philephedra tuberculosa

®@Ferrisia sp.

@Ferrisia dasylirii

® Diaspis boisduvalii

® Pseudococcus elisae

®@ Dysmicoceus brevipes

& Capitisetella migrans

® Geococcus johorensis

@ Geococcus coffeae

@ Rhizoecus calombiensis

@ Rhizoecus arabicus

® Dysmicoccus texensis

@ Ripersiella andensis

©@ Dysmicoccus neobrevipes

® Dysmicoccus complx joannesiae

®@ Dysmicoccus radicis

® Mixorthezia minima

@ Phenacoceus sisalanus

@ Rhizoecus spinipes

® Coccidella ecuadorina

®@Dysmicoccus varius

@ Neochavesia caldasiae

® Phenacoccus solani

§ Ripersiella campestris

§ Williamsrhizoecus coffeae

@ Dysmicoccus perotensis

®@ Coccus viridis

@ Akermes colombiensis

®@ Dysmicoccus mackenziei

®@ Spilococcus pressus

® Coccus sp.

® Dysmicoceus sp.

® Toumeyella sp.

®@ Toumeyella coffeae

@ Pseudorhizoecus bari

@ Dysmicoccus caribensis

®@ Dysmicoccus grassii

@ Rhizoecus americanus

@ Rhizoecus coffeae

®@ Planoceccus minor

® Pseudorhizoecus proximus

@ Rhizoecus variabilis

® Phenacoccus parvus

® Chorizococcus caribaeus

@ Rhizoecus mayanus

@ Rhizoecus compotor

@ Rhizoecus atlanticus

& Rhizoecus stangei

® Mixorthezia neotropicalis

@Ferrisia uzinuri

@ Akermes sp.

®@ Pseudococecus landoi

= Puto barberi

@ Dysmicoccus complx fexensis

@ Rhizoecus setosus

; @ Rhizoecu s caladii

8 Kurhizococcus colombianus

@ Rhizoecus cacticans

®@ Coccus hesperidum

@ Coccidella sp.

@ Spilococcus mamillariae

@Phenacoccus hurdi

®@Saissetia coffeae

® Pseudococcus calceolariae

@ Saissetia sp.

®@ Hemiberlesia rapax

®@ Chrysomphalus die oepern

®Ferrisia kondoi

® Pinnaspis aspidistrae

® Crypticerya abrahami

e Hemileeantan guanabana

§ Acanthococcus mokanae

® Protopulvinaria longivalvata

® Aonidiella orientalis

®@ Pseudaonidia trilobitiformis

® Pseudoparlatoria bennetti

®@ Ischnaspis longirosiris

® Pseudoparlatoria suelda

e ee genistae

a Uhieria araucariae

® Aonidiella comperei

® Pseudococcus longispinus

® Planchonia stentae

Lt beaetey da pustulans

@ Pinnaspis buxt

® Toumeyella pini

@ Puto mexicanus

& Rhizoecus cyperalis

@ Pseudoparlatoria parlatorioides

@ Ceroplastes mosquerai

® Asterolecaniidae

@ Coccidae

@ Ortheziidae

Scale insects of the UNAB museum

Saccharum officinarum

Ficus sp.

Lagerstroemia speciosa

Psidium guineense

Mangifera indica

Gossypium sp.

Amaranthus sp.

Spondias sp.

Musa sp.

Crocosmia sp.

Musa acuminata

Cyperus sp.

Coffea arabica

Conyza bonaeriensis

Cuphea lanceolata

Emilia sonchifolia

Equisetum sp.

Erigeron bonariensis

Panicum maximum

Plantago major

Bidens pilosa

Morus sp.

Archontophoenix cunninghamiana

Cyperus ferax

Galinsoga parviflora

Paspalum notatum

Commelina diffusa

Populus sp.

Eleusine indica

Holcus sp.

Spermacoce alata

Aloe vera

Hibiscus sp.

Moss

Pennisetum clandestinum

Rumex acetosella

Bromus sp.

Chrysanthemum sp.

Conyza sp.

Cynodon dactyion

Dactylis glomerata

Holcus lanatus

Hypochoeris sp.

Ipomoea sp.

Lolium sp.

Oreopanax fluribundus

Oxalis sp.

Polygonum nepalense

Polygonum sp.

Richardia scabra

Rumex crispus

Sida sp.

Taraxacum officinale

Tradescantia gracilis

Trifolium pratense

Trifolium repens

Sonchus sp.

Sonchus oleraceous

Oxalis corniculata

Sida acuta

Anthurium sp.

Lantana camara

Mamumillaria sp.

Tecoma grandis

Tecoma sp.

Ficus americana

Prunus persica

Retrophyllum sd a

Syzygium paniculatum

Ficus andicola

Theobroma cacao

Callistemon sp.

Licania tomentosa

Annona muricata

Capsicum sp.

Hibiscus sp.

Citrus sp.

Nerium oleander

Cocos nucifera

Elaeis oleifera X Elaeis guineensis

Veitchia merrillii

Persea americana

Arachis pintoi

Araucaria heterophylla

Cryptomeria japonica

Arbutus unedo

Phormium tenax

Citrus aurantifolia

Citrus sinensis

Cyclamen persicum

Euphorbia trigona

Liriope sp.

Manilkara zapota

Monstera deliciosa

Opuntia sp.

Passiflora edulis

Pinus silvestris

Quercus humboltii

Rosa sp.

Thymus vulgaris

Sercoyucca elephantipes

Solanum betaceum

~ Dactyloptidae

@ Pseudococcidae

@ Saccharicoccus sacchari

® smicoccus boninsis

Pulvinaria elongata

©@ Duplachionaspis divergens

® Pinnaspis strachani

® Macrocepicoceus loranthi

®@ Planococcus hallt

® Leptococcus neotropicus

® Maconellicoccus hirsutus

@Unaspis citri

®@ Philephedra tuberculosa

® Ferrisia sp.

@Ferrisia dasylirii

®@ = Pseudococcus jackbeardsleyi

® Diaspis boisduvalii

@ = Pseudococcus elisae

& Capitisetella migrans

B Geococcus johorensis

™ Geococcus coffeae

@ Rhizoecus colombiensis

@ Rhizoecus arabicus

@ = Dysmicoccus texensis

@ Ripersiella andensis

®@ Dysmicoccus radicis

® Mixorthezia minima

®@ Phenacoccus sisalanus

@ Rhizoecus spinipes

®@ Coccidella ecuadorina

@ Dysmicoccus varius

| Neochavesia caldasiae

® Phenacoccus solani

@ Ripersiella campestris

& Williamsrhizoecus coffeae

® Coccus viridis

@ Akermes colombiensis

@ = Dysmicoccus mackenziei

Spilococcus pressus

@ Cocecus sp.

®@ Toumeyelia sp.

®@ Toumeyella coffeae

= Pseudorhizoecus bari

@ Dysmicoccus caribensis

®@ Dysmicoccus grassii

@ Rhizoecus americanus

@ Rhizoecus coffeae

®@ Planococeus minor

@ Rhizoecus variabilis

®@ Phenacoccus parvus

® Chorizococcus caribaeus

@ Rhizoecus mayanus

@ Rhizoecus compotor

@ Rhizoecus atlanticus

@ Rhizoecus stangei

@Ferrisia uzinuri

@ Akermes sp.

® Hemiberlesia sp.

® Odonaspis sp.

= Puto barberi

@ = Dysmicoccus complx texensis

@ Rhizoecus setosus

®@ Planococcus complx citri-minor

@ Rhizoecus caladii

@ = Lurhizococcus colombianus

| Rhizoecus cacticans

® Coccus hesperidum

= Coccidella sp.

@Pulvinaria psidii

@ Spifococcus mamillariae

® Saissetia coffeae

®Ferrisia wilamsi

® Pseudococcus calceolariae

@ Chrysomphatus dictyospermi

®Ferrisia kondoi

® Hemiletaniun guanabana

& Acanthococcus mokanae

®@ Protopulvinaria longivalvata

® Aonidiella orientalis

@Parlatoria ziziphi

® Pseudaonidia trilobitiformis

® Ischnaspis longirostris

®@ Pseudoparlatoria suelda

e 7 eB genisitae

ahieria araucariae

® Melanaspis sp.

® Aonidiella comperei

eo Paruidcocens longispinus

@ Planchoniad stentae

® Hemiberlesia cyanophyllt

= Russellaspis pustulans

@ Pinnaspis buxi

® Pseudaulacaspis pentagona

® Toumeyella pini

@ Puto mexicanus

@ Rhizoecus cyperalis

@ Pseudoparlatoria parlaiorioides

@ Ceroplasies mosquerai

@ Diaspididae

®@ Putoidae

® Eriococcidae

@ Rhizoecidae

169

Saccharum officinarum

Ficus sp.

Lagerstroemia speciosa

Psidium guineense

Mangifera indica

Gossypium sp.

Amaranthus sp.

Spondias sp.

Musa sp.

Crocosmia sp.

Musa acuminata

Cyperus sp.

Coffea arabica

Conyza bonaeriensis

Cuphea lanceolata

Emilia sonchifolia

Equisetum sp.

Erigeron bonariensis

Panicum maximum

Plantago major

Bidens pilosa

Morus sp.

Archontophoenix cunninghamiana

Cyperus ferax

Galinsoga parviflora

Paspalum notatum

Commelina diffusa

Populus sp.

Eleusine indica

Holcus sp.

Spermacoce alata

Aloe vera

Hibiscus sp.

Moss

Pennisetum elandestinum

Rumex acetosella

Bromus sp.

Chrysanthemum sp.

Conyza sp.

Cynodon dactylon

Dactylis glomerata

HAolcus lanatus

Hypochoeris sp.

Ipomoea sp.

Lolium sp.

Oreopanax fluribundus

Oxalis sp.

Polygonum nepalense

Polygonum sp.

Richardia scabra

Rumex crispus

Sida sp.

Taraxacum officinale

Tradescantia gracilis

Trifolium pratense

Trifolium repens

Sonchus sp.

Sonchus oleraceous

Oxalis corniculata

Sida acuta

Anthurium sp.

Lantana camara

Mamiunillaria sp.

Tecoma grandis

Tecoma sp.

Ficus americana

Prunus persica

Retrophylium rospiglios ii

Syzygium paniculatum

Ficus andicola

Theobroma cacao

Callistemon sp.

Licania tomentosa

Annona muricata

Capsicum sp.

Hibiscus sp.

Citrus sp.

Nerium oleander

Cocos nucifera

Elaeis oleifera X Elaeis guineensis

Veitchia merrillii

Persea americana

Arachis pintoi

Araucaria heterophylla

Cryptomeria japonica

Arbutus unedo

Phormium tenax

Citrus aurantifolia

Citrus sinensis

Cyclamen persicum

Euphorbia trigona

Liriope sp.

Manilkara zapota

Monstera deliciosa

Opuntia sp.

Passiflora edulis

Pinus silvestris

Quercus humboltii

Rosa sp.

Thymus vulgaris

Sercoyucca elephantipes

Solanum betaceum

@ Margarodidae

Fig. 2. Interaction network of association between scale insects and hosts based on storage samples in the scale insect collection

of the entomological museum “Universidad Nacional Agronomia Bogota” (SIC-UNAB). A. The bipartite graph on the left em-

phasizes scale insect species with the same color indicating the rectangle of the species and the line of the link. B. The graph on

the right emphasizes plant hosts and their links. The width of the rectangle next to each species name is proportional to the sum of

interactions involving this species, while the width of the lines linking scale insect species and plant species is again proportional

to the number of interactions between the connected species.

Bonn zoological Bulletin 69 (2): 165-183

©ZFMK

170

Ripersiella kellaggi

Puto mexicanus

Ceroplastes mosquerai

Saissetia sp.

Rhizoecus cyperalis

Pseudoparlatoria parlatorioides

Phenacoccus hurdi

Hemiberlesia rapax

Chrysomphalus dictyospermi

Uhleria araucariae

Pseudococcus longispinus

Pseudococcus calceolariae

Spilococcus mamillariae

Planchonia stentae

Dactylopius sp.

Rhizoecus cacticans

Coccidella sp.

Puto antioquensis

Pulvinaria psidii

Melanaspis sp.

Hemiberlesia sp.

Coccidella ecuadorina

Mixor thezia neotropicalis

Dysmicoccus sylvarum

Dysmicoceus mackenziei

Dysmicoceus quercicolus

Eurhizococcus colom bianus

Rhizoecus setosus

Rhizoecus caladii

Rhizoecus stangei

Spilococcus pressus

Coecus sp.

Ferrisia uzinuri

Pseudococcus landoi

Pulvinaria elongata

Rhizoecus compotor

Rhizoecus arabicus

Dysmicoecus radicis

Planocoeccus halli

Coccus hesperidum

Rhizoecus mayanus

Coceus viridis

Dysmicoceus neobrevipes

Dysmicoecus caribensis

Dysmicoccus complex joannesiae

Dysmicoccus complex texensis

Rhizoecus colombiensis

Dysmicoecus texensis

Geococcus coffeae

Akermes colombiensis —

Dysmicoccus varius

Dysmicoccus grassii

Puto barberi

Hemiberlesia eyanophylli

Ischnaspis longirostris

Insignorthezia insignis

Toumeyella coffeae

Saissetia coffeae

Rhizoecus variabilis

Phenacoccus solani

Pinnaspis buxi

Rhizoecus spinipes

Planococeus complex citri-minor

Pseudokermes vitreus

Ripersiella andensis

Rhizoecus americanus

Phenacoceus parvus

Dysmicoccus sp.

Planocoecus minor

Rhizoecus atlanticus

Chorizececcus caribaeus

Neochavesia caldasiae

Protopulvinaria pyriformis

Rhizoecus coffeae

Pseudococcus elisae

Dysmicoccus boninsis

Phenacoccus sisalanus

Dysmicoceus brevipes

Mixorthezia minima

Toumeyella sp.

Dysmicoccus perotensis

Pseudorhizoecus bari

Akermes sp.

Phenacoceus madeirensis

Laurencella colombiana

Williamsrhizoecus coffeae

Crypticerya brasiliensis

Pinnaspis aspidistrae

Saccharicoceus sacchari

Pseudoparlatoria bennetti

Macrocepicoccus loranthi

Hemilecanium guanabana

Crypticerya abrahami

Diaspis boischevalii

Ferrisia williamsi

Aonidiella orientalis

Rhizoecus neostangei

Maconellicoceus hirsutus

Ripersiella campestris

Duplachionaspis diver gens

Pseudorhizoecus proximus

Crypticerya genistae

Ferrisia kondoi

Pinnaspis strachani

Philephedra tuberculosa

Aonidiella comperei

Toumeyella pini

Protopulvinaria longivalvata

Phenacoccus dearnessi

Antonina graminis

Aspidiotus destructor

Capitisetella migrans

Geococcus johorensis

Russellaspis pustulans

Pseudococeus jackbeardsleyi

Pseudaonidia trilobitiformis

Ferrisia dasylirii

Ferrisia sp.

Parlatoria ziziphi

Acanthococcus mokanae

Species

500

1000

ote

Alejandro Caballero et al.

ma.s.l.

1500

2000

doeeemooses, x

2500

3000

Sd oo 60¢ & 00 OO 66 + 6B ONE 40O HO OO

Eriococcidae

Pseudococcidae

Monophlebidae

Rhizoecidae

Diaspididae

Asterolecaniidae

Coccidae

Ortheziidae

Putoidae

Margarodidae

Dactylopiidae

Fig. 3. Altimetry graphic with range by species given in meters about sea level (m a.s.1.). Each point indicates one sample. Color

and shape indicate taxonomic family.

Bonn zoological Bulletin 69 (2): 165-183

©ZFMK

Scale insects of the UNAB museum 171

Puto barberi (Cockerell, 1895) and Geococcus coffeae

(Green, 1933) are the species most recurrent in the collec-

tion samples (Fig. 2 A), but this contrasts with their host

associations. Both species have several samples on Cof-

fea arabica (Rubiaceae), due to the large sampling effort

on coffee in one of the most important projects that built

the collection (Caballero et al. 2018, 2019). Puto barberi

is recorded in association with Hibiscus sp. (Malvaceae),

however, this species is polyphagous and has been re-

corded from more than 50 plant species (Williams et al.

2011; Garcia Morales et al. 2016). Geococcus coffeae is

also polyphagous, associated with 63 plant species (Wil-

liams 1968; Garcia Morales et al. 2016), however, in the

collection it is recorded on only four hosts, one of them

corresponding to an earlier record (C. arabica) and three

new records, 1.e., Crocosmia sp. (Iridiaceae), Galinsoga

parviflora (Asteraceae) and Musa acuminata (Musace-

ae).

The plant species with the highest number of interac-

tions with scale insect species (63) was C. arabica, which

is also an indicator of the large sampling effort in coffee

cultivation. The remaining plant species are recorded in

association with no more than seven species of scale in-

sects (Fig. 2B).

The focus of the UNAB museum Is agricultural ento-

mological diversity, which means the study of arthropods

associated with plant species of agricultural importance.

As aresult of different studies, the SIC-UNAB preserves

samples that represent 45% (63 species) of the world-

wide scale insect diversity recorded on C. arabica, which

is 141 species (Garcia Morales et al. 2016; Caballe-

ro et al. 2019). Other plants of agricultural importance

for Colombia are cotton (Gossypium sp.) and plantain

(Musa acuminata Colla, 1820), both with seven scale in-

sect species recorded, banana (Musa paradisiaca) with

Six; Sugarcane (Saccharum officinarum) with five; man-

go (Mangifera indica) with four; and soursop (Annona

muricata L., 1753) with three. The number of associa-

tions are indicated in Figure 2B.

Altitudinal and geographic distribution

The analysis showed that Rhizoecus colombiensis 1s

the species with the widest altitude range, being pres-

ent from 6 ma.s.l. on M. acuminata to 2,792 m a.s.l. on

Holcus sp. (Poacaeae) (Fig. 3). The species is polyph-

agous (Ramos-Portilla & Caballero 2016) and its hosts

include banana and plantains (Musa sp.), which can grow

from sea level up 2,000 m a.s.l., Coffea arabica, which

can grow between 1,000 and 2,300 m a.s.l. (Federacion

Nacional de Cafeteros 2013), and Holcus sp. which is

able to grow up to 3,300 m as.l. (Apraez et al. 2019).

Other species with wider altitude range are R. arabicus,

R. cacticans and G. coffeae (Rhizoecidae) which cover

around 2,000 meter. Rhizoecus arabicus and G. coffeae

Bonn zoological Bulletin 69 (2): 165-183

were found from sea level to 2,200 m a.s.l., and R. cacti-

cans from 1,200 m a.s.l. to 3,100 maz.s.l.

Pseudokermes vitreus (Cockerell, 1894) and Cryptic-

erya brasiliensis (Hempel, 1900) both present a special

situation. For each of these species there are only two

samples, and in each case, the samples are from extreme

altitude points with more to 2,000 meters between them

(Fig. 3). The altitude points for P. vitreus are 244 and

2,694 m a.s.l. in Caqueta and Boyaca departments, re-

spectively. Crypticerya brasiliensis was found at 24

and 2,357 m a.s.l., in Providencia Island and Boyaca,

respectively. These data agree with previously recorded

information on both species, which are polyphagous and

associated with plants from warm and temperate regions

(Kondo & Hardy 2008; Garcia Morales et al. 2016; Kon-

do et al. 2016b).

Regarding the geographic distribution, the SIC-UNAB

has an important representation of the Colombian Coc-

comorpha fauna from the Andean and Caribbean bio-

geographic regions (Fig. 4). This bias 1s due to UNAB

projects that have been focused on coffee crops, which

are mostly cultivated in the Andean region.

A sanctuary for scale insects in Colombia

Research on SIC-UNAB has provided new records of spe-

cies and hosts for Colombia and Mexico, taxonomic keys

and descriptions of new scale insect species found on

crops such as citrus, sugarcane and coffee (Kondo et al.

2016b; Ramos-Portilla & Caballero 2016, 2017; Caballe-

ro et al. 2017, 2018; Caballero & Ramos-Portilla 2018).

In addition, the collection has authoritative taxonomic

determinations and stores type material of Acanthococ-

cus mokanae Gonzalez, Ramos & Caballero, 2019, Fer-

risia williamsi Kaydan & Gullan, 2012, Rhizoecus co-

lombiensis Ramos & Caballero, 2016, Pseudorhizoecus

bari Caballero & Ramos, 2018, Tillancoccus koreguajae

Caballero & Ramos, 2018 and Williamsrhizoecus coffeae

Caballero & Ramos, 2018 (see Appendix I: Table 1).

Compared to the main scale insect collections of Co-

lombia, the SIC-UNAB conserves the most significant

collection, as we show below:

Instituto Alexander Von Humbolt (I[AVH): No scale in-

sect specimens (J.C. Neita, Bogota, pers. comm. 2020).

International Center for Tropical Agriculture Arthro-

pod Reference Collection (CIATARC): 259 slide-mount-

ed scale insect specimens, 84 voucher liquid samples,

representing six families, 21 genera, and 29 species (data

of genera and species no provided) (M.I. Gomez, Valle

del Cauca, pers. Comm. 2019).

Coleccion Taxonomica Nacional de Insectos Luis Ma-

ria Murillo (CTNI): 631 slide-mounted specimens of two

families: Coccidae with six genera and 14 species, Rhi-

zoecidae one genus and one species. This collection con-

serves type material of Bombacoccus aguacatae Kondo,

2010 (holotype), Ceroplastes boyacensis Mosquera, 1979

©ZFMK

72 Alejandro Caballero et al.

S nm rn

@ Asterolecaniidae . $

® Coccidae

A Dactylopiidae

Z A Diaspididae

Monophlebidae

++ Pseudococcidae

. + Putoidae

+ Rhizoecidae

kilometers

Fig. 4. Map of Colombia with distribution of Coccomorpha samples under conservation in Scale Insect Collection of entomological

museum “Universidad Nacional Agronomia Bogota” (SIC-UNAB). Samples discriminated by families with symbols and colors.

Bonn zoological Bulletin 69 (2): 165-183 ©ZFMK

Scale insects of the UNAB museum 173

(holotype and paratypes), Ceroplastes cundinamarcensis

Mosquera, 1979 (holotype and paratypes), Ceroplastes

martinae Mosquera, 1979 (holotype and paratypes),

Ceroplastes mosquerai Ben-Dov, 1993 (holotype and

paratypes), Ceroplastes ocreus Mosquera, 1984 (holo-

type and paratypes), Ceroplastes trochezi Mosquera,

1979 (holotype and paratypes), Cryptinglisia corpoica

Kondo & Montes (holotype and paratypes), Cryptinglisia

ica Montes & Kondo (holotype and paratypes), Pulvinar-

ia caballeroramosae Tanaka & Kondo, 2015 (paratypes),

and Rhizoecus colombiensis Ramos-Portilla & Caballero,

2016 (paratype) (E. Vergara, Bogota, pers. Comm. 2020)

Museo Entomologico Francisco Luis Gallego (ME-

FLG): 52 slide-mounted scale insect specimens. Pseudo-

coccidae: 13 genera, 24 species. Diaspididae: 15 genera,

22 species. Margarodidae: seven genera, eight species.

Coccidae: 13 genera, 19 species. (J. Quiroz, Medellin,

pers. Comm. 2019)

Museo de Historia Natural del Instituto de Ciencias

Naturales (ICN): 15 slide-mounted scale insect specimen

of families Pseudococcidae and Coccidae (data of genera

and species no provided). This collection conserves ma-

terial Type of Leptococcus rodmani Kondo, 2008 (para-

type) and Akermes colombiensis Kondo & Williams,

2004 (paratype). (F. Fernandez, Bogota, pers. Comm.

2019)

Universidad Nacional Agronomia Bogota (UNAB):

7,052 slides-mounted scale insects specimens (details in

Appendix I: Table 1).

New records for Colombia

Geococcus johorensis Williams, 1969 [UNAB N° cat.

1861]* COLOMBIA: Antioquia, Apartado, Vda. Chu-

ridé, Fea. Villa Nancy, 7°47°38.72” N, 76°38°56.94” W,

27 m a.s.l., ex roots Musa acuminata (AAB) (Musace-

ae), Feb-2015, collector N. Herrera, 6 99 adults; An-

tioquia, Carepa, Vda. Las Trecientas, Fca. Villa Adis,

7°46’56.93” N, 76°46°6.56” W, 17 m as.l., ex roots

Musa acuminata (AAB) (Musaceae), Feb-2015, col-

lector O. Giraldo, 7 9° adults; Antioquia, Chigorod6,

Vda. Saden Guacamaya, Fca. Las Anitas, 7°42’45.86” N,

76°46’23.09” W, 6 m as.l., ex roots Musa acumina-

ta (AAB) (Musaceae), Feb-2015, collector N. Herrera,

3 9° adults; Antioquia, Chigorod6, Vda. Saden Can-

delaria, Fea. Dofia Mayo, 7°42750.26”N, 76°46’6.56” W,

6ma.s.l., ex roots Musa acuminata (AAB) (Musaceae),

Feb-2015, collector O. Giraldo, 6 99 adults; Antioquia,

Chigorod6, Vda. Saden Colorada, Fca. San Ignacio,

7°42’18.72” N, 76°46°23.09” W, 6 m as.l., ex Musa

acuminata (AAB) (Musaceae), Feb-2015, collector L.

Escobar, 5 9 9 adults; Antioquia, Turbo, Vda. Barro Col-

orado, Fea. Villa Arelis, 8°1’43.18” N, 76°39’26.89” W,

26 m a.s.l., ex roots Musa acuminata (AAB) (Musace-

ae), Feb-2015, collector N. Herrera, 4 99 adults; An-

tioquia, Turbo, Vda. Barro Colorado, Fca. La Mejor Es-

Bonn zoological Bulletin 69 (2): 165-183

quina N° 2, 8°1°55.45” N, 76°39°56.52” W, 25 mas.l.,

ex roots Musa acuminata (AAB) (Musaceae), Feb-2015,

collector O. Giraldo, 2 99 adults; Antioquia, Turbo,

Vda. La Esperanza, Fca. La Esperanza, 8°5’43.76” N,

76°40’ 16.68” W, 21 m as.l., ex roots Musa acumina-

ta (AAB) (Musaceae), Feb-2015, collector L. Escobar,

2 2° adults; Antioquia, Turbo, Vda. Villa Maria, Fca.

Los Tres Hermanos, 8°6’41.98” N, 76°42’24.52” W,

5 m. a.s.l. ex roots Musa acuminata (AAB) (Musaceae),

Feb-2015, collector L. Escobar, 5 9 9 adults.

* All samples with the same catalogue number.

Phenacoccus hurdi McKenzie, 1964 [UNAB N° cat.

1861] COLOMBIA: Cundinamarca, Bogota D.C., Lo-

calidad Teusaquillo, Universidad Nacional de Colombia.,

4°38°9.49” N, 74°5’°20.22” W, 2564 m a.s.l., ex leaves,

stems, and flowers of Lantana camara (Vervenaceae).

2-Abr-2012, collector A. Caballero, 10 9° adults.

Puto mexicanus (Cockerell, 1893) [UNAB N° cat.

5538] COLOMBIA, Boyaca, Arcabuco, 5°44’17.00” N,

74°24’52.00” W, 2742 m a.s.l., ex leaves of Quercus

humboldtii (Fagaceae). 10-Abr-2019, collector P. Rodri-

guez, 3 29 adults and 4 9 9 3rd instars.

CONCLUSIONS

In a megadiverse country like Colombia, research to in-

crease awareness of diversity, with taxonomy as the main

tool, should be a priority. The entomological museum

UNAB contributes to this crucial task through curation

and conservation of specimens as vouchers of species

richness. Its collection of scale insects has become the

most important in Colombia due to the number of speci-

mens, diversity of species and associated information on

their geographical distribution. The information stored in

this collection has contributed to the knowledge of Coc-

comorpha taxonomy and Colombian phytosanitary sta-

tus, providing a list of 115 species, new records of three

scale insects and 61 host plants and distribution informa-

tion. Of the 252 species recorded so far for Colombia,

the SIC-UNAB has 115 species 1.e., 41% of total of the

current Colombian Coccomorpha diversity. This col-

lection provides new information about associations of

scale insects with host plants of economic importance to

Colombia, their locations, and confirmation of previous

records. This information will be useful to phytosanitary

authorities and will enable research centers to plan regu-

lation and investigation activities.

The ecological analysis allowed us to infer the sam-

pling frequency by species, and to identify association

networks between scale insects and their hosts, and geo-

spatial distributions. The analysis presented here gives

an insight into how to direct and structure new research.

Based on the geographic analysis, the SIC-UNAB should

©ZFMK

174 Alejandro Caballero et al.

redirect its field collecting to northern, west, and south-

eastern Colombia, which coincides with biodiversity

hotspots such as the Caribbean, Pacific and Amazonas re-

gions. New analyses of species richness and host associ-

ations should be directed towards economically import-

ant crops to evaluate their impact in ecosystems of the

country. Good examples might be banana and avocado

crops, whose cultivated areas are substantial in Colom-

bia and their production systems influence other associ-

ated plant species. Regarding identification methodolo-

gy, so far the UNAB museum had used a morphological

approach but in the future, it should include molecular

techniques and ecological analysis as new information

sources, trying to get closer to integrative taxonomy.

The mission of the entomological museum UNAB, as

part of a public institution and as an element of the most

important university in Colombia, is to provide informa-

tion about Colombian insect diversity and related issues.

In that sense, we encourage the coccidology community

to consider the SIC-UNAB as a collaborating institution

in future studies and for housing samples.

Acknowledgements. We thank Takumasa Kondo (AGRO-

SAVIA, Colombia), Lucia Claps (Universidad Nacional de

Tucuman, Argentina), Ana Lucia Peronti (Sao Paulo State Uni-

versity, Brazil), Douglass Miller (USDA, U.S.A.) and Penny

Gullan (The Australian National University, Australia) for their

identifications. We are grateful to Pedro Rodriguez and staff

of the Instituto Colombiano Agropecuario (ICA), Pablo Bena-

vides, Zulma Gil and staff of the Centro de Investigaciones del

Café (CENICAFE) for providing samples. The SIC-UNAB

project was funded by the Facultad de Ciencias Agrarias of

Universidad Nacional de Colombia, sedé Bogota. Thanks are

also due to Fernando Fernandez and Jhon Albeiro Quiroz (Uni-

versidad Nacional de Colombia), Cesar Neita (Instituto de In-

vestigacion de Recursos Biologicos Alexander von Humboldt,

Colombia) and Maria Isabel Gomez (Internacional Center for

Tropical Agriculture, Colombia) for information about the scale

insects in their respective collections.

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APPENDIX I:

miptera: Sternorrhyncha: Coccoidea: Putoidae) and Ceroputo

Sulc (Pseudococcidae) with a comparison to Phenacoccus

Table 1. List of species represented in the Scale Insect Collection at the UNAB entomological museum “Universidad Nacional

Agronomia Bogota” (SIC-UNAB), with information on location, host, catalogue number, material type, number of mounted spec-

imens and liquid vouchers.

SPECIES LOCALITY HOST CAT | HTY | PTY seas LV

(2° adults)

Asterolecaniidae

Planchonia stentae (Brain,1920) Cun EUPHORDIG SE SRG CEU aoa 27 x

rbiaceae)

Russellaspis pustulans (Cockerell, Adl Manilkara zapota (Sapo- 4973 15 x

1892) taceae)

Coccidae

Akermes colombiensis Kondo & Ant, Cal, Cau, | Coffea arabica (Rubia- 3404 AI x

Williams, 2004 Qui ceae)

Akermes sp. Qui Rone gna rea (RUD 2 4771 1 x

ceae)

Coropiasies mosquerai Ben-Dov, Nar Solanum betaceum (So- 493] 10 X

1993 lanaceae)

Coccus hesperidum (Linnaeus, 1758) | Ant Hibiscus sp. (Malvaceae), | 4848 4 x

Coffea arabica (Rubia- 3498

Coccus sp. Cal, Tol ane) 4888 7, x

Coffea arabica, Fara-

Coccus viridis (Green, 1889) An Cal Gane || eg eRe e | eae 33 x

; Ris, Tol (Rubiaceae); Cestrum

nocturnum (Solanaceae)

Hemilecanium guanabana Kondo & Vdc Annona muricata (Anno- 4939 1 xX

Hodgson, 2013 naceae)

Philephedra tuberculosa Nakaha- Gossypium sp. (Malva-

ra & Gill, 1985 Tol Bis 4948 9 Xx

se MVEA LOUEE GIG CHTCCM, Caq Capsicum sp. (Solanaceae) | 4962 10 xX

Protopulvinaria pyriformis (Cocke- Vdc Euphorbiaceae 4958 3 X

rell, 1894)

joner a vireus@ ek ered Boy, Caq Ficus sp. (Moraceae) 4965 34 x

Pulvinaria elongata Newstead, 1917 | Cal, VdC maccani oucincilin oe 1 x

(Poaceae) 1836

Pulvinaria psidii Maskell, 1893 Cun ae deabicgRUpiae 1854 33 x

Schinus molle (Anacarde-

ie Cal, Cun, Qui, | aceae); 7ecoma grandis 873

Saissetia coffeae (Walker, 1852) Ris (BisnbhaccancCaved 354 66 xX

arabica (Rubiaceae)

Bonn zoological Bulletin 69 (2): 165-183 ©ZFMK

Scale insects of the UNAB museum ewe

SPECIES LOCALITY HOST CAT | HTY | PTY Bee

(2° _

Saissetia sp. Ficus andicola (Moraceae)

Tillancoccus koreguaje Caballero & Ca Saccharum officinarum

Ramos, 2017 4 (Poaceae)

Toumeyella coffeae Kondo, 2013 Cau, NdS, VdC oe Beare RUDE

Toumeyella pini King, 1901 Ind (USA) Pinus silvestris (Pinaceae)

Dactylopiidae

Dactylopius sp. Cun Opuntia sp. (Cactaceae) 5537 | x

Aonidiella comperei McKenzie, Tol Citrus aurantifolia (Ruta- 1837 40 x

1937 ceae)

Ayer lis (N d Nerium oleander (Apocy-

1 304). Aroneai ai UNE Walcan Atl, Cau naceae); Citrus limon (Ru-_ | 4845 8 xX

taceae)

Aspidiotus destructor Signoret, 1869 | Ant Musa sp. (Musaceae) 4846 19 x

: ; :

CHO Roranaats dictyospermi (Morg Gar Callistemon sp. (Myrta 4847 7 x

an, 1889) ceae)

oe od eke erred 4849

Diaspis boisduvalii (Signoret, 1869) | Ant, VdC Musa sp. (Musaceae) 4932 20 xX

Duplachionaspis divergens (Green Saccharum officinarum 667

> | Met, R 11 x

1899) nee (Poaceae) 4852

eee ET EHOPINHE(SIEROWS | aii Liriope sp. (Liliaceae) 4861 15 Xx

Hemiberlesia rapax (Comstock, Cun Callistemon sp. (Myrta- 4938 3 x

1881) ceae)

Hemiberlesia sp. Cal CeUeacia cea Rubs: 4573 1

ceae)

Ischnaspis longirostris (Signoret, ae Cocos nucifera (Arecace- 1010 7 Xx

1882) ae) 4940

23 J

LEPIGOSUpHES beckii (Newman, Vdc Gossypium sp. (Malva 4942 ee 4

1869) ceae)

Arbutus unedo (Ericaceae); 1501

Melanaspis sp. Ant, Cun Phormium tenax (Aspho- 13 xX

1502

delaceae)

Odonaspis sp. Ant PODER RUDI 4629 3 x

ceae)

Veitchia merrillii, Cocos

Pseudoparlatoria bennetti (Wil- Vdc nucifera, Blaess aIcUes 1504 32 4

liams, 1969) ra xX Elaeis guineensis

(Arecaceae)

Parlatoria ziziphi (Lucas, 1853) Atl Citrus sp. (Rutaceae) 1885 15

Pinnaspis aspidistrae (Signoret, Tol Annona muricata (Anno- 1863 15

1869) naceae)

Pinnaspis buxi (Bouché, 1851) Ant ae GOMES Cage 3 x

Bonn zoological Bulletin 69 (2): 165-183 ©ZFMK

178

Alejandro Caballero et al.

SPECIES LOCALITY HOST CAT | HTY | PTY sae LV

(2° adults)

Gossypium sp. (Malvace-

Pinnaspis strachani (Cooley, 1898) | Cal, Suc, Tol ae); Saccharum officinar- 25 x

um (Poaceae)

Pseudaonidia trilobitiformis (Green, Atl, Bol Nerium oleander (Apocy- 18 Xx

1896) naceae)

Pseudaulacaspis pentagona (Targio- Passiflora edulis (Passiflo-

NdS 8 x

ni Tozzetti, 1886) raceae)

Pseudoparlatoria parlatorioides ane Yucca elephantipes (Aspa- 5 -

(Comstock, 1883) ? ragaceae)

Pseudoparlatoria suelda Wolff, Ri Persea americana (Lau-

. is - xX

2001 raceae)

nye Gossypium sp. (Malva-

Unaspis citri (Comstock, 1883)? Gossypium sp. (Malva 2 x

ceae)

Eriococcidae

Acanthococcus mokanae Gonzalez, Hibiscus sp. (Malvaceae); x x AI x

Ramos & Caballero, 2019 Capsicum sp. (Solanaceae)

Araucaria heterophylla

Uhleria araucariae (Maskell, 1879) Ce auearlaceae) CESS 16 xX

meria japonica (Cupres-

saceae)

Margarodidae

ian oanbi } Aloe vera (Asphodelace-

urhizococcus colombianus Ja- ;

kubski, 19652 ae); Coffea arabica (Rubi- 2 xX

aceae)

Monophlebidae

Crypticerya abrahami (Newstead, vdc Annona muricata (Anno- , x

1917) naceae)

C Aaneiionsa 1 Mangifera indica (Ana-

ieoae nesitienshs (rietape!: Boy, ASP cardeaceae); Psidium 12 xX

guineense (Myrtaceae)

Crypticerya genistae (Hempel, 1912) | Atl, VdC Arachis pintoi (Fabaceae) 6 x

Crypticerya multicicatrices (Kon- ;

do & Unruh, 2009) 2 Cun Citrus sinensis (Rutaceae) 3 x

Laurencella colombiana Foldi & Ca Persea americana (Lau- g

Watson, 2001 raceae)

Ortheziidae

Insignorthezia insignis (Browne Cnet Mex), ;

1887) ‘ Ant, Cau, Qui, | Coffea arabica (Rubiacea) 52 xX

Ris

Mixorthezia minima Konczné Bene-_ | Chi (Mex); ;

dicty & Kozér, 2004 NdS Coffea arabica (Rubiacea) 6 xX

eviges neotropicalis (Silvestri, Coffea arabica (Rubiacea) 1

Pseudococcidae

Antonina graminis (Maskell, 1897) | Cor, Met Poaceae 4929 25 xX

Chorizococcus caribaeus Wil- Cal Coffea arabica (Rubia- 3495 4

liams & Granara de Willink, 1992 ceae)

Bonn zoological Bulletin 69 (2): 165-183 ©ZFMK

SPECIES

Dysmicoccus boninsis (Kuwana,

1909)

Dysmicoccus brevipes (Cockerell,

1893)

Dysmicoccus caribensis Granara de

Willink, 2009

Dysmicoccus complex joannesi-

ae-neobrevipes

Dysmicoccus complex texensis-neo-

brevipes

Dysmicoccus grassii (Leonardi,

1913)

Dysmicoccus mackenziei Beardsley,

1965

Dysmicoccus neobrevipes Beardsley,

1959

Dysmicoccus perotensis Granara de

Willink, 2009

Dysmicoccus quercicolus (Ferris,

1918)

Dysmicoccus radicis (Green, 1933)

Dysmicoccus sp.

Dysmicoccus sylvarum Williams &

Granara de Willink, 1992

Dysmicoccus texensis (Tinsley,

1900)

Dysmicoccus varius Granara de

Willink, 2009

Ferrisia dasylirii Kaydan & Gullan,

2012"

Ferrisia kondoi Kaydan & Gullan,

2012?

Ferrisia sp.

Ferrisia uzinuri Kaydan & Gullan,

2012

Scale insects of the UNAB museum

Ant, Boy, Cho,

Tol

Ant, Cal, Cau,

NdS, Qui, Ris,

Tol, VdC

Cal, Hui. NdS,

Qui, Tol, VdC

Cau, Tol

Ant, Cal, Cau,

Hui, Qui, Ris,

Tol, VdC

Cau, NdS, Qui,

Tol

Cal, Hui

Ant, Cal, Cau,

Qui, Ris, VdC

Cal, Cau

Qui, Ris

Cun, NdS, Ris

Cal, Cau, Tol

Chi (Mex);

VdC

Ant, Cal, Cau,

NdS, Tol

Ant, Atl, Cor,

Suc, Tol, VdC

Caq, Hui

Cor

Tol

Bonn zoological Bulletin 69 (2): 165-183

Saccharum officinarum

(Poaceae)

Cyperus sp. (Cyperaceae);

Musa acuminata (Musace-

ae); Coffea arabica (Rubi-

aceae);

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Mangifera indica, Spon-

dias sp. (Anacardiaceae);

Amaranthus sp. (Amarant-

haceae); Gossypium sp.

(Malvaceae); Musa sp.

(Musaceae)

Licania tomentosa

(Chrysobalanaceae); Theo-

broma cacao (Malvaceae)

Gossypium sp. (Malva-

ceae)

Coffea arabica (Rubia-

ceae)

830

1390

3500

4622

4853

1391

4643

4854

1398

3785

4934

4626

4777

3787

4933

1394

3786

4570

4769

4624

4572

1398

4628

3787

4627

1397

1496

1393

1395

457]

1860

1834

4936

4776

269

510

233

158

161

179

LOCALITY HOST CAT | HTY | PTY meek

(2° adults)

©ZFMK

180

SPECIES

Ferrisia williamsi Kaydan & Gullan,

2012?

Leptococcus neotropicus (Wil-

liams & Granara de Willink, 1992)

Maconellicoccus hirsutus (Green,

1908)

Macrocepicoccus loranthi Morrison,

1919

Paraputo sp.

Phenacoccus dearnessi King, 1901

Phenacoccus hurdi McKenzie,

196412

Phenacoccus madeirensis Green,

1923

Phenacoccus parvus Morrison, 1924

Phenacoccus sisalanus Granara de

Willink, 2007

Phenacoccus solani Ferris, 1918

Planococcus complex citri-minor

Planococcus halli Ezzat & McCon-

nell, 1956 ?

Planococcus minor (Maskell, 1897)

Planococcus sp.

Pseudococcus calceolariae (Lidgett,

1898)?

Pseudococcus elisae Borchsenius,

1947

Pseudococcus jackbeardsleyi Gim-

pel & Miller, 1996

Alejandro Caballero et al.

LOCALITY HOST CAT | HTY

Ant, Cun, Caq

Caq, Mag

Ant, Atl

VdC

Cau

Ind (USA)

Cun

San

Ant

Ant, Cal, Qui,

Ris, VdC

Ant, Cal, Cau,

Qui, Ris, Tol,

VdC

Cal; Rom

(ITA)

Ant

VdC

Cas

Cun

Ant, Cal, Cau,

NdS Qui, Ris,

Tol, VdC

Ant, Cal, Cau,

Cor, Qui, Ris,

Suc

Bonn zoological Bulletin 69 (2): 165-183

Tecoma sp. (Bignonia-

ceae); Theobroma cacao

(Malvaceae)

Mangifera indica (Anacar-

diaceae); Ficus sp. (Mo-

raceae)

Mangifera indica (Ana-

cardiaceae); Lagerstroe-

mia speciosa (Lythraceae)

é?

Coffea arabica (Rubia-

ceae)

é?

Lantana camara (Verbe-

naceae)

Myrtaceae

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae); Populus sp. (Sali-

caceae)

Lagerstroemia speciosa

(Lythraceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Tecoma sp. (Bignonaceae);

Ficus americana (Mora-

ceae); Callistemon sp.,

Syzygium paniculatum,

(Myrtaceae); Retrophyllum

rospigliosii (Podocarpace-

ae); Prunus persica (Ro-

saceae)

Musa sp. (Musaceae); Cof-

fea arabica (Rubiaceae)

Spondias sp. (Anacardi-

aceae); Gossypium sp.

(Malvaceae); Musa sp.

(Musaceae); Coffea arabi-

ca (Rubiaceae),

4935

1500

4945

4943

4944

4631

1503

1505

4952

4632

1402

3508

1404

3507

3788

4955

4959

1403

4954

1877

1405

SoZ

3513

PTY

SPCM

(2° adults) -

25 x

19 xX

11 xX

15 x

10 xX

8 xX

99 xX

71 x

10 xX

6 xX

l xX

a) x

38 xX

404 xX

53 x

©ZFMK

SPECIES

Pseudococcus landoi (Balachowsky,

1959)

Pseudococcus longispinus (Targioni

Tozzetti, 1867)

Pseudococcus sp.

Saccharicoccus sacchari (Cockerell,

1895)

Spillococcus mamillariae (Bouche,

1844)

Spilococcus pressus Ferris, 1950

Putoidae

Puto barberi (Cockerell, 1895)

Puto antioquensis (Murillo, 1931)

Puto mexicanus (Cockerell, 1893)!

Rhizoecidae

Capitisetella migrans (Green, 1933)?

Coccidella ecuadorina Konczné

Benedicty y Foldi, 2004

Coccidella sp.

Geococcus coffeae Green, 19337

Geococcus johorensis Williams,

1969!

Neochavesia caldasiae (Balachows-

ky, 1957)

Neochavesia eversi (Beardsley,

1970)

Scale insects of the UNAB museum

LOCALITY HOST CAT | HTY | PTY re

(2° adults)

Ant, Cal, Qui,

Ris, Tol, VdC

Cun

Cau, Cor, Tol

Cau, Put, Tol

Cun, Qui

Cau, Ris

Ant, Cal, Cas,

Cau, Hui, Nar,

NdS, Qui, Ris,

San, Tol, VdC

Cau, Cun, Nar

Ant, Cun, Nar

Ant, Cal, Cau,

Cun, Nar, NdS,

Qui, Ris, Tol,

VdC

Ant

Ant, Cal, Ris,

VdC

Cun, Tol

Bonn zoological Bulletin 69 (2): 165-183

Coffea arabica (Rubia-

ceae)

Cyclamen persicum (Pri-

mulaceae)

Ocimum basilicum (Lamia-

ceae); Gossypium sp. (Mal-

vaceae); Coffea arabica

(Rubiaceae)

Saccharum officinarum

(Poaceae)

Mammuiillaria sp. (Cac-

taceae), Coffea arabica

(Rubiaceae)

Coffea arabica (Rubia-

ceae)

Hibiscus sp. (Malvaceae);

Coffea arabica (Rubia-

ceae)

é?

Quercus humboldtii (Fa-

gaceae)

Musa acuminata (Musa-

ceae)

Coffea arabica (Rubia-

ceae)

Bryophyta; Sonchus olera-

ceous, Sonchus sp. (Aster-

aceae); Sida acuta (Malva-

ceae); Oxalis corniculata

(Oxalidaceae), Pennisetum

clandestinum (Poaceae),

Rumex acetosella (Poly-

gonaceae); Coffea arabica

(Rubiaceae)

Galinsoga parviflora (As-

teraceae); Crocosmia sp.

(Iridaceae); Musa acumi-

nata (Musaceae); Poaceae;

Coffeae arabica (Rubia-

ceae),

Musa acuminata (Musa-

ceae)

Coffeae arabica (Rubia-

ceae)

Cyperaceae, Poaceae

3496

1400

1498

3504

4937

1861

1401

3505

831

966

181

©ZFMK

182

SPECIES

Pseudorhizoecus bari Caballero &

Ramos, 2018

Pseudorhizoecus proximus Green,

1933

Rhizoecus americanus (Hambleton,

1946)

Rhizoecus arabicus Hambleton,

1976

Rhizoecus atlanticus (Hamleton,

1946)

Rhizoecus cacticans (Hambleton,

1946) ?

Rhizoecus caladii Green, 1933

Rhizoecus coffeae Laing, 1925

Alejandro Caballero et al.

LOCALITY HOST CAT | HTY

NdS

Chi (MEX)

Ant, Cau, NdS,

Qui, Ris, VdC

Ant, Cal, Cau,

Cun, Qui, Ris,

Tol

Ris

Ant, Boy, Cal,

Cau, Cun, Nar,

Ris, Tol

Ant, Cal, Cun

NdS

Bonn zoological Bulletin 69 (2): 165-183

Coffeae arabica (Rubia-

ceae)

Coffeae arabica (Rubia-

ceae)

Coffeae arabica (Rubia-

ceae)

Musa acuminata (Musa-

ceae); Coffeae arabica

(Rubiaceae)

Coffeae arabica (Rubia-

ceae)

Bryophyta; Oreopanax

floribundus (Araliaceae);

Conyza sp., Chrysanthe-

mum sp., Galinsoga par-

viflora, Hypochaeris sp..,

Sonchus oleraceous,

Taraxacum officinale (As-

teraceae);_7radescantia_

gracilis (Commelinaceae);

Ipomoea sp. (Convol-

vulaceae); Cyperus sp.

(Cyperaceae); 7rifolium

pratense, Trifolium repens

(Fabaceae); Crocosmia sp.

(Iridaceae); Sida acuta

(Malvaceae);_Oxalis_

corniculata, Oxalis sp.

(Oxalidaceae); Bromus sp.,

Cynodon dactylon, Dac-

tylis glomerate, Eleusine

indica, Holcus lanatus,

Lolium sp., Pennisetum

clandestinum (Poaceae);_

Polygonum nepalense,

Rumex acetosella, Rumex

crispus (Polygonaceae);

Coffea arabica, Richardia

scabra (Rubiaceae); Lanta-

na camara (Verbenaceae),

Commelina diffusa (Com-

melinaceae); Cyperus ferax

(Cyperaceae); Musa acu-

minata (Musaceae); Pas-

palum notatum (Poaceae);

Coffea arabica, Sperma-

coce alata (Rubiaceae)

Coffea arabica (Rubia-

ceae)

1807 | X

1875

1326

4576

4637

484

4638

483

3518

1495

4577

4966

1409

PTY

SPCM

(2° adults) :

6 xX

ms x

34 xX

129 xX

220 xX

9 xX

©ZFMK

SPECIES

Rhizoecus colombiensis Ramos &

Caballero, 2016

Rhizoecus compotor Williams &

Granara de Willink, 1992

Rhizoecus cyperalis (Hambleton,

1946)?

Rhizoecus mayanus (Hambleton,

1946)

Rhizoecus neostangei Miller &

McKenzie, 1971

Rhizoecus setosus (Hambleton,

1946)

Rhizoecus spenipes (Hambleton,

1946)

Rhizoecus stangei McKenzie, 1962

Rhizoecus variabilis Hambleton,

1978

Ripersiella andensis (Hambleton,

1946)

Ripersiella campestris Hambleton,

1946

Ripersiella kelloggi Ehrohrn & Co-

ckerell, 1901

Williamsrhizoecus coffeae Cabal-

lero & Ramos, 2018

Scale insects of the UNAB museum

Ant, Cal, Cau,

Nar, Qui, Ris,

Tol, VdC

Ris

Cun

Cal

Chi (MEX)

Cau, Cun, Ris,

Tol

Ant, Cal, Qui,

Ris, Tol

Tol

Ant, Cal, Cun,

Qui, Tol

Ant, Cal, Qui,

Ris, Tol, VdC

Chi (MEX)

Cun

Ant; Chi

(MEX)

Bidens pilosa, Emilia son-

chifolia, Erigeron bonari-

ensis, Galinsoga parviflora

(Asteraceae); Cyperus

ferax (Cyperaceae); Equi-

setum sp. (Equisetaseae);

Crocosmia sp. (Iridaceae);

Cuphea lanceolata (Ly-

thraceae); Musa acuminata

(Musaceae); Eleusine in-

dica, Holcus sp., Panicum

maximum, Paspalum nota-

tum, Pennisetum clandes-

tinum (Poaceae); Plantago

major (Plantaginaceae)

Coffea arabica (Rubia-

ceae)

Thymus vulgaris (Lamiace-

ae); Rosa sp. (Rosaceae)

Coffea arabica (Rubia-

ceae)

Poaceae

Archontophoenix cunning-

hamiana (Arecaceae); Cof-

fea arabica (Rubiaceae)

Coffea arabica (Rubia-

ceae)

Coffea arabica (Rubia-

ceae)

Cuphea lanceolata (Ly-

thraceae); Coffea arabica

(Rubiaceae)

Coffea arabica (Rubia-

ceae)

Poaceae, Coffea arabica

(Rubiaceae)

ves

Coffea arabica (Rubia-

ceae)

678

5019

4578

488

soe

1508

4579

3521

4773

4580

1411

3523

4636

1497

489

4642

4639

494

145

183

LOCALITY HOST CAT | HTY | PTY meek LV

(2° adults)

Abbreviations: Cat. N° (catalogue number); Ant (Antioquia), ASP (The San Andres, Providencia and Santa Catalina Archipielago), Atl (Atlanti-

co), Boy (Boyaca), Cal (Caldas), Caq (Caqueta), Cas (Casanare), Cau (Cauca), Cho (Choco), Cor, (Cordoba), Cun (Cundinamarca), Hui (Huila),

Mag (Magdalena), Met (Meta), Nar (Narifio), NdS (Norte de Santander), Put (Putumayo), Qui (Quindio), Ris (Risaralda), San (Santander) Suc

(Sucre), Tol (Tolima), VdC (Valle del Cauca); ITA (Italy), Rom (Roma); MEX (Mexico), Chi (Chiapas); USA (United States of America), Ind (In-

diana); ? (No information); 'New country record, * New host record (scientific names underline); HTY holotype; PTY paratype; N° SPCM number

of mounting-slide specimens; LV Liquid voucher available.

Bonn zoological Bulletin 69 (2): 165-183

©ZFMK

BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (2): 185-189

2020 - Koppetsch T. et al.

https://do1.org/10.20363/BZB-2020.69.2.185

ISSN 2190-7307

http://www.zoologicalbulletin.de

Scientific note

urn:|sid:zoobank.org:pub:63 BS66ED-656E-4F 86-B173-3C0576114EFF

Crossing the Weber Line:

First record of the Giant Bluetongue Skink Tiliqua gigas (Schneider, 1801)

(Squamata: Scincidae) from Sulawesi, Indonesia

Thore Koppetsch'’, Letha L. Wantania’, Farnis B. Boneka*® & Wolfgang Béhme‘

'4Herpetology Section, Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany

?.3 Department of Fisheries and Marine Science, Universitas Sam Ratulangi, Manado, North Sulawesi, Indonesia

* Corresponding author: Email: t.koppetsch@leibniz-zfmk.de

'urn:lsid:zoobank.org:author:6028DD4F-017F-4A42-A3A2-621993201402

2 urn:lsid:zoobank.org:author:C 1 8E09B6-D0C1-43C3-A64C-12C1B6509F55

2urn:Isid:zoobank.org:author: D7CFFB56-9D50-4A94-BCBD-A06210527235

2urn:Isid:zoobank.org:author: FFAC2972-9F52-404B-BA9C-489C7793FF8D

Abstract. We report for the first time the Giant Bluetongue Skink Tiliqua gigas (Schneider, 1801) from the Indonesian

island of Sulawesi. This find constitutes the westernmost record for the species and represents the first record of Tiliqua

Gray, 1825 from west of the Weber Line and for Wallacea. The possible origin of the specimen found and its taxonomic

status are discussed in a biogeographical context.

Key words. New record, Wallacea, Scincidae, Tiliqua, Sulawesi, Indonesia, biogeography.

INTRODUCTION

Bluetongue skinks of the genus Til/iqua Gray, 1825 are

exceptional large representatives of the Scincidae, one

of the most diverse lizard families with nearly 1700 spe-

cies described (Uetz et al. 2020). They are well-known

for stretching out their bright blue to blackish coloured

tongue towards potential predators when disturbed,

though this behaviour might also serve as intraspecific

signaling (Abramyan et al. 2015).

As popular reptiles that often can be found in herpeto-

culture, bluetongue skinks are of particular interest for

the international pet trade (Yuwono 1998; Iskandar &

Erdelen 2006; Chng et al. 2016), although they can be

easily bred also in captivity (Brauer 1980; Schade 1980;

Lapthorne & Lapthorne 1987; Gassner 2000).

Five of the seven species of Ti/iqua are distributed in

Australia, where they occur in various habitats from arid

to humid climate conditions and at different elevations

(Shea 2000a). Only two species of bluetongue skinks are

found outside of the Australian continent: Tiliqua gigas

(Schneider, 1801) and Tiliqua scincoides (White, 1790)

(Hitz & Hauschild 2000).

For a long time all non-Australian bluetongue skinks

were assigned to 7’ gigas. However, based on studies by

Shea (1992), populations from the Tanimbar and Baber

Islands (eastern Lesser Sundas, Indonesia) were found

Received: 26.02.2020

Accepted: 01.07.2020

to be different from 7’ gigas and were described as T7il-

iqua scincoides chimaerea Shea, 2000, i.e., a subspecies

of a taxon previously known only from Australia (Shea

2000b). In the southeastern region of Irian Jaya (Mer-

auke) bluetongue skinks with a phenotype sharing char-

acteristics of both 7’ gigas and T! scincoides were report-

ed and appear as “Irian Jaya Bluetongue” in the pet trade

(Hitz & Hauschild 2000; Noél 2009).

As shown on Figure 1, 7) gigas has a widespread but

fragmented distribution reaching from the eastern parts of

New Guinea to eastern Indonesia and being spread over

several islands (Shea 2000c).

Within this range three subspecies are distinguished

showing differences in head scalation, body size and co-

louration. Populations found in the Aru and Kei archi-

pelagos (southeastern Maluku Islands, Indonesia) are as-

signed to the endemic subspecies Tiliqua gigas keyensis

Oudemans, 1894 (Shea 2000c; Karin et al. 2018). Tiliqua

g. evanescens Shea, 2000 occurs in southern and eastern

New Guinea and also on islands off the north-eastern and

eastern coast of New Guinea (Admiralty, D’Entrecas-

teaux and Trobriand Islands) (Shea 2000c). This subspe-

cies is geographically separated from the northern sub-

species 7’ g. gigas by the central New Guinea Highlands

and its mountain chains. This biogeographical pattern is

also present in other New Guinean reptiles, see, for ex-

ample, the recent separation of the southern Crocodylus

Corresponding editor: P. Wagner

Published: 15.07.2020

186 Thore Koppetsch et al.

@ Tiliqua gigas gigas

|_| Tiliqua gigas evanescens

|| Tiliqua gigas keyensis

Weber Line

é dante MAL me ia

Fig. 1. Distribution map of Tiliqgua gigas and its subspecies (modified from Shea, 2000c). 7’ g. keyensis is restricted to the Aru

and Kei Islands. 7: g. evanescens is geographically separated from the northern subspecies 7’ g. gigas by the central New Guinea

Highlands and its mountain ranges. The black star denotes the new distribution record for Sulawesi, Indonesia.

halli Murray et al., 2019 from the northern populations of

C. novaeguineae Schmidt, 1928.

Tiliqua g. gigas shows the westernmost distribution of

all non-Australian bluetongue skinks with records from

the Maluku Islands: Ambon, Halmahera (though not re-

corded recently by Setiadi & Hamidy [2006]), Misool,

Morotai, Saparua, Seram and Ternate, but it can be also

found in northern New Guinea and islands along its north-

ern coast (Biak, Doom, Karkar, Seleo, Yapen) (Kopstein

1926; Mys 1988; Shea 1982, 1992, 2000c).

Some old mentions of bluetongue skinks from Java and

Sumatra (Boulenger 1887; Dumeéril & Bibron 1839; Wer-

ner 1910) remained unconfirmed and were most likely

caused by misidentification of collection data or provid-

ing the location of the port of shipment (Shea 2000a).

Fig. 2. Photography of the living specimen of Tiliqua gigas gi-

gas found near Airmadidi in Northern Sulawesi, Indonesia.

Bonn zoological Bulletin 69 (2): 185-189

Apart from those early and doubtful locality data, all

reliable and confirmed records of Tiliqua are located east

of the Weber line (Shea 2000a). Here we report the first

record of 7: g. gigas from Sulawesi, Indonesia (Fig. 2).

MATERIAL AND METHODS

A large scincid lizard was discovered on 6 August 2019

near Airmadidi, Minahasa Utara, North Sulawesi, Indo-

nesia (Fig. 1), where it was kept alive by locals. Airmadidi

is a village located southeast and in about 15 kilometers

distance to Manado, as well as in proximity to the highest

volcano of Sulawesi, Mount Klabat, raising 1,995 meters

a.s.1.. This specimen of 7: gigas had been caught in some

distance to the village located nearby in the undergrowth

of secondary rainforest at around 215 meters a.s.l.. The

habitat was characterized by a dense and flourishing

ground vegetation, mainly consisting of creepers (Fig. 3).

No streams or pools of water can be found directly near

to the collection site. Since bluetongue skinks are partial-

ly under a high collection pressure for purposes of pet

trade and cases of intense suchlike collection or extirpa-

tion had been reported from type or first record localities,

for instance in the eublepharid gecko Goniurosaurus luii

Grismer, Viets & Boyle, 1999 (Lindenmayer & Scheele

2017), we refrain from providing detailed location data,

like geographical coordinates. Identification and record

are based on the live specimen that was returned to be

kept alive in the village after examination.

©ZFMK

First record of Tiliqua gigas for Sulawesi 187

ie od, f ae Ps bis ns rk

oL < 4 : in ®: ee

RESULTS AND DISCUSSION

The specimen found can be easily identified as a member

of the bluetongue skinks Ti/iqua due to its characteristic

tongue and body colouration, a large body size and com-

pact body shape (Fig. 4). Identification as T’ gigas gigas

could be confirmed by the presence of black, unspotted

or slightly spotted limbs, an extensive black-striped and

deep orange spotted pattern on the ventral side and black-

ish edged head scales based on the diagnostic characters

presented in Hauschild & Hitz (2000) and Shea (2000c).

Moreover, the basic dorsal colouration of the specimen

found is dark-reddish brown with ten narrow black trans-

verse bands on the trunk and 14 broad black bands on

the tail. It shows an unpatterned and bright orange-co-

loured throat. In addition, the snout-vent length is about

290 mm, the tail length is 228 mm (measured in the field

by one of the authors).

Habitus and size of the specimen resembles specimens

from the northern Maluku Islands (Ternate, Halmahera,

Misool). Even though this subspecies shows a high de-

gree of variability within in its geographical range (Shea

1992), individuals from the northern Maluku Islands

normally have a snout-vent length of more than 270 mm

and more darkish colouration (Shea 2000c). In addition,

Bonn zoological Bulletin 69 (2): 185-189

Fig. 3. Habitat in which TJiliqua gigas was found in Northern Sulawesi.

a dark-striped belly pattern was recorded for most speci-

mens from Halmahera (Shea 2000c).

Bluetongue skinks of the genus Tiliqua have never

been recorded from Sulawesi before (Iskandar & Tjan

1996; Gillespie et al. 2005; Wanger et al. 2011; Koch

2012). This new record is situated about 250 km distance

west of the distribution known so far and expands the

distribution range of 7’ gigas from eastern New Guinea

to Sulawesi within the Wallacea to about 3.000 km in to-

tal. Bluetongue skinks are normally well-known to local

people as they are hunted for consumption (Wolter 1980;

Shea 2000c). In New Guinea specimens of Tiliqua are

also known under the local name ‘ular panana’ (‘ular’ =

snake; see Kopstein 1926), indicating that they are often

mistaken for a snake and thought to by venomous, due to

their cylindrical, short-legged appearance and their con-

spicuous defensive display. However, bluetongue skinks

were unknown to the local people at the location where

our specimen was found. Therefore, an unintentional in-

troduction by humans has to be taken into account and

cannot be ruled out.

The geographically nearest distance to places, where

7. gigas is recorded from, are in the northern Maluku Is-

lands (Ternate and Halmahera). Nevertheless, these is-

lands are still more than 250 km away from our northern

©ZFMK

188 Thore Koppetsch et al.

Fig. 4. Defensive posture of Tiliqua gigas from Northern Su-

lawesi, Indonesia. Note the blueish tongue stretched out to-

wards potential predators.

Sulawesi site. This gap implies a crossing of the biogeo-

graphically important Weber Line running east of Su-

lawesi and separating the Oriental and Oceanian faunas

(Weber 1902; Lohman et al. 2011; Holt et al. 2013; Vil-

hena & Antonelli 2015).

An unintentional introduction by humans via transport

in freight and cargo is common in different small-sized

skink species (Kohler et al. 1997; Chapple et al. 2015).

That is, however, unlikely at least for adult individuals

of such a large and conspicuous skink species like Ti/i-

qua gigas. Of course this cannot be ruled out completely,

since also lizards of larger size have been introduced to

islands out of their distribution range, for example, Aga-

ma agama (Linnaeus, 1758) on islands of Macaronesia,

in the Mediterranean Sea or in the Indian Ocean (Wagner

et al., 2012). Finally, pet trade for herpetoculture is not

widespread especially in rural areas of Sulawesi, since

larger reptiles like monitor lizards are caught and kept for

consumption. Consequently, escaped specimens from the

pet trade are improbable in this case.

An undetected population of 7. gigas in northern Su-

lawesi cannot be excluded, since also during intensive

herpetological field surveys bluetongue skinks were not

observed, even from islands they had been recorded from

previously (Setiadi & Hamidy 2006; Karin et al. 2018).

Especially skinks are known for their dispersal poten-

tial even to islands located away from the coast line of

the main land (Adler et al. 1995). Not only small and

Bonn zoological Bulletin 69 (2): 185-189

inconspicuous lizard species can remain undiscovered

for a long time, as shown by recent discoveries of sev-

eral species of monitor lizards from Indonesian and New

Guinean Islands (Ziegler et al. 2007; Weijola et al. 2016;

Bohme et al. 2019). Therefore, even such relatively large

lizards, like Tiliqgua, seem to show some potential for

new discoveries and unanswered questions like the blue-

tongue skinks from Irian Jaya (Hitz & Hauschild 2000;

Noél 2009) or the subspecies of 7’ gigas described by

Shea (2000b, c).

Acknowledgements. The authors thank Dr. Robert Hitz (Thal,

Switzerland) for providing comparative photo material of cap-

tive-bred 7? gigas specimens, and Morris Flecks (ZFMK) for

assisting in preparing a distribution map. TK is grateful to Dr.

Fabian Herder (ZFMK) for the possibility to participate in field

work on Sulawesi and to the German Academic Scholarship

Foundation for providing a travel grant.

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©ZFMK

BHL

Blank Page Digitally Inserted

FORSCHUNGS

AQ Z5ENiG Bonn zoological Bulletin 69 (2): 191-223 ISSN 2190-7307

2020 - Klein B. et al. http://www.zoologicalbulletin.de

https://do1.org/10.20363/BZB-2020.69.2.191

Research article

urn:|sid:zoobank.org:pub:607B577 1-A379-42B6-A9A7-BSDS5A2AB27FB

Larval development and morphology of six Neotropical poison-dart frogs

of the genus Ranitomeya (Anura: Dendrobatidae)

based on captive-raised specimens

Benjamin Klein', Ruth Anastasia Regnet”, Markus Krings’ & Dennis Rédder*”

!.2.3.4Zoologisches Forschungsmuseum Alexander Koenig, Leibniz Institute for Animal Biodiversity,

Adenauerallee 160,D-53113 Bonn, Germany

4 Programa de Pos Graduacdo em Zoologia, Universidade Estadual de Santa Cruz - UESC, Rodovia Jorge Amado, Km 16,

45662-900 Salobrinho, Ilhéus, Bahia, Brazil

“Corresponding author: Email: d.roedder@leibniz-zfmk.de

'urn:|lsid:zoobank.org:author:5F4659E8-4E44-4F22-A 1 D4-7BBEF1D3ES5F1

urn:|sid:zoobank.org:author: 1 B245FFB-03C5-4386-A06E-C149C8A40AC6

3urn:lsid:zoobank.org:author:D78A5661-FC8 1-42BA-B9E4-948E2 1 E2D6BC

*urn:Isid:zoobank.org:author: C7 DOE2AF-2147-43FA-A89A-D770AAEA150E

Abstract. Larval development is a crucial step during the ontogeny of amphibians, concomitantly it is the most sensitive

life phase in this group. Due to the complex morphological, physiological and anatomical changes, in addition to their

susceptibility to the environment changes, this phase is known as one of the most critical period of development as well

as an obstacle in ex-situ breeding programs. Tadpole growth rates can be used to predict the effects of biotic interactions,

as well as to predict the survival rate on environmental changes. The assessment of the mortality rate during this phase

can be performed using a non-invasive image-based tool, programmed on the open source statistical platform R, SAISAQ

(semi-automatic quantification of image-based surface area). It allows analyzing semi-automatically a sequence of stan-

dardized image files in order to quantify growth rates. However, the current literature lacks estimates of the larval growth

rates for the most species of amphibians, which 1s also true for species of the genus Ranitomeya Bauer, 1986. Herein,

we present the data of the complete larval development of Ranitomeya amazonica (Schulte, 1999), R. benedicta Brown,

Twomey, Pepper & Sanchez-Rodriguez, 2008, R. imitator (Schulte, 1986), R. reticulata (Boulenger, 1884), R. sirensis

(Aichinger, 1991) and R. vanzolinii (Myers, 1982), assisted by photographs, drawings and tables with detailed information

about the metamorphosis. In addition, we provide a new larval description for R. benedicta. The results presented here

also provide new data of the larval development and morphology for the target species, based on a sample series for each

species. With this information, we want to contribute to a better understanding of the group and provide important data to

help solve the systematic relationships puzzle. Providing also a baseline to improve further research on captive breeding,

our results may have important implications for conservation breeding programs.

Keywords. Amazon, conservation, ex-situ, Ranitomeya benedicta, SAISAQ, tadpole.

Resumen. El desarrollo larvario es un periodo crucial en la ontogenia de los anfibios y al mismo tiempo la fase mas sen-

sible de la vida de este grupo. Debido a los complejos cambios morfoldgicos, fisioldgicos y anatomicos, ademas de la sus-

ceptibilidad a los cambios ambientales, esta fase es conocida como uno de los periodos mas criticos de desarrollo asi como

un obstaculo en los programas de reproduccion ex-situ. Las tasas de crecimiento de los renacuajos pueden ser empleadas

para predecir los efectos de las interacciones bidticas, asi como predecir la tasa de supervivencia de los anfibios a los

cambios ambientales. Se puede realizar la evaluacion de la tasa de mortalidad de los renacuajos mediante una herramienta

no invasiva basada en imagenes, programada en la plataforma estadistica de cédigo abierto R, SAISAQ (Semi-Automatic

Surface Image-Based Quantification). Por medio de este, es posible obtener una secuencia semi automatica de archivos de

imagen estandarizados, con el fin de evaluar el crecimiento en relacion al tiempo. Sin embargo, la literatura actual presenta

una carencia de estimaciones de la tasa de crecimiento basadas en imagenes del desarrollo larvario para la mayoria de las

especies de anfibios, algo igualmente observado para las especies del género Ranitomeya Bauer, 1986. Asi, presentamos

aqui los datos del desarrollo larvario completo de Ranitomeya amazonica (Schulte, 1999), R. benedicta Brown, Twomey,

Pepper & Sanchez-Rodriguez, 2008, R. imitator (Schulte, 1986), R. reticulata (Boulenger, 1884), R. sirensis (Aichinger,

1991) y R. vanzolinii (Myers, 1982), asistidos por fotografias, ilustraciones y tablas con informacion detallada acerca de

la metamorfosis. Ademas proporcionamos una descripcion larvaria inédita para R. benedicta. Los resultados aqui presen-

tados también proporcionan nuevos datos acerca de la morfologia y el desarrollo larvario de las especies aqui estudiadas,

basados en una serie de muestras para cada especie. Estas informaciones contribuyen para una mejor comprension del

grupo y proporcionan datos importantes para ayudar a resolver el tan complejo rompecabezas de las relaciones sistemati-

cas. Ademas promueven una base de conocimiento para futuras investigaciones sobre la cria en cautividad de anfibios, una

importante herramienta en los programas de cria en cautividad para la conservacion de especies de anfibios amenazadas.

Palabras clave. Amazonia, cria en cautividad, ex situ, renacuajo, Ranitomeya benedicta, SAISAQ.

Received: 09.04.2018 Corresponding editor: W. Bohme

Accepted: 20.08.2020 Published: 31.08.2020

192 Benjamin Klein et al.

INTRODUCTION

Anurans currently include more than 7,000 described

species (Frost 2020) and are by far the most species-rich

and evolutionary successful group among the extant am-

phibians. This evolutionary success is promoted by their

wide diversity of survival and reproductive strategies,

as well as their life histories (Duellman & Trueb 1986;

Wells 2007). The huge variety of functional types, in-

cluding terrestrial, aquatic, fossorial and arboreal forms

and their morphological adaptations allowed anurans to

occupy a wide array of terrestrial and fresh-water niches

(Duellman & Trueb 1986; Wells 2007). However, due to

their thin and permeable skin as well as their ectothermy,

they are highly susceptible to humidity and temperature

variations, the most important abiotic factors within their

habitats (Wells 2007).

Poison-dart frogs belong to the superfamily Dendroba-

toidea Cope, 1865 and include about 328 known species

divided into the families Aromobatidae and Dendrobati-

dae (Grant et al. 2006; Brown et al. 2011; Frost 2020).

All members have a small to medium size of 2-6 cm

snout-vent length (SVL) in combination with a high-

ly complex social and reproductive behavior (Lotters

et al. 2007; Brown et al. 2011). The genus Ranitomeya

Bauer, 1986, which is placed within the family Dendro-

batidae, consists of 16 species arranged into four species

groups, namely the R. defleri Twomey & Brown, 2009,

R. reticulata (Boulenger, 1884), R. vanzolinii (Myers,

1982) and R. variabilis (Zimmermann & Zimmermann,

1988) groups (Brown et al. 2011). Species of that genus

are characterized by their diminutive size with SVL less

than 21 mm, their bright aposematic coloration and an

almost smooth to slightly granular dorsal surface (Daly

et al. 1987; Vences et al. 2003; Brown et al. 2011). Fur-

thermore, the first finger is reduced and shorter than the

second, which is the largest of all four fingers (Brown

et al. 2011).

In 2011, Brown et al. published a revision of the genus

Ranitomeya, which represents the actual and widely ac-

cepted classification for this group (e.g., Sanchez 2013;

Vargas-Salinas et al. 2014; Krings et al. 2017). Within

their study, systematic arrangements and the history of

that genus are explained, based on molecular phylogenet-

ics in combination with adult and larval morphology. For

understanding the systematic and phylogenetic relation-

ships, it is a general consensus that morphological data

is an indispensable tool. Regarding taxonomic and phy-

logenetical purposes, we cannot neglect the knowledge

about the morphology of the amphibian larval phase (1.e.,

tadpoles), where many of the descriptions of the larval

stage are quite incomplete, based on a single sample or

data are totally absent.

For the genus Ranitomeya, many of the tadpole de-

scriptions are based on back riding tadpoles during the

transport by the adults to water bodies (Sanchez 2013).

Bonn zoological Bulletin 69 (2): 191-223

At this stage of development, the tadpoles often lack ful-

ly developed tooth rows or other specific characteristic

traits of the species (Brown et al. 2011). Furthermore,

clutches of Ranitomeya species are very small, which

makes it difficult to obtain a larger number of specimens

at a time, and tadpoles that have already been carried by

adults to a water site where they will develop are hard to

find. One way to locate tadpoles at this stage 1s observing

the adults, which are shy and therefore hard to discover

(Sanchez 2013). In a captive breeding framework, higher

numbers of tadpoles can be analyzed across a long time

span making it possible to document the complete devel-

opment. Furthermore, as conservation breeding becomes

more and more important detailed information on devel-

opmental rates can be very helpful for ex-situ breeding

programs. By optimizing husbandry conditions, potential

effects of artificial nutrition and artificial environmental

conditions can be minimized, although they may oc-

cur. Thus, results obtained from captive bred specimens

should be ideally complemented and confirmed by data

collected in the field.

The aim of this study is to provide, as accurately as

possible, data concerning the complete larval morpholo-

gy and development of the tadpoles of Ranitomeya am-

azonica (Schulte, 1999), R. benedicta Brown, Twomey,

Pepper & Rodriguez, 2008, R. imitator (Schulte, 1986),

R. reticulata, R. sirensis (Aichinger, 1991) and R. van-

zolinii based on specimens obtained from captive breed-

ing. In the study by Brown et al. (2011), descriptions of

R. amazonica tadpoles are presented based on a tadpole

in Gosner’s stage 29, as well as those of R. imitator based

on a tadpole in stage 26, of R. reticulata based on a tad-

pole in stage 30 and of R. vanzolinii based on a tadpole

in stage 38. The tadpole description of R. benedicta in-

cludes only a mouthpart description which was presented

by Brown et al. (2008). As stated by the authors the sam-

ple ended up being ruined by the fixation process, mak-

ing it impossible to describe the tadpole (Brown et al.

2008). The tadpole of R. sirensis from the stages 25—36

was described in detail by May et al. (2008a) under the

name Ranitomeya biolat (Morales, 1992) (c.f. Brown

et al. 2011) which is considered to be a synonym of R. si-

rensis (Frost 2020).

We present in this study the first larval description of

R. benedicta and provide image-based growth rate esti-

mates of larval development for all target species, based

on the SAISAQ (Semi Automatic Image based Surface

Area Quantification, Kurth et al. 2014) tool. In addition,

all data presented herein will contribute to fill knowledge

gaps of the amphibian larval development, which is also

useful for ex-situ breeding programs, in response to the

biodiversity crisis, which requires a moral and ethical

obligation for proactive interventionist conservation ac-

tions to assist species recovery and reduce the population

decline.

©ZFMK

Larval characterization of six poison-dart frogs 193

MATERIALS AND METHODS

Captive Management and Breeding

Adult specimens of the species R. amazonica, R. bene-

dicta, R. imitator, R. reticulata, R. sirensis and R. vanzo-

linii were acquired from pet trade and kept in customized

terraria at the Zoologisches Forschungsmuseum Alex-

ander Koenig (ZFMK) in Bonn, Germany. According to

the venders the specimens were captive bread as F, from

specimens exported from the countries of origin. Correct

taxonomy was confirmed by comparing the external mor-

phology with the respective original descriptions.

For the course of the study, groups of five specimens

of Ranitomeya amazonica, two specimens of R. imitator,

two specimens of R. reticulata, four specimens of R. si-

rensis and four specimens of R. vanzolinii were kept in

terraria of 40x50x40 cm, while three specimens of R. ben-

edicta, four specimens of R. imitator and four specimens

of R. vanzolinii were kept in terraria of 60x50x50 cm

size. Ranitomeya individuals did not have contact with

other individuals of the other species of the genus, also

kept in terrariums, thus avoiding hybridization between

species.

Each terrarium was equipped on the base with a filter

mat which was covered with local leaf litter. The rear and

one of the sides were covered with cork tile (Lucky Rep-

tile®, Schwarzkorkriickwande). Artificial lighting was

promoted with a LED light (Solar Stinger, 1100 Sunstrip

Dimmable Driver, 25W) and daily, artificial daylight was

provided from 8 a.m. to 8 p.m. In addition, the terrartum

had a bottom irrigation system, a small body of standing

water with a drain in a sieve form, located in one of the

front corners of the terrarium and a misting system. The

misting system was activating three times a day for 120

seconds, divided into twelve alternating intervals of ten

seconds spraying, followed by ten seconds pause. Aver-

age air and water temperature fluctuated between 22 and

26eC:

In order to ensure a finely storied vertical structure

and provide opportunities to refuge and breeding sites,

the terraria were heavily planted with Ficus pumila L.,

Scindapsus sp. as also Neoregelia sp. “fireball bromeli-

ad” which provides a natural phytotelm for the anurans,

important resource for laying the eggs. Additionally,

the micro ambient was equipped with stones, roots and

film containers (35mm) thus providing additional arti-

ficial phytotelms. The amphibians were fed with a diet

of Drosophila melanogaster Meigen, 1830 or collembo-

lans, every two to three days, and the food was enriched

with vitamins and minerals (Herpetal® Mineral + Vitamin

D3, Korvimin ZVT + Reptil).

Detected clutches were removed with aid of water and

pipettes and placed into petri dishes. To ensure stable

conditions, the clutches were transferred into an envi-

ronmental test chamber (MLR-352H-PE, Panasonic Bio-

Bonn zoological Bulletin 69 (2): 191-223

medical Sales Europe BV, Netherlands), which was set to

a humidity of 80%, a temperature of 24 °C and a twelve

hour photoperiod from 8 a.m. — 8 p.m. Every second day

all eggs were wetted, except the clutches of R. amazonica

which were completely covered with enriched pure wa-

ter, attending the reproductive behavior of the species, as

e.g. mentioned in Poelman & Dicke (2007) and Poelman

éFal(2013).

After hatching, the larvae were kept separated with-

in small translucent plastic containers (10x 10x10 cm),

which were filled with enriched pure water and several

oak leaves as well as a stem of Ceratophyllum demer-

sum. Each container was placed into the environmental

test chamber and got a specific identification number.

Every two to three days, two thirds of the water were ex-

changed, in order to preserve the favorable environment

for the tadpole. The larvae were fed with a finely ground

ration of several types of algae and fish food ad Jibitum,

which is different from the natural food. These species

are known for their oophageal and predatory behavior in

the natural environment (Lotters 2007; Poelman & Dicke

2007). In addition, specimens could graze on biofilm and

algae that naturally grew within their container.

When the forelimbs emerged, a small piece of cork

tile was placed on the water surface in order to provide

a small “land area”. During the latest steps of metamor-

phosis, when the tail was resorbed, the froglets were

transferred to a new container with a huge “land area”,

covered with oak leafs, as well as a small water body

(18x13x6 cm). The container was sealed with a perfo-

rated cover to ensure air exchange. From this moment,

the froglets were fed with a diet of Drosophila melano-

gaster and collembolans.

The climate at each known location of the six different

species, as defined by Brown et al. (2011), was obtained

using ArcGIS (Environmental Systems Resource Insti-

tute, ArcGIS 10.2.2, Redlands, California). In order to do

so, the longitudinal and latitudinal values of the locations

were received through georeferencing of available dis-

tribution maps. On the one hand, these coordinates were

used to generate a new map which contains the distribu-

tion areas of the study organisms (Fig. 1). Expert range

maps provided by IUCN were randomly sampled every

10 km? to estimate annual mean, and monthly minimum

and maximum temperatures within the geographic range

of each species. Modern climate data with a spatial res-

olution of 30 arc sec was obtained from the free global

online database CHELSA (Karger et al. 2017a, b).

Measurements

During their development, the growth rate of the active

and mobile tadpoles was documented using a photo cam-

era (EOS 600D, Canon® Deutschland GMBH, Krefeld,

Germany), which was mounted on a table-top tripod in

a fixed distance to the object. Photographs were taken

©ZFMK

194 Benjamin Klein et al.

Elevation [m]

[| -431-225 [| 494-834

[| 225-494 [| 834-1,747

[J 1,747-3,307

| | 3,307-8,233

@ R. amazonica

R. reticulata

@ R.benedicta @ R. imitator e Locality record

®@ R. sirensis @ R. vanzolinii Mf Type locality

Fig. 1. Known distribution of Ranitomeya amazonica (green), R. benedicta (light blue), R. imitator (red), R. reticulata (yellow),

R. sirensis (blue) and R. vanzolinii (orange). Darker shades of gray indicate higher elevations. The inset map displays the distribu-

tion of all six compared species, which are shown in the upper right corner of that figure with the corresponding color code.

three times a week, on alternate days. For this purpose,

the larvae were placed into a translucent petri dish on top

of a light source (CL 6000 LED, Carl Zeiss° Microscopy

GMBH, Jena, Germany) which was modified by an ala-

baster glass. Thus, the light was homogenously distrib-

uted and therefore ensured a high contrast between the

object and the background.

In all photography sessions, first a standard picture was

taken to calibrate an image analysis software programmed

in the open source statistics platform R (R Development

Bonn zoological Bulletin 69 (2): 191-223

Core Team, 2014), which allows a semiautomatic proces-

sion of standardized image files (SAISAQ, Kurth et al.

2014). Subsequently the settings and distances were kept

constant and all tadpoles were photographed. The soft-

ware measured the surface area of each tadpole, which is

strongly correlated to the body mass. Therefore, a picture

series of the same individual documenting its develop-

ment leads to a graph which represents the growth rate.

Every tadpole was photographed with four different set-

tings, ranging in light intensity and different sensitivities

©ZFMK

Larval characterization of six poison-dart frogs 195

of the camera (Appendix I) which allows observing the

tadpole in more details and assisting the software to set

the threshold between the object and the background

more efficiently. Dorsal and ventral high-resolution pic-

tures, of each tadpole, were created with a special camera

setup (Canon EOS 7D mounted on a P-51 Cam-Lift, Dun

Inc., Virginia, USA), which perform automatically mul-

tiple pictures in different depths and stacks the photos in

order to create a final clear image.

Length based measurements were taken to the nearest

of 0.1 mm with a stereomicroscope and its integrated

eyepiece (Stemi 2000 C, Carl Zeiss° Microscopy GmbH,

Jena, Germany) or ImageJ (National Institutes of Health,

ImageJ 1.42q, Bethesda, Maryland). The morphological

terminology, characters and measurements are deter-

mined following McDiarmid & Altig (1999) (Fig. 2) ex-

tended by larval measurements from Lavilla & Scrocchi

(1986) as cited in Miyares-Urrutia (1998).

Characters and measurements following McDiarmid &

Altig (1999; Fig. 2) are: first anterior tooth row (A1); sec-

ond anterior tooth row (A2); medial gap in first anterior

tooth row (A1-GAP); anterior (upper) labium (AL); body

length, measured from the tip of the snout to the junc-

tion of the posterior body wall with the axis of the tail

myotomes (BL); internarial distance, measured between

centers of narial apertures (IND); interorbital distance,

measured between centers of pupils OD); lower jaw

sheath (LJ); lateral process of upper jaw sheath (LP);

labial tooth row formula (LTRF); mouth (M); marginal

papillae (MP); maximum tail height (MTH); oral disc

(OD); posterior (lower) labium (PL); first posterior tooth

row (P1); second posterior tooth row (P2); third posterior

tooth row (P3); medial gap in first posterior tooth row

(P1-GAP); tail length (TAL); tail muscle height at base

(TMH), tail muscle width at base (TMW)); total length

(TL); submarginal papillae (SM); upper jaw sheath (UJ).

Characters and measurements following Lavilla &

Scrocchi (1986) as cited in Mijares-Urrutia (1998) are:

body width at eye level (BWE); body width at nostril

level (BWN); horizontal eye diameter (ED); eye nostril

distance (END); maximum body height (MBH); maxi-

mum body width (MBW); oral disc width (ODW); ros-

tro-eye distance, from tip of snout to the center of the eye

in lateral view (RED); rostro-nasal distance, from tip of

snout to the center of the nostril in lateral view (RND);

rostro-spiracle distance, from tip of snout to center of the

spiracle in lateral view (RSD).

Besides that, staging of the development process took

place according to Gosner (1960), voucher specimens

were euthanized using a saturated solution of Chlorobu-

tanol, subsequently preserved in 6% formalin, and after

an ascending alcohol series, preserved in 70% ethanol at

the herpetological section of ZFMK. The voucher num-

bers of each tadpole are provided in the results section.

A brief description of the natural history of each species

covered in this study can be found in Appendix II.

Bonn zoological Bulletin 69 (2): 191-223

RESULTS

Species Accounts

Ranitomeya amazonica (Schulte, 1999)

Breeding behavior in captivity. The breeding pairs,

among the five specimens of R. amazonica, placed the

clutches of four to six anthracite eggs in the bromeliad

phytotelm. While those egg depositions had no clear fre-

quency, later depositions in a water filled film container

occurred every two to five days. Thereby, the clutches

were placed directly underneath the water surface of the

vertically orientated container, which was placed on the

ground next to a large stone. Moreover, at one day a sin-

gle tadpole at stage 25 was found at the ground of the

container, beneath a newly produced clutch.

Larval morphology. The description of the tadpole is

based on one specimen at stage 41 (ZFMK 97374). Fur-

ther voucher specimens are ZFMK 97357, 97362, 97366,

97370-97373. According to McDiarmid & Altig (1999),

R. amazonica tadpoles belong to the exotrophic, lentic,

benthic, arboreal larval type. All measurements that were

used to calculate the following proportions and its com-

parison with the other species of this study, can be found

in Appendix III.

Dorsal view: Body shape is oval and moderately elon-

gated (MBW/BL=0.75). The snout is short and mod-

erately pointed (RED/BL=0.23, BWN/BWE=0.56),

nares are small and elliptical, positioned dorsally and

orientated laterally. Nares are situated closer to snout

than to eyes (RND/RED=0.43). Eyes are large (ED/

BL=0.12), positioned dorsally and orientated laterally.

Internarial distance is smaller than interorbital distance

(IND/IOD =0.52). Single, sinistral spiracle is not visible

in dorsal view.

Lateral view: Body is depressed (MBH/MBW =0.59),

snout is rounded. The spiracle is positioned below the

longitudinal axis, at the second half of the body (RSD/

BL=0.64), the inner wall is free from the body, open-

ing is round and the spiracle tube is short. The maximum

body height is situated between the eyes and the tail. The

tail is long and narrowly rounded (TAL/BL=1.95, TAL/

TL=0.66). The musculature is well developed (TMH/

MTH=0.58, TMW/MBW=0.33). The “V-shaped myo-

septa are visible along the whole length of the tail, par-

ticularly at the first half. Upper fin originates posterior

to the tail-body junction and the margin of the lower fin.

Upper fin is slightly higher than the lower fin. Ventral

tube is dextral, emergence from abdomen sagittal, open-

ing 1s rounded. Hindlimbs are fully developed. Oral ap-

paratus is visible in lateral view.

Oral apparatus: Oral disc is elliptical, positioned ven-

trally and covers nearly one third of the body width

(ODW/MBW =0.27), emarginated. Marginal, ensiform,

©ZFMK

196 Benjamin Klein et al.

lOD TMW

C UJ A1-GAP

oa i) Sy arta Sp My, +; A2

"es ay SP

Ew, Ji Ree) LLLLZ/ MIE

\ My) i ! as

mY’ (F . My Gir rs § wee /

ete ZT, grit sil P1

PL f 2 : mr MITT wai! mill |

of eh. : SUA pe P2

LP ee ome

P1-GAP

Fig. 2. Landmarks and measurements of a tadpole body and definitions of the oral apparatus. A. Lateral view. B. Dorsal view. C. Oral

apparatus. Abbreviations A-B: BL=body length; TAL=tail length; TL=total length; TMH=tail muscle height, MTH=maximum

tail height; IND=internarial distance; IOD=interorbital distance; TMW =tail muscle width. The dotted line indicates the accurate

progression of the measurement which represents the body length. Abbreviations C: Al =first anterior tooth row; A2=second ante-

rior tooth row; A2-GAP=medial gap in second anterior tooth row; AL=anterior (upper) labium; LJ=lower jaw sheath; LP=lateral

process of upper jaw sheath; M=mouth; MP=marginal papillae; OD=oral disc; PL=posterior (lower) labium; P1 =first posterior

tooth row; P2=second posterior tooth row; P3=third posterior tooth row; SM=submarginal papillae; UJ=upper jaw sheath.

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs 197

Table 1. Ranitomeya amazonica (n=5) larvae morphometric measurements at the stages 26—41. Not all stages are represent-

ed; all measurements are given in [mm]. Abbreviations: BL=body length; BWE=body width at eye level; BWN=body with at

nostril level; ED=horizontal eye diameter, END=eye nostril distance; INFD=internarial distance; IOD=interorbital distance;

MBH=maximum body height; MBW=maximum body width, MTH=maximum tail height; ODW=oral disc width; TAL=tail

length; TMH=tail muscle height at base; TMW=tail muscle width at base; TL=total length; RED=rostro-eye distance, from tip

of snout to the center of the eye in lateral view; RND=rostro-nasal distance, from tip of snout to the center of the nostril in lateral

view; RSD=rostro-spiracle distance.

Stage 26 31 34 38 41

BL SID 12 8.33 8.33 9.38

BWE 3.9 4.24 4.70 5.00 res

BWN 243 2,73 3.03 He fe: 3.14

ED 0.45 0.61 0.76 0.83 L138

END 0.91 | b52 esp 1.23

IND 1.14 1.36 V52 1.59 Mede

IOD 1.97 2.42 213 3.08 3.00

MBH 2.05 3.03 3.18 3.18 4.14

MBW 3.94 Sls 5.76 maa 7.00

MTH 1.97 3.00 3.33 3403 oll

ODW 1.14 L79 1:97 1 OF 1.86

TAL 10.30 13:79 15.13 15.15 18.29

TMH 0.91 1.67 1.82 1.74 2.14

TMW 1.06 1.67 107 Dalz 229

TL 15.45 20791 23.48 23.48 24.64

RED 1.52 Le 2.42 2.42 pa

RND 0.61 0.76 0.98 0.98 0.92

RSD 3.26 4.85 5.68 5.76 6.00

MBW/BL 0.76 0.72 0.69 0.71 0.75

RED/BL 0.29 0.28 0.29 0.29 0.23

ED/BL 0.09 0.09 0.09 0.10 0.12

RND/RED 0.40 0.38 0.41 0.41 0.43

IND/IOD 0.58 0.56 0.56 0.52 0.52

TMW/MBW 0.27 0.32 0.34 0.36 0.33

MBH/MBW 0.52 O39 0.55 0.54 0.59

TAL/BL 2.00 1.94 1.82 1.82 F95

TAL/TL 0.67 0.66 0.65 0.65 0.66

TMH/MTH 0.46 0.56 0.55 0.58 0.58

TMW/MBW 0.27 0.32 0.34 0.36 0.33

ODW/MBW 0.29 0.35 0.34 0.33 0.27

RSD/BL 0.63 0.68 0.68 0.69 0.64

BWN/BWE O72 0.64 0.65 0.67 0.56

rounded and transparent papillae are present at the poste-

rior side, with a moderate medial gap, and absent at the

anterior side, except the most lateral part (seven papil-

lae). Submarginal papillae are absent. Anterior labium

contains two tooth rows of the same width (Al, A2),

large medial gap in second anterior tooth row (A2-GAP).

Posterior labium contains three tooth rows (P1, P2, P3),

Bonn zoological Bulletin 69 (2): 191-223

moderate medial gap in first tooth row (P1-GAP). Black

jaw sheaths, both with serrations. The upper jaw sheath

is wider than the lower jaw sheath. The labial tooth row

formula is 2(2)/3(1) (Fig. 3D). Characteristic traits and

the correlated proportions do not change during the de-

velopment stages 26 to 41 (Table 1).

©ZFMK

198 Benjamin Klein et al.

Table 2. Ranitomeya amazonica (n=4): development stages of embryos and hatchlings.

ege diameter 1.5 mm; eggs anthracite to dark gray; swam beneath the water surface;

19 large yolk sack present; embryonic body assumes larval shape; head and tail region

elongation of the tail; gills present, circulation recognizable; tail fins slightly visible;

elongation of the tail and the gills; tail pointed; overall body size increased; upper and

reduction of the right gill; oral apparatus discernible; yolk sack almost fully atrophied

n=4 Day Stage _ Traits

1 8

transparent egg integument; highly glutinous; no pigmentation

= 2 10 eges with brown pigmentation; dorsal lip visible

im roe

2 $ 13 neural plate visible

= 4 -

fae

visible; larva dun, spotted beige; gill buds present; mouth slightly perceptible

6 20

tn myosepta visible; vent tube bud visible

2 Re 21222

= lower tail fins more transparent; denser pigmentation of body and tail region

e 8 22 eyes visible; nares discernible; atrophy of the yolk sack initiated

9 23-24

10 24-25 gills absent in 75% of the clutch; yolk sack completely atrophied

11-12 25 gills absent; spiracle forming on the left

Coloration of a living tadpole of R. amazonica (ZFMK

97374). The dorsum is black to grey, with a yellowish

green median stripe and two dorsolateral stripes of the

same color, which run parallel to the longitudinal axis,

and two lateral stripes (Fig. 3A1, A2). The two dorsolat-

eral stripes originate at one point posterior to the nares,

become separated and run next to the eyes to the base of

the tail, with a moderate gap on eye level. The median

one lies in between the two others, starts at eye level and

ends prior to the tail-body junction. The lateral stripes are

situated differently. One of the lateral stripes is situated

at the first half of the body below the longitudinal axis,

while the other one is located above the longitudinal axis

at the second half of the body. The hindlimbs are dark

bluish with large black spots. The tail shows a brownish

coloration and is covered with dark and bright spots, the

second half is brighter than the first half. Fins are trans-

parent and spotted with beige dots. The density of dots

wanes till the tip.

During metamorphosis, the dorsal coloration of tadpoles

changed in regard to the different development stages

(Fig. 4). Reaching stage 25 some specimens displayed

a few isolated yellowish green spots while the majori-

ty showed no coloration. At stage 28 some parts of the

medial and dorsolateral stripes were present at the first

half of the dorsum. In comparison to the final coloration,

those areas were yellowish green instead of yellow and

lacked a continuous connection. At stage 36 the color

pattern was yellow, the dorsolateral stripes reached the

second half of the body and the medial stripe ended close

to the posterior margin of the eyes. While the dorsolateral

stripes were continuous, the medial stripe was spotted.

At stage 41, the dorsolateral stripes reached the tail-body

Bonn zoological Bulletin 69 (2): 191-223

junction and the medial line ended at the second half of

the body. Moreover, each flank displayed the initiation of

the ventrolateral stripes posterior to the forelimb pouch-

es, which were visible in dorsal view, as well as the typi-

cal color pattern of the hindlimbs (Fig. 3C1, C2).

Coloration of a preserved tadpole of R. amazonica

(ZFMK 97374). The dorsum is dark gray, with a brown-

ish area at the forelimb pouches. Dorsolateral and me-

dian stripes are whitish and run on top or parallel to the

longitudinal axis, clearly discernible on the head and the

first half of the body. Dorsolateral stripes originate and

bifurcate at one point posterior to the nares and run next

to the eyes, with a moderate gap on eye level. The median

stripe runs in between the eyes, not fusing with the ori-

gin of the dorsolateral stripes. The hindlimbs are bluish

gray, spotted with dark dots. The tail is brownish; the first

half is darker than the second one, which is almost trans-

parent. Fins are transparent and spotted with beige dots.

Ventral side has a dark grey to brown coloration, except

one bright spot at the chin, posterior to the oral disc.

Larval staging. During their embryonic development,

all four to six eggs of the same clutch develop at the same

pace, except the reduction of the gills. While the majority

of the eggs swam separately beneath the water surface,

two in each clutch stayed as a pair (Fig. 5B). Eggs up

to stage 10 were not pigmented (Fig. 5A). At stage 10,

when the dorsal lip was visible, the pigmentation start-

ed and the eggs became brownish. After three days, the

neural plate was discernible (Fig. 5C). Reaching stage

18, a whitish yolk sack was present at the ventral side

of the embryo and body parts were slightly differentiat-

©ZFMK

Larval characterization of six poison-dart frogs 199

10 mm 10 mm

ait’

asi

ee yt! att

yeu

Fig. 3. Illustrations of the tadpole of Ranitomeya amazonica, stage 41 of Gosner (1960). Al. Dorsal view, photograph. A2. Dorsal

view drawing. B1. Ventral view, photograph. B2. Ventral view, drawing. C1. Lateral view, photograph. C2. Lateral view, drawing.

D. Drawing of the oral disc. LTRF=2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

200 Benjamin Klein et al.

avy

Fig. 4. Development of the color pattern of Ranitomeya amazonica. A. Tadpole at stage 25 with isolated colored spots. B. Tadpole

at stage 25 without isolated colored spots. C—D. Different densities at Gosner stage 30. E. Tadpole at Gosner stage 36. F. Tadpole

at Gosner stage 41, typical color pattern on hindlimbs.

ed (Fig. 5D). At stage 19, the embryo slowly assumed a

larval shape. The head and tail region were visible and

the larva had a dun coloration with beige spots. While

the gill buds, the opening of the mouth and the ventral

tube emerged, the eyes were absent. At stage 20, the

gills and the correlated circulation were present while

the whole body was elongated (Fig. 5E, Table 2). Upper

and lower tail fins were slightly visible and the myosepta

were present. Between stages 21 and 22, the tail and the

gills were even more elongated, the overall body size in-

creased and the pigmentation of all structures was denser.

Tail fins were transparent, the tail was pointed. At stage

22, eyes were visible, nares were discernible and the de-

crease of the yolk sack was initiated (Fig. 5F). During

the transition from stage 23 to 24, the sinistral gills were

present while the dextral gills were completely reduced

(Fig. 5G). The yolk sack was almost fully atrophied and

the oral apparatus was formed. The transition to a free

living and mobile tadpole started at stage 25, while the

majority of the clutch was no longer enclosed by the jelly

layer and the yolk sack was fully reduced. The spiracle

was formed on the left, and after eleven to twelve days

of development, the hatchlings swam freely within the

water column (Fig. 5H—I).

Bonn zoological Bulletin 69 (2): 191-223

Right after hatching, the free-swimming larvae had a

surface area of 0.10 + 0.02 cm? (Table 3). Between the

stages 25 to 27, while the hindlimb bud was slightly de-

veloped, the surface increased by 330%, resulting in an

area of 0.33 + 0.20 cm?. At stage 28, which half of the

tadpoles had reached after 49 to 67 days (median=56

days), they had a mean surface area of 0.74 + 0.12 cm?

(Table 3). The hindlimb bud was as long as wide and the

dorsal color pattern was slightly visible at the first half

of the body. Between stages 29 to 40, where the comple-

tion of the hindlimb development took place, the larvae

had a mean surface area of 0.98 + 0.19 cm?. Thus, all

toes, the metatarsal tubercles and the subarticular patch-

es were discernible. With an area of 1.17 + 0.12 cm/?,

half of all tadpoles reached stage 41 after 69 to 88 days

(median=84 days). Forelimb buds were visible and the

hindlimbs showed the typical color pattern of the adult

frog (Fig. 3A1, Bl). Furthermore, colored dorsolateral

stripes were discernible and the ventral tube as well as

the oral apparatus was still present. While the forelimbs

grew inside the body, during the transition from stage

41 to 42, the larvae reached their maximum size with

a surface area of 1.19 + 0.12 cm’. After 82 to 94 days

(median=89 days), 50% of all metamorphs had emerged

©ZFMK

Larval characterization of six poison-dart frogs 201

i> ~.

y ;

Fig. 5. Embryos and hatchlings of Ranitomeya amazonica. A. Isolated egg at stage 8. B. Egg pair at stage 9-12. C. Embryo at stage

13-14. D. Embryo at stage 18-19. E. Hatchling at stage 20. F. Hatchlings at stage 22. G. Hatchling at stage 23-24. H. Hatchlings

at stage 25. I. Free swimming larva at stage 25-26.

forelimbs, while the surface area decreased to 1.08 +

0.17 cm?. The resorption of the tail started after 91 to 99

days (median=96 days), while the tadpoles had a mean

surface area of 0.86 + 0.15 cm?. During the next days,

the tail atrophied until the larva completed the metamor-

phosis, whereby the area of the larva was reduced to 0.82

+ 0.15 cm?. Thus, the transition from a free-swimming

larva to a froglet with a remnant of the tail lasted 91 to 99

days (median=96 days), while some individuals needed

less (84 days) and others more time (105 days, Fig. 6).

Bonn zoological Bulletin 69 (2): 191-223

= “ : P+ 2: OR Se 2 yy Tey _ ae ete ane

An additional and more detailed staging table, based on

stereomicroscopic determinations of 17 specimens be-

tween stages 25 to 41, can be found in the Table 4.

The complete development, from the embryogenesis

through hatching and larval period to metamorphosis,

was observed under constant conditions with a tempera-

ture of 24 °C while the annual mean temperature within

the natural distribution area of R. amazonica is slight-

by highiers( 1) Was 2e°C 1 Pao a a Cl 2184 C.

Karger et al. 2017a,b; Fig.7)

©ZFMK

202

Benjamin Klein et al.

Table 3. Ranitomeya amazonica (n= 16) larvae and metamorphs development stages based on image analyses. Area [cm?] is highly

correlated with body mass.

n=16 Stage (n) Traits Area [cm?’|

25 (16) spiracle present; oral apparatus clearly visible; typical dorsal color pattern 0.10 40.02

absent

25-27 (16) hindlimb bud slightly developed, diameter < length; typical dorsal color 0.33 + 0.20

pattern slightly visible at the first half of the body

a5 28 (14) length of the hindlimb bud equal to the diameter, no pigmentation 0.74 + 0.12

> 28-40 (14) hindlimb bud length > diameter; foot paddle slightly visible; indentation 0.98 +0.19

§ between toes 4—5 and 3-4; indentation between toes 4-5, 3-4 and 2-3;

Indentation between toes 4—5, 3-4, 2—3 and 1-2; toes 3—5 separated; all toes

separated; metatarsal tubercle present; subarticular patches present; hindlimbs

with pigmentation; typical dorsal color pattern present

Al (14) forelimb buds present; typical color pattern on hindlimbs present; lateral 1.17+0.12

Stripes present

2 41-42 (14) enlargement of the forelimb buds LOE O12

S 42 (9) forelimbs emerged 1.08 + 0.17

S&S 43 (10) initiation of tail resorption 0.86 + 0.15

> 43—46 (10) reduction of the tail until metamorphosis was completed 0.82 +0.15

Table 4. Ranitomeya amazonica (n=17) larval development stages based on stereomicroscopic determinations. Area [cm7?] is

highly correlated with body mass.

n=17 Stage(n)_ Traits Area [cm?|

25(3) spiracle present; oral apparatus clearly visible; typical dorsal color pattern is 0.25+0.01

absent

28(5) — hind limb bud slightly developed, diameter < length; typical dorsal color 0.49+0.09

pattern slightly visible at the first half of the body

29 (9) length of the hind limb bud 1.5 times of the diameter 0.59 + 0.08

z3 30 (4) length of the hind limb bud two times of the diameter 0.66 + 0.07

> 31(4) — foot paddle is slightly visible, slight pigmentation at the base of the hindlimb 0.75+0.11

ss 33(7) indentation between toes 4—5 and 3-4 0.80 + 0.14

35(9) indentation between toes 4—5, 3-4, 2—3 and 1-2 0.87+0.14

36(3) toes 3—5 are separated; dorsal color pattern is denser and exceeds the first half 1.28+0.11

of the body

39 (4) all toes are separated; metatarsal tubercle is present; subarticular patches are 1.30+0.08

present

41(2) forelimb buds are present; typical color pattern on hind limbs present; lateral 1.36+0.12

stripes are present

Ranitomeya benedicta Brown, Twomey, Pepper & San-

chez-Rodriguez, 2008

Breeding behavior in captivity. The breeding pair

among the three available specimens mainly deposited

their clutches of two to three eggs inside a dry and hori-

zontally orientated film container which was attached to

the cork tile. In rare cases, they placed the clutches within

Bonn zoological Bulletin 69 (2): 191-223

the bromeliad phytotelm. Reproduction did not obey a

standardized way.

Larval morphology. Tadpole description is based on one

individual at stage 41 (ZFMK 97363). Further vouch-

er specimens are ZFMK 97367 and 97376. According

to McDiarmid & Altig (1999), the larva belongs to the

exotrophic, lentic, benthic and arboreal larval type. All

measurements that were used to calculate the following

©ZFMK

Larval characterization of six poison-dart frogs 203

A R. amazonica B R. benedicta

Size [cm2]

Traits

Time [d] Time [d]

CR. imitator D R. reticulata

1.0

Size [cm2]

04 06 08 1.0 1.2

0.4

0.2

Traits

Time [d] Time [d]

E R. sirensis F R. vanzolinii

Size [cm2]

5 02 04 06 08 10 1.2

Traits

Time [d] Time [d]

Fig. 6. Developmental series of six Ranitomeya species during the transition from a hatchling to a froglet. The upper panel illus-

trates the increase of surface area over time, whereby the surface area [cm?] is highly correlated with the body mass. Warmer colors

indicate a higher sample density; each circle represents one data point. Loess function represented by the red lines, whereby the

outer lines display the 95% confidence interval. The lower panel illustrates the temporal occurrence of the following traits: 1=no

limb bud discernible; 2=hindlimb bud discernible; 3=forelimb pouches discernible; 4=forelimbs emerged; 5=initiation of tail

resorption.

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

204

proportions and its comparison with the other species of

this study, are to be found in Appendix III.

Dorsal view: The body is oval shaped and moderate-

ly elongated (MBW/BL=0.78). The snout is short and

rounded (RED/BL=0.18, BWN/BWE=0.57). The nares

are positioned and orientated laterally; their shape is not

visible in dorsal view. A skin fold connects the nares with

the anterior edge of the eyes. Nares are closer to the snout

than to the eyes (RND/RED=0.41). The eyes are large

(ED/BL=0.11), positioned dorsally and orientated later-

ally. Internarial distance is smaller than the interorbital

distance (IND/IOD=0.40). The single and sinistral spir-

acle is not visible in dorsal view.

Lateral view: The body is depressed (MBH/MBW=

0.59), the snout pointed. Nares are small and elliptical.

The spiracle is situated below the longitudinal axis, at the

second half of the body (RSD/BL=0.56). The inner wall

of the spiracle 1s free from the body, the opening is round,

and the spiracle tube is short. Maximum body height is

situated posterior to the eye. The tail is long and rounded

(TAL/BL=2.06, TAL/TL=0.67), the musculature well

developed (TMH/MTH=0.62, TMW/MBW=0.33).

The “V”-shaped myosepta are visible along the whole

length of the tail. Both tail fins are of the same height

and originate posterior to the tail-body junction, the low-

er fin slightly anterior to the upper fin. The ventral tube

is small, dextral; emergence from abdomen is sagittal,

opening is elliptical. Hindlimbs are fully developed. Oral

apparatus is visible in lateral view.

Oral apparatus: The oral disc is elliptical, positioned

ventrally and covers nearly one third of the body width

(ODW/MBW =0.29), emarginated. Marginal, ensiform,

rounded and transparent papillae are present at the pos-

terior labium and absent at the anterior labium, except

Benjamin Klein et al.

the most lateral part (five papillae). Submarginal papillae

are absent. The anterior labium contains two tooth rows

(Al, A2) of the same width, whereas the second row is

divided by a large medial gap (A2-GAP). The posterior

labium contains three rows of teeth (P1, P2, P3) with a

moderate medial gap in the first tooth row (P1-GAP). P1

P2 and P3 have the same width. Both jaw sheaths are

black and serrated. The upper jaw sheath is wider than

the lower jaw sheath. Lateral processes are present, ex-

tending barely past the lower jaw. The tooth row formula

is 2(2)/3(1) (Fig. 8D).

Coloration of a living tadpole of R. benedicta (ZFMK

97363). The basic color of the dorsum is black to dark

gray, with a reddish area anterior and posterior to the

eyes, which starts posterior to the nares and ends at the

first half of the body in dorsal view (Fig. 8A1, A2). In

between both eyes light coloration is lacking, except one

narrow stripe which connects the posterior and anterior

part of the color pattern. The hindlimbs are as black as

the dorsum. The tail 1s brownish beige and covered with

darker dots. Fins are transparent and spotted with beige

dots.

Coloration of a preserved tadpole of R. benedicta

(ZFMK 97363). The basic color of the dorsum is dark

gray, except some brighter areas at the forelimb pouch-

es and at the muscle attachment of the tail. Additionally,

there is a bright area anterior and posterior to the eyes.

While the anterior part is bright orange, the posterior

part is auburn. Both parts are fused medially, creating a

face mask. The hindlimbs are as gray as the dorsum, with

some slightly bright areas at the tip of the toes. The tail is

beige, covered with grayish dots; the first half is brighter

Table 5. Ranitomeya benedicta (n=4) larvae and metamorphs development stages based on image analyses. Area [cm7?] is highly

correlated with body mass.

n=4 Stage(n)_ Traits Area [cm?]

25(4) sinistral spiracle present; oral apparatus clearly visible 0.23 + 0.04

25-27(4) hindlimb bud slightly visible, length < diameter; body depressed 0.60 + 0.24

28 (3) length of the hindlimb bud equal to the diameter, no pigmentation LODE Od 1

x hindlimb bud length > diameter; foot paddle slightly visible; indentation

5 between toes 4—5 and 3-4; indentation between toes 4—5, 3—4 and 2-3;

— 28-40(3) Indentation between toes 4—5, 3-4, 2—3 and 1-2; toes 3—5 separated; all toes 1.20 4:0: 16

separated; metatarsal tubercle present; subarticular patches present; hindlimbs

with pigmentation; typical dorsal color pattern present

; , Sees +

41 (3) forelimb buds present; typical color pattern on hindlimbs present ere

4 41-42(3)_ enlargement of the forelimb buds 1.45 + 0.09

e 42 (1) forelimbs emerged 39

= 43 (1) initiation of tail resorption 1.03 + 0.00

E 43-46 (1) reduction of the tail until metamorphosis was completed 1.00 + 0.13

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs 205

18 20 22 24 26

Annual Mean Temperature [°C]

20 22

Min Temperature Coldest Month [°C]

12 14 16

24 26 28 30

Max Temperature Warmest Month [°C]

R. amazonica_ R. benedicta R. imitator R. reticulata R. sirensis R. vanzolinii

Species

Fig. 7. Climatic characteristics within the geographic ranges of six Ranitomeya species in terms of annual mean temperature, min-

imum and maximum temperature of the coldest / warmest month. Boxplots show the 95% range, lower and upper hinge enclosing

50% of the samples and the median based on a random sample per 10 km”.

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

206 Benjamin Klein et al.

10 mm 10 mm

wt an

1mm

Fig. 8. Illustrations of the tadpole of Ranitomeya benedicta, stage 41 of Gosner (1960). Al. Dorsal view, photograph. A2. Dorsal

view, drawing. B1. Ventral view, photograph. B1. Ventral view, drawing. C1. Lateral view, photograph. C2. Lateral view, drawing.

D. Drawing of the oral disc. LTRF = 2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs

than the second half. The ventral side is as gray as the

dorsum, with an auburn area around the oral disc which

fades till the tail-body junction.

Larval staging. Right after hatching, the free-swimming

larvae had a surface area of 0.23 + 0.04 cm? (Table 5).

During the transition from stage 25 to 27, while the hind-

limb buds were slightly visible, the surface area increased

to 0.60 + 0.24 cm? (Table 5). This development period

lasted for at least 54 to 70 days (median=61 days), when

half of all individuals reached stage 28. At this point

the hindlimb buds were equal in length and diameter

and therefore clearly discernible, while the tadpoles had

reached a surface area of 1.01 + 0.11 cm?. Between stages

29 to 40, where the completion of the hindlimb develop-

ment took place, the tadpoles had a mean surface area of

1.20 + 0.16 cm?. Thus, all toes, the metatarsal tubercles

as well as the subarticular patches were discernible. After

80 to 94 days (median=88 days), 50% of the individuals

reached stage 41. The forelimb pouches were visible and

the larvae had a surface area of 1.38 + 0.13 cm?. While

the forelimbs evolved within the body, during the transi-

tion from stage 41 to 42, the tadpoles reached the peak

of their growth with an area of 1.45 + 0.09 cm’. After

105 days, the forelimbs emerged and the remaining larva

reached stage 42. Seven days later, the resorption of the

tail was initiated, ensuring the transition from a hatchling

to a young froglet. Therefore, the area of the metamorph

was reduced to a size of 1.00 + 0.13 cm?. Altogether, the

development from a free-swimming larva to a young

froglet lasted around 114 days (Fig. 6).

The development was observed under constant condi-

tions with a temperature of 24 °C, while the annual mean

temperature within the natural distribution area of R. ben-

edicta is slightly higher (T,,.,,=25.3 °C, T,,,,=28.8 °C,

Tyg=2l3"E: Katger etal) 2017a, 'b, Fig. 7).

Ranitomeya imitator (Schulte, 1986)

Breeding behavior in captivity. The single breeding

pair deposited the clutches of one to two whitish to beige

eggs directly in the bromeliad phytotelm or in a horizon-

tally orientated film container, which was attached to the

side wall of the terrarium, which was kept moist by the

misting system. Reproduction did not obey a standard-

ized way.

Larval morphology. Description of the tadpole is based

on two specimens at stage 41 (ZFMK 97358). Further

voucher specimens are ZFMK 97364, 97368 and 97377.

According to McDiarmid & Altig (1999), the larvae be-

long to the exotrophic, lentic, benthic and arboreal larval

type. All measurements that were used to calculate the

following proportions and its comparison with the other

species of this study, can be found in Appendix III.

Bonn zoological Bulletin 69 (2): 191-223

207

Dorsal view: The body is shaped elliptically and

slightly elongated (MBW/BL=0.75). The snout is short,

rounded and moderately pointed (RED/BL=0.26, BWN/

BWE=0.65). The shape of the nares is not visible in dor-

sal view. A skin fold, which originates at the nares, ends

close to the anterior margin of the eyes; the two land-

marks are not connected. Nares are located closer to the

snout than to the eyes (RND/RED=0.39). Eyes are large

(ED/BL=0.09), situated dorsally and orientated laterally.

Internarial distance is smaller than the interorbital dis-

tance (IND/IOD=0.46). The single sinistral spiracle is

not visible in dorsal view.

Lateral view: Body is depressed (MBH/MBW =0.73),

snout is pointed. Nares are round, positioned and orien-

tated dorsally. The spiracle is positioned below the lon-

gitudinal axis, at the posterior part of the body (RSD/

BL=0.56), the inner wall is free from the body and the

opening is round, spiracle tube is short. The maximum

body height is situated between the eyes and the tail-body

junction. The tail is long and the tip is broadly round-

ed (TAL/BL=1.83, TAL/TL=0.65). The musculature is

well developed (TMH/MTH=0.49; TMW/MBW = 0.34).

The “V”- shaped myosepta are visible along the whole

length of the tail, particularly in the first half. The up-

per fin originates anterior, the lower posterior to the tail-

body junction. Upper fin is slightly higher than lower

fin. Ventral tube partially absorbed, dextral; emergence

from the abdomen sagittal, the opening is triangular and

has smooth edges. Hindlimb development is completed.

Parts of the oral apparatus are visible in lateral view, par-

ticularly the margins.

Oral apparatus: The oral disc is shaped elliptically,

positioned ventrally, emarginated and covers almost one

third of the body width (ODW/MBW=0.31). Two rows

of marginal, ensiform, rounded and transparent papillae

are present at the posterior labium (around 20 papillae)

and except one short row at the most lateral part, absent

at the anterior labium (three to five papillae). Submargin-

al papillae are absent. The anterior labium contains two

tooth rows of equal width (Al, A2) with a large medial

gap in the second row (A2-GAP). The posterior labium

contains three tooth rows (P1, P2, P3) with a moderate

medial gap in the first tooth row (P1-GAP). Black jaw

sheaths, both serrated. Upper jaw sheath is wider than

the lower jaw sheath. Lateral processes are present, ex-

tending slightly past the lower jaw. Tooth row formula is

2(2)/3(1) (Fig. 9D).

Coloration of a living tadpole of R. imitator (ZFMK

97358). The basic color of the dorsum is beige, heavily

covered with puce to black dots. Additionally, the first

half of the body is strongly dotted with yellowish green

spots, which are able to reflect the light and become gold-

en yellow, while the second half is almost completely

covered with black dots, except some single yellowish

green spots. The hindlimbs are beige with dark spots. The

©ZFMK

208 Benjamin Klein et al.

10 mm 10 mm

Bi B2

10 mm 10 mm

pe: as “att ut Mt

eit it ht

mee “ft

7) \\

vt " dunt set we

ANY am

ty 14

Lon, Wty Merny ; ret

Mey

Mity

1mm

Fig. 9. Illustrations of the tadpole of Ranitomeya imitator, stage 41 of Gosner (1960). Al. Dorsal view, photograph. A2. Dorsal

view, drawing. B1. Ventral view, photograph. B2. Ventral view, drawing. C1. Lateral view, photograph. C1. Lateral view, drawing.

D. Drawing of the oral disc. LTRF = 2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs 209

tail is dun and spotted with puce dots; the second half is

brighter than the first one. Fins are transparent and spot-

ted with beige dots.

Coloration of a preserved tadpole of R. imitator

(ZFMK 97358). Dorsum is beige, densely spotted

with gray dots, with some brighter areas at the forelimb

pouches and the muscle structures at the tail-body junc-

tion. The hindlimbs and the tail are of the same color as

the dorsum, spotted with gray dots. While the dots on the

hindlimbs are evenly distributed along their length, the

pigmentation of the tail decreases towards the tip. The

fins are transparent and spotted with gray dots. The ven-

tral side is beige and spotted with gray dots, while the

concentration of that pigmentation increases to the tail-

body junction.

Larval staging. One egg with a diameter of around

1.2 mm was found within a bromeliad phytotelm, where

it swam beneath the water surface. At this time, it was

not pigmented, had a transparent egg integument and

was encompassed by a highly glutinous layer (Fig. 10A).

Fig. 10. Embryos and hatchlings of Ranitomeya imitator. A. Isolated egg at stage 8. B. Embryo at stage 14-15. C. Embryo at stage

16-17. D. Embryo at stage 19. E. Embryo at stage 20. F. Hatchling at stage 21. G. Hatchling at stage 24. H. Free swimming larva

at stage 25—26. Picture C is from a different clutch.

Bonn zoological Bulletin 69 (2): 191-223

©ZFMK

210

Benjamin Klein et al.

Table 6. Ranitomeya imitator (n=1) embryo and hatchling development stages.

n=1 Day Stage

Traits

i 8 egg diameter 1.2 mm; egg whitish to beige; cells moderately large; swam beneath

a the water surface; transparent egg integument; highly glutinous; no pigmentation

>. 2 9 egg coloration paler than before; higher number of smaller cells

3 3 11 yolk plug visible

= 4 14 neural fold present

3 19 large yolk sack present; embryonic body assumes larval shape; head and tail region

visible; larva pale; gill buds present

6 20 elongation of the tail; gills present; circulation recognizable; tail fins slightly visible;

myosepta visible; vent tube bud visible

7 21-22 elongation of the tail and the gills; tail pointed: overall body size increased; upper

and lower tail fins more transparent; denser pigmentation of body and tail region

8 22 elongation of the gills; eyes visible; atrophy of the yolk sack initiated

a 9 D2 tail fins are higher; pigmentation of the body denser; nares are discernible; yolk sack

2 covered with blood vessels

= 10 23 tail fins transparent and spotted with dots; yolk sack almost completely atrophied:

s oral apparatus discernible

- 11-12 24 dextral gills absent, sinistral gills present; pigmentation of body and tail denser,

spotted with beige dots; upper tail fin spotted with dark dots, lower tail fin with

bright dots; anterior and posterior labia discernible; papillae present

13 24 sinistral gill partially reduced; yolk sack completely atrophied; maximum body

width in the second half of the body

14-15 25 gills absent; spiracle forming on the left

16 25 upper and lower jaw sheath visible (black); larva hatched

Table 7. Ranitomeya imitator (n=3) larvae and metamorphs development stages based on image analyses. Area [cm?] is highly

correlated with body mass.

n=3 Stage(n) _ Traits

Area [cm?]

29°C) spiracle present; oral apparatus clearly visible; typical dorsal color pattern absent 0.22 + 0.00

hindlimb bud slightly developed, diameter < length; typical dorsal color pattern

— - 3s: +

22-29, (Oe a ohtig, wasiblactinenist halk onthe body Ye ia ee

% 28 (3) length of the hindlimb bud equal to the diameter, no pigmentation 0:69°0.11.

S hindlimb bud length > diameter; foot paddle slightly visible; indentation

between toes 4-5 and 3-4; indentation between toes 4-5, 3-4 and 2-3;

28-40 (3) Indentation between toes 4—5, 3-4, 2—3 and 1-2; toes 3-5 separated; all toes 0.89+0.16

separated; metatarsal tubercle present; subarticular patches present; hindlimbs

with pigmentation; typical dorsal color pattern present

4] (3) forelimb buds present; typical color pattern on hindlimbs present 1.11 £0.04

2 41-42 (2) enlargement of the forelimb buds 1.18 + 0.09

a. 42 (2) forelimbs emerged L200 217

= 43(2) initiation of tail resorption 1.03 + 0.10

= 43—46 (2) reduction of the tail until metamorphosis was completed 103-010

Bonn zoological Bulletin 69 (2): 191-223

©ZFMK

Larval characterization of six poison-dart frogs 211

Table 8. Ranitomeya imitator (n=4) larval development stages based on stereomicroscopic determinations. Area [cm?] is highly

correlated with body mass.

n=4 Stage(n) Traits Area [cm?’|

25(1) sinistral spiracle present; oral apparatus clearly visible; first half of the body 0.20

brighter than the second half; first half of the tail darker than second half

26(1) — hindlimb bud slightly developed, length < % diameter 0.25

28 (1) length of the hindlimb bud equal to the diameter 0.40

F, 29 (15) length of the hindlimb bud 1.5 times of the diameter 0.59

> 30 (1) length of the hindlimb bud two times of the diameter 0.69

5 31 (1) foot paddle slightly visible 0.75

S33) indentation between toes 4—5 and 3-4 0.82

34(1) indentation between toes 4—5, 3-4 and 2-3: dorsal color pattern slightly visible 1.024 0.03

35 (1) indentation between toes 4—5, 3-4, 2—3 and 1-2; hindlimbs with pigmentation 1.09

36(2) toes 3-5 separated 1.15 +0.09

37 (2) all toes separated; metatarsal tubercle present; subarticular patches present 1.16+0.05

Al forelimb buds present; typical color pattern on hind limbs present 1.18 +0.09

After one day it reached stage 9, the coloration became

paler and the number of discernible cells increased (Ta-

ble 6). At day three the egg reached stage 11 and the

yolk plug was visible, followed by the neural fold at day

four (Fig. 10B). A large yolk sack was discernible and

the embryonic body assumed a larval shape at stage 19

(Fig. 10D). Thus, the head and tail region became visible

and the gill buds were present. After six days of devel-

opment the gills were discernible and the tail underwent

several changes. The upper and lower tail fins together

with the myosepta were slightly visible, while the whole

tail was elongated (Fig. 10E). That elongation went on

until day eight, as the hatchling reached stage 22.

The tail was pointed, the overall body size and the area

of the gills increased, whereby the yolk sack atrophied.

The pigmentation of the body and tail region became

denser; the tail fins more transparent (Fig. 10F). At day

nine, the hatchling was still at stage 22. The tail fins were

higher, the nares discernible and the yolk sack was cov-

ered with blood vessels. When the larva reached stage

23, the transparent tail fins were spotted with beige dots,

the oral apparatus was clearly visible and the yolk sack

was almost completely atrophied. During day eleven and

twelve, at stage 24, the dextral gill was reduced while

the sinistral gill was still present (Fig. 10G). Additional-

ly, the pigmentation of the body and tail region became

denser and the anterior and posterior labia together with

the papillae were discernible. At stage 25, both gills were

absent while the sinistral spiracle was present. After 16

days of development the tadpole hatched from the jelly

layer and swam free in the water body (Fig. 10H). At this

time it had a surface area of 0.22 cm? (Table 7).

Between stages 25 to 27, where the hindlimb bud was

slightly discernible, the larvae had a surface area of 0.39

+ 0.12 cm? (Table 7). After 24 to 43 days (median=34

days), half of all individuals had a hindlimb bud that was

Bonn zoological Bulletin 69 (2): 191-223

equally in width and length and a surface area of 0.69

+ 0.11 cm? (Table 7). Between stages 28 to 40, the tad-

poles had a surface area of 0.89 + 0.16 cm?. During this

development period, the hindlimbs grew, all toes became

separated and the typical dorsal color pattern was dis-

cernible. After 48 to 53 days (median=51 days), 50% of

the tadpoles reached stage 41, with a surface area of 1.11

+ 0.04 cm?. The forelimb buds were clearly perceptible

and the hindlimbs displayed their typical reticulated col-

or pattern. The forelimbs emerged after around 63 days,

while the larvae reached their peak of growth with a sur-

face area of 1.20 + 0.17 cm?, followed by the resorption

of the tail after 67 days. During the transition to a young

froglet, the surface area decreased to a mean value of

1.03 + 0.10 cm? (Fig. 6, Table 7). A more detailed staging

table based on stereomicroscopic determinations of four

specimens between stages 25 to 37 can be found within

Table 8.

The development was observed under constant condi-

tions with a temperature of 24 °C, while the annual mean

temperature within the natural distribution area of R. im-

itator is slightly higher (T,,,.=25.5 °C, T,,,.=29.2 °C,

We, we Ul OC ANatger et al. 2017asby Fig, 57).

Ranitomeya reticulata (Boulenger, 1884)

Breeding behavior in captivity. The breeding pair de-

posited the clutches, consisting of an egg, within the bro-

meliad phytotelm. Reproduction was occasionally.

Larval morphology. Description is based on three tad-

poles at developmental stage 41 (ZFMK 97359). Further

voucher specimens are ZFMK 97360, 97365 and 97378.

According to McDiarmid & Altig (1999), the larvae be-

long to the exotrophic, lentic, benthic and arboreal larval

type. All measurements that were used to calculate the

©ZFMK

212 Benjamin Klein et al.

Al A2

10 mm 10 mm

B1 B2

10 mm 10 mm

* «

“. squatter <a ae

ae a ~ b *

at we ote ee

ys “ we

ee in) Me a

Nig Ef yicnece Ling

Ait getesnnt a ‘vo

“ay anna

tu gure ttl

D Ani las

1mm

Fig. 11. Illustrations of the tadpole of Ranitomeya reticulata, satage 41 of Gosner (1960). Al. Dorsal view, photograph. A2. Dorsal

view, drawing. B1. Ventral view, photograph. B2. Ventral view, drawing. C1. Lateral view, photograph. C2. Lateral view, drawing.

D. Drawing of the oral disc. LTRF = 2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs 213

Table 9. Ranitomeya reticulata (n=3) larvae development stages based on image analyses. Area [cm?] is highly correlated with

body mass. Note that data concerning metamorphs is missing as no specimen reached this stage.

n=3 Stage(n)_ Traits Area [cm?’|

273) spiracle present; oral apparatus clearly visible; typical dorsal color pattern 0.23 + 0.09

absent

25-27 (3) hindlimb bud slightly developed, diameter < length 0324011

< 28 (2) length of the hindlimb bud equal to the diameter, no pigmentation 0.81 + 0.01

. 28-40 (2) hindlimb bud length > diameter; foot paddle slightly visible; indentation 0.88 + 0.06

between toes 4—5 and 3-4; indentation between toes 4—5, 3-4 and 2-3;

Indentation between toes 4—5, 3—4, 2—3 and 1-2; toes 3—5 separated; all toes

separated; metatarsal tubercle present; subarticular patches present; hindlimbs

with pigmentation; typical dorsal color pattern discernible

Al (2) forelimb buds present; typical color pattern on hindlimbs present eA tom

Table 10. Ranitomeya reticulata (n=5) larval development stages based on stereomicroscopic determinations. Area [cm7?] is highly

correlated with body mass.

n=5 Stage(n)_ Traits Area [cm?|

31(3) foot paddle is present; hindlimb bud length is two times of the diameter 0.53 +0.01

34 (2) indentation between toes 4—5, 3-4 and 2-3 0.64 + 0.13

ag 36 (5) indentation between toes 4—5, 3—4, 2—3 and 1—2; toes 3—5 are separated; dorsal 0.72 +0.08

> color pattern extends from the posterior edge of the nares to the second half of

s the body

37(4) all toes are separated OnE? 0,06

39 (5) subarticular patches present; dorsal color pattern is denser, has cross 0.80 + 0.05

connections and ends at tail-body junction

41(5) forelimb buds are visible; vent tube is still present 0.78 + 0.02

following proportions and its comparison with the other

species of this study, are be found 1n the Table 13.

Dorsal view: The body is oval and elongated (MBW/

BL=0.62). The snout is short and moderately pointed

(RED/BL=0.28, BWN/BWE=0.65). The shape of the

nares 1s not visible in dorsal view, nares are closer to the

snout than to the eyes (RND/RED=0.40). A skin fold,

which originates at the nares, ends close to the anterior

margin of the eyes; the two landmarks are not connected.

The eyes are large (ED/BL=0.09), positioned dorsally

and orientated laterally. The internarial distance is small-

er than the interorbital distance (IND/IOD=0.53). The

single, sinistral spiracle as well as parts of the oral appa-

ratus are visible in dorsal view.

Lateral view: Body is slightly depressed (MBH/

MBW =0.68), the snout is pointed. Nares are round, lo-

cated and orientated dorsally. The spiracle is situated be-

low the longitudinal axis, at the second half of the body

(RSD/BL=0.64), the inner wall is free from the body

and the opening is round. The maximum body height is

located posterior to the eye. The tail is long and moder-

ately pointed (TAL/BL= 1.64, TAL/TL=0.62). The “V”-

shaped myosepta are visible along the whole length of

the tail. The upper fin originates posterior to the lower

Bonn zoological Bulletin 69 (2): 191-223

fin and the tail-body junction, the margin of the lower fin

is nearly parallel to the margin of the tail muscle. Ven-

tral tube is strongly atrophied, emergence from abdomen

sagittal. Hindlimbs are completely developed. Oral appa-

ratus is visible in lateral view.

Oral apparatus: The oral disc is elliptical, emarginated,

located anteroventrally and covers more than one third

of the maximum body width (ODW/MBW =0.40). Mar-

ginal, pointed and pigmented papillae are present at the

posterior labium and except the most lateral part, absent

at the anterior labium. Submarginal papillae are absent.

The anterior labium contains two tooth rows of an equal

width (Al, A2), the second tooth row has a large medial

gap (A2-GAP). The posterior labium contains three tooth

rows (P1, P2, P3), with a moderate gap in the first row

(P1-GAP). Tooth row P1 and P2 are of the same width,

the width of the P3 was not discernible. Both jaw sheaths

are black and serrated. The tooth row formula is 2(2)/3(1)

(Fig. 11D).

Coloration of a living tadpole of R. reticulata (ZFMK

97359). The dorsum has an anthracite basic color, with

three golden to orange stripes running on top or parallel

to the longitudinal axis (Fig. 11A1, A2). The two dorso-

©ZFMK

214

lateral stripes originate at one point posterior to the nares,

bifurcate and run close to the eyes, with a moderate gap

on eye level. The medial stripe runs in between the two

others, situated on the symmetry line of the body. De-

pending on the specimen, the medial and the dorsolateral

stripes are fused, originating from one point posterior to

the nares and anterior to the eyes. The distance between

the stripes decreased at the second half of the body. The

hindlimbs and the tail are as anthracite as the dorsum,

spotted with darker dots. Fins are transparent and spotted

with grayish dots.

Coloration of a preserved tadpole of R. reticulata

(ZFMK 97359). The dorsum has a beige basic color, with

some darker areas at the outermost part of the forelimb

pouches and one small line at the anterior margin of the

dorsolateral stripes. The area in between the dorsolateral

stripes, which extends to the tail-body junction, is of the

same color as the dark areas mentioned beforehand. The

dorsolateral and median stripes are clearly discernible on

the head and the first half of the body, running on top or

parallel to the longitudinal axis. The dorsolateral stripes

originate and bifurcate at one point posterior to the nares

and run next to the eyes, with a moderate gap on eye

level. The whitish median stripe originates in between

the eyes, not fusing with the origin of the dorsolateral

stripes. Anterior to the eye, the dorsolateral stripes are

beige, posterior they are whitish. The hindlimbs and the

tail are as beige as the dorsum, spotted with some dark

dots. Fins are transparent and spotted with dark dots. The

ventral side is beige, spotted with gray dots. The hind-

limbs’ ventral side is brighter than the dorsal side.

Larval staging. At stage 25, right after hatching, the tad-

poles had a surface area of 0.23 + 0.09 cm?. During the

transition from stage 25 to 27, where the hindlimb buds

were slightly visible, the surface area increased to 0.32 +

0.11 cm?. After 29 to 41 days (median =36 days), half of

all larvae had developed a hindlimb bud that was equally

Benjamin Klein et al.

in diameter and length and reached a surface area of 0.81

+ 0.01 cm?. Between the stages 28 to 40, the larvae had

a surface area of 0.88 + 0.06 cm?. During this develop-

ment period, the hindlimbs grew, all toes became separat-

ed and the typical dorsal color pattern was present. The

forelimb pouches were discernible after a minimum of 42

and a maximum of 63 days, while half of all individuals

reached that development stage after 54 to 58 days (me-

dian=56 days). At this point, the tadpoles had a surface

area of 1.02 + 0.11 cm?. Not a single larva completed the

full metamorphosis to a young froglet (Fig. 6, Table 9). A

more detailed staging table based on stereomicroscopic

determinations of five specimens from an external source

between stages 25 to 37 can be found within the Table 10.

The development was observed under constant condi-

tions with a temperature of 24 °C, while the annual mean

temperature within the natural distribution area of R. re-

ticulata is slightly higher (T,,,.,= 24-8 °C, Ty. 28-2 °C,

Tyin = 21.5 °C: Karger et al. 2017a,b; Fig. 7).

Ranitomeya sirensis (Aichinger, 1991)

Breeding behavior in captivity. The breeding pairs

among the four specimens deposited clutches of up to

two eggs in the bromeliad phytotelm. Reproduction oc-

curred occasionally.

Larval morphology. The description is based on lat-

eral and dorsal pictures of one specimen at stage 29.

Thus, no voucher specimen is available. According to

McDiarmid & Altig (1999), the tadpole belongs to the

exotrophic, lentic, benthic and arboreal larval type. All

measurements that were used to calculate the following

proportions and its comparison with the other species of

this study, can be found in Appendix III.

Dorsal view: Body shape 1s oval and slightly elongated

(MBW/BL=0.86). The snout is short and round (RED/

BL=0.24, BWN/BWE=0.88). Nares are oval in dorsal

view. The eyes are large (ED/BL=0.09), located dorsally

Fig. 12. Illustrations of the tadpole of Ranitomeya sirensis, stage 29 of Gosner (1960). A. Frontolateral view. B. Lateral view.

C. Ventral view. Photo credit: Morris Flecks.

Bonn zoological Bulletin 69 (2): 191-223

©ZFMK

Larval characterization of six poison-dart frogs

215

Table 11. Ranitomeya sirensis (n=31) embryos and hatchlings development stages based on image analyses. Area [cm?] is highly

correlated with body mass.

n=31 Stage(n) Traits Area [cm?|

25 (31) sinistral spiracle present; oral apparatus clearly visible 0.16+ 0.04

25-27 (31) hindlimb bud slightly visible, length < diameter 0.29 40.13

28 (15) hindlimb bud length=diameter O53: Oall

2 28-40 (15) hindlimb bud length > diameter; foot paddle slightly visible; indentation 0.86 + 0.23

5 between toes 4—5 and 3-4; indentation between toes 4-5, 3-4 and 2-3;

= Indentation between toes 4—5, 3-4, 2—3 and 1—2; toes 3—5 separated; all

toes separated; metatarsal tubercle present; subarticular patches present;

hindlimbs with pigmentation; typical dorsal color pattern present

41 (15) forelimb buds present; typical color pattern on hindlimbs present; lateral | Bal Des 6

stripes present

2 41-42 (15) enlargement of the forelimb buds 1.18+0.20

= 42 (15) forelimbs emerged 120 OehG

= 43 (15) initiation of tail resorption 1.04+0.16

> 43—46 (15) _ reduction of the tail until metamorphosis was completed BOL OG

and oriented dorsolaterally. Internarial distance in small-

er than interorbital distance (IND/IOD=0.48). Sinistral

spiracle is clearly visible in dorsal view.

Lateral view: The body is depressed (MBH/

MBW=0.71), the snout 1s moderately pointed. Nares

are almost round. Sinistral spiracle is situated below the

longitudinal axis, at the second half of the body (RSD/

BL=0.53), oriented laterally with an elliptical opening,

whereas the inner wall of the spiracle is free from the

body wall. The maximum body height is situated poste-

rior to the spiracle. The tail is long and broadly rounded

(TAL/BL=1.90, TAL/TL=0.66). The tail musculature is

well developed (TMH/MTH=0.51), “V-shaped myo-

septa are visible at the first two thirds of the tail. Both fins

are equal in height and originate at the tail body junction.

The ventral tube is situated dextrally, the emergence from

the abdomen is sagittal and the opening is oval. Hind-

limb development is not completed (length > 150% of

the diameter). Upper and lower labia are clearly visible

in lateral view.

Oral Apparatus: The oral disc is emarginated, ellipti-

cal, positioned ventrally and covers more than one third

of the maximum body width (ODW/MBW =0.39). Mar-

ginal papillae are present at the posterior labrum and at

the outermost parts of the anterior labium. The anterior

labium contains two tooth rows of the same width (A1,

A2), with a large gap in the second row (A2-GAP). The

posterior labium contains three tooth rows (P1, P2, P3),

of which the first has a moderate medial gap (P1-GAP).

The first two rows (P1, P2) have the same width, while

the third one (P3) is slightly shorter. The tooth row for-

mula is 2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223

Coloration of living tadpole of R. sirensis. The basic

color is beige, densely coverered with dark dots. Two

light blue spots anterior to the nares, fused medially

(Fig. 12A). The first half of the dorsum is brighter than

the second half, additionally slightly transparent below

the longitudinal axis (Fig. 12B). Inner organs are visible

in ventral and lateral view (Fig. 12C). The hindlimb buds

are white, slightly pigmented at the base. The tail has the

same coloration as the dorsum, the color density of the

dark pigmentation wanes to the posterior end. The tip of

the tail lacks any pigmentation. Fins are transparent and

spotted with brown dots. The density of those dots de-

creases to the tip.

Larval staging. During the stages 25 to 27, before the

hindlimb buds were clearly discernible, the larvae had

a mean surface area of 0.29 + 0.13 cm? (Table 11). Af-

ter 24 to 39 days, half of the tadpoles reached stage 28

(median=31 days). At this time, the hindlimb buds were

almost equal in width and length and the surface area in-

creased to 0.58 + 0.11 cm?. In between the stages 29 to

40, the hindlimb development was completed and the lar-

vae had a mean surface area of 0.86 + 0.23 cm?. After 47

to 56 days, 50% of the individuals reached stage 41 (me-

dian=52 days). The forelimb buds were perceptible and

the tadpoles had a surface area of 1.15 + 0.17 cm”. While

the forelimbs grew inside the dorsum, the larval growth

rate decreased. After 56 to 65 days, half of the tadpoles

reached stage 42 and the forelimbs emerged through the

body wall (median=60 days). At this time, the tadpoles

reached their peak of growth with a surface area of 1.20

+ 0.16 cm?. Afterwards, between day 60 and 71 (me-

dian=63 days), the resorption of the tail was initiated.

Close to the end of the metamorphosis, when the froglets

©ZFMK

216

had just a short remnant of the tail, the metamorphs had a

surface area of 1.01 + 0.16 cm? (Fig. 6, Table 11).

The development was observed under constant condi-

tions with a temperature of 24 °C, while the annual mean

temperature within the natural distribution area of R. si-

rensis is Slightly higher (T,,,,,.=24-7 °C, T,,,,=29-1 °C,

Twin 18.8 °C: Karger et al. 2017a,b; Fig. 7).

Ranitomeya vanzolinii (Myers, 1982)

Breeding behavior in captivity. Successful reproduc-

tions were observed in two different terraria, each inhab-

ited by four specimens. While the breeding pairs of the

first tank deposited the clutches of two to three whitish to

beige eggs in a horizontally orientated and dry film con-

tainer, the breeding pairs of the second tank placed their

clutches of similar size in the bromeliad phytotelm. In

rare cases, tadpoles at different development stages were

found within the bromeliad phytotelm. Reproduction oc-

curred occasionally.

Larval morphology. The description is based on a single

specimen at stage 41 (ZFMK 97361). Further voucher

specimens are ZFMK 97369 and 97379. According to

McDiarmid & Altig (1999), the tadpole belongs to the

exotrophic, lentic, benthic and arboreal larval type. All

measurements that were used to calculate the following

proportions and its comparison with the other species of

this study, can be found in Appendix III.

Dorsal view: Body shape is oval and elongated (MBW/

BL=0.76). The snout is short and moderately pointed

(RED/BL=0.23, BWN/BWE=0.65). The shape of the

nares is not visible in dorsal view. A skin fold connects

the nares with the anterior margin of the eyes. Eyes are

large (ED/BL=0.10), located dorsally and orientated

Benjamin Klein et al.

laterally. Internarial distance is smaller than interorbital

distance (IND/IOD=0.48). The single sinistral spiracle

is not visible in dorsal view.

Lateral view: Body is depressed (MBH/MBW =0.71),

snout is round. Nares are shaped elliptically, located lat-

erally and orientated ventrolaterally. The single, sinistral

spiracle is situated below the longitudinal axis, at the sec-

ond half of the body (RSD/BL =0.61), and is oriented

laterally. The inner wall is free from the body and the

opening is round. The maximum body height is situated

posterior to the eye. The tail is long and broadly round-

ed (TAL/BL=1.87, TAL/TL=0.65). The musculature is

well developed (TMH/MTH=0.54, TMW/MBW =0.33).

“V”-shaped myosepta are visible along the whole length

of the tail, particularly in the second half. At the maxi-

mum tail height, the upper fin is nearly double as high as

the lower fin. Both fins originate at the tail-body junction.

Ventral tube is slightly reduced, dextral, emergence sagit-

tal from abdomen. Hindlimb development is completed.

Upper and lower labia are visible in lateral view.

Oral apparatus: The oral disc is elliptical, emarginated,

positioned ventrally and covers nearly one third of the

maximum body width (ODW/MBW=0.27). Marginal,

transparent and rounded papillae are present at the pos-

terior labium and except of six to seven papillae at the

most lateral part, absent at the anterior labium. Submar-

ginal papillae are absent. The anterior labium contains

two tooth rows of the same width (Al, A2) with a large

medial gap in the second row (A2-GAP). The posterior

labium contains three tooth rows (P1, P2, P3) of which

the first row has a moderate medial gap (P1-GAP). P2 is

slightly shorter than P1, P3 is slightly shorter than P2.

Both jaw sheaths are black and serrated, lateral processes

of the upper jaw sheath are present and extend barely past

Table 12. Ranitomeya vanzolinii (n= 13) larvae and metamorphs development stages based on image analyses. Area [cm?] is highly

correlated with body mass.

n=13 Stage (n) Traits Area [cm?|

25,0132) sinistral spiracle present; oral apparatus clearly visible 0.19+0.05

25-27 (13) hindlimb bud slightly visible, length < diameter O34 OMld

28 (11) length of the hindlimb bud equal to the diameter 0:53:20. 15.

x 29-40 (11) hindlimb bud length > diameter; foot paddle slightly visible; indentation O76 +0413

: between toes 4—5 and 3-4; indentation between toes 4—5, 3-4 and 2-3;

- Indentation between toes 4—5, 3-4, 2—3 and 1-2; toes 3—5 separated; all

toes separated; metatarsal tubercle present; subarticular patches present;

hindlimbs with pigmentation

Al (9) forelimb buds present 0.98 + 0.09

2 41-42 (9) — enlargement of the forelimb buds 1.00 + 0.10

e 42 (9) forelimbs emerged LOSE O11

= 43 (9) initiation of tail resorption O92 Oat

2 43-46 (9) reduction of the tail until the completion of the metamorphosis 0.86 40.13

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

Larval characterization of six poison-dart frogs 217

10 mm 10 mm

B1 B2

10 mm 10 mm

C1 C2

10 mm 10 mm

t v

lag." edmaetytw j

Meena A

ee -

ee 8

‘

1mm

Fig. 13. Illustrations of the tadpole of Ranitomeya vanzolinii, stage 41 of Gosner (1960). Al. Dorsal view, photograph. A2. Dorsal

view, drawing. B1. Ventral view, photograph. B2. Ventral view, drawing. C1. Lateral view, photograph. C1. Lateral view, drawing.

D. Drawing of the oral disc. LTRF = 2(2)/3(1).

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

218

the lower jaw sheath. The tooth row formula is 2(2)/3(1)

(Fig. 13D).

Coloration of a living tadpole of R. vanzolinii (ZFMK

97361). The basic color of the dorsum is dark gray to

black and lacks any pattern of another color (Fig. 13A1,

A2). Hindlimbs are equally colored. The tail is brighter

than the dorsum, with a color gradient between the first

and the second half of the tail, whereas the color becomes

brighter till the tip. The transparent fins are spotted with

dark dots.

Coloration of a preserved tadpole of R. vanzolinii

(ZFMK 97361). The basic color of the dorsum is anthra-

cite, with some beige spotted areas at the forelimb pouch-

es and the muscle attachment of the tail as well as a light

gray area which originates at the tip of the snout and ex-

tends to the posterior margin of the eyes. The hindlimbs

are of the same color as the dorsum, slightly spotted with

beige dots. The tail 1s beige; the anterior half 1s darker

than the posterior one. Fins are transparent and spotted

with gray dots. The ventral side is as anthracite as the

dorsal side, slightly spotted with beige dots.

Larval staging. At stage 25, right after hatching, the tad-

poles had a surface area of 0.19 + 0.05 cm?. During the

transition from stage 25 to 27, when the hindlimb bud

was just slightly visible in some rare cases, the tadpoles

had a surface area of 0.32 + 0.11 cm? (Table 12). After

32 to 52 days, 50% of the larvae had reached stage 28.

At this time, while the hindlimb bud was as long as wide

and therefore clearly discernible, the tadpoles had a mean

surface area of 0.53 + 0.15 cm?. In between the stages

29 to 40, the development of the hindlimbs was com-

pleted and the larvae had a mean surface area of 0.76 +

0.13 cm?. All toes became separated and the hindlimbs

pigmented. After 51 to 73 days (mean=60 days), half of

all tadpoles had reached stage 41 (Fig. 6). The forelimb

buds were clearly discernible and the larvae had a mean

surface area of 0.98 + 0.09 cm?. While the forelimbs

grew inside the body, the larval growth rate decreased.

After 64 to 94 days (median=73 days), half of the tad-

poles reached stage 42 and the forelimbs emerged. At this

time the tadpoles reached their peak of growth with a sur-

face area of 1.03 + 0.11 cm?. Afterwards, as a part of the

ongoing metamorphosis during the stages 43 to 46, the

tail was reduced and the mean surface area decreased to

a value of 0.86 + 0.13 cm? (Fig. 6, Table 12). Altogeth-

er, the transition from a free living larva to a metamorph

which initiated the resorption of the tail lasted 61 to 107

days, while half of all tadpoles reached that development

period after 66 to 91 days (median=77 days).

The development was observed under constant condi-

tions with a temperature of 24 °C, while the annual mean

temperature within the natural distribution area of R. van-

Bonn zoological Bulletin 69 (2): 191-223

Benjamin Klein et al.

zolinii is slightly higher (T,,.,,=24.6 °C, T,,,.=28.9 °C,

Ty, =19.6"°C. Kareeret al 2017 eb igs 2).

DISCUSSION

We presented new data on the tadpole morphology and

development of six Ranitomeya species allowing for the

first time the identification of specimens in different de-

velopmental stages in a captive breeding setup. The de-

velopment, as studied herein, strongly coincides with the

tadpole staging system provided by Gosner (1960). How-

ever, few morphological variations between the herein

studied tadpoles and a generalized tadpole at Gosner

stage 41 were not compatible with those reported in the

literature. We observed a delay among the atrophy of the

ventral tube on R. amazonica tadpoles as well as a delay

among the atrophy of the oral apparatus on R. vanzolinii

tadpoles. The ventral tube in R. amazonica was still fully

developed, different from that observed for the tadpoles

of the other species studied herein, where the ventral tube

was partially absorbed. The tadpoles of R. vanzolinii in

this study displayed a complete oral apparatus, includ-

ing all anterior and posterior rows of teeth, different from

what is reported in Brown et al. (2011) where the tooth

rows of R. vanzolinii are irregular at stage 40.

The complete metamorphosis was described for five of

the six species studied here, as unfortunately none of the

tadpoles of R. reticulata completed the full metamorpho-

sis. In.R. amazonica, a species of the variabilis group, the

tadpoles needed 91—99 days for the complete metamor-

phosis. The tree species of the vanzolinii group studied

herein, namely R. sirensis, took 60-71 days, R. imitator

grew up within 67 days and R. vanzolinii needed 66-91

days for the complete metamorphosis. R. benedicta of the

variabilis group needed 114 days for the complete meta-

morphosis.

Waldram (2008) stated that tadpoles of R. sirensis (as

R. biolat) needed 58 days until they completed the meta-

morphosis in a natural environment. Herein we observed

a difference in relation of these results, where the tadpoles

of R. sirensis, which were bred at a constant temperature

of 24 °C with an artificial food resource needed 60-71

days before the absorption of the tail was initiated. In the

natural environment, anuran larvae respond to tempera-

ture variation by an alteration of their growth and devel-

opmental rates (Alvarez & Nicieza 2002; Smith-Gill &

Berven 1979). In our study, all clutches were bred un-

der constant conditions (24 °C) and in equivalent water

chemistry and nutrition. However, Kam et al. (2001) no-

ticed that the fluctuations in the temperature of phytotel-

mata mirrored fluctuations in air temperature and hence

the water temperatures in the phytotelms are not likely

to be constant. Findings of Poelman et al. (2013) support

this assumption, as the water temperatures reported in the

studied phytotelms present similar averages as the data

©ZFMK

Larval characterization of six poison-dart frogs 219

of air temperatures obtained from the CHELSA data set

(Karger et al. 2017a,b). It needs to be noted that the nu-

tritional conditions in a natural environment are different

from that provided during our study.

However, even if the development of the tadpoles

studied herein took place in an environment which 1s dif-

ferent from natural conditions, our results suggest only

small morphological differences compared to other de-

scriptions based on tadpoles collected in the field. There-

fore, we suggest that if the temperature in the climatic

test chamber mimics as closely as possible the known

temperatures within the natural habitats of the species,

the pace of larval development is presumably more ac-

curate under artificial conditions as they can be easily

standardized.

While the coloration of the eggs can be used to dis-

tinguish the vanzolinii clade from all remaining groups,

the coloration of tadpoles does not allow this. Neverthe-

less, the typical color pattern and the reticulation of the

hindlimbs verify the assignment of the specimens to the

genus Ranitomeya. The provided pictures, drawings and

descriptions of the tadpoles should allow to at least the

identification of specimens on genus level, which could

be useful to help customs officials to recognize CITES

protected animals in earlier development stages and

therefore reduce the illegal trade.

Methods criticism: Advantages, limitations and effi-

ciency

Recent studies provide growth rates in order to classify

the fitness of a species and therefore predict the effects of

changing environmental conditions or biotic factors (e.g.,

as reviewed by Dmitriew 2011). They are either obtained

by length-based measurements, quantified by weight or

image-based approaches (Relyea 2004; Davis et al. 2008;

Pham et al. 2015). As the body length of the tadpole at

Gosner stage 35 or greater is highly correlated with the

SVL of the young froglet, growth rates based on the for-

mer approach usually end at this point of development,

as seen in Amolops cremnobatus (Inger & Kottelat 1998)

(McDiarmid & Altig 1999; Pham et al. 2015). Thus, it

implies that the change in body size over time stops as

well, although shape changes alter the tadpoles’ body

mass as well as the surface area during this period. More-

Over, repeated measurements of living specimens, either

with calipers or integrated eye pieces, are stressful for

fragile individuals like tadpoles. Studies based on the lat-

ter approach use the surface area of a tadpole as a proxy

for its body mass. SAISAQ, the method used in this study

to generate growth rates of the tadpoles, was introduced

by Kurth et al. in 2014, extending the image-based con-

cept of Davis et al. (2008). Instead of manually analyzing

images with software packages like Fovea Pro or ImageJ,

the implementation into the open source statistic plat-

form R allows a semiautomatic procession based on stan-

Bonn zoological Bulletin 69 (2): 191-223

dardized image files. Nonetheless, the capabilities of this

method are limited. The emerging forelimbs at Gosner

stage 41 may affect the dorsal surface to mass relation-

ship, which could falsify the results of the actual and sub-

sequent stages. Moreover, the calibration of the camera

in a fixed angle and distance to the object influences the

picture quality. While the surface area is sharp and high

in contrast, the depth of field decreases. Thus, staging ta-

bles based on those pictures need conspicuous traits, re-

ducing their resolution. Nevertheless, SAISAQ allows to

document, quantify and monitor the tadpole development

in a time-efficient way, obtaining huge amounts of data

which could be used to extend our current knowledge of

several anuran species.

In order to maximize the sample size while reducing the

mortality rate, documentations of the embryogenesis as

well as microscopic determinations of the developmental

stages were neglected until the growth rate related data

acquisition was done. Species which stopped their repro-

duction at this time of the study lack these measurements

(Ranitomeya benedicta, R. sirensis and R. vanzolinii).

Thus, staging tables that allow a comparison of all six

Species are based on image analyses of the growth rate

related photographs, which are less detailed than micro-

scopic examinations. Therefore, further studies should

either start with the documentation of detailed staging

tables and the embryonic development, or conduct both

methods simultaneously to add to the completeness of

current descriptions. Additionally, an adjustment of the

climatic test chamber in regard to the temperatures of the

macro-habitats of the species could prove the statement

that specimens develop faster if the artificial environment

mirrors their natural conditions.

In times of a global biodiversity crisis and wide spread

population declines in amphibians, conservation breed-

ing programs become increasingly important. Our data

may provide a baseline for further research how to opti-

mize captive breeding in Ranitomeya species. The devel-

opmental staging tables and growth rates can be used to

compare different husbandry and breeding setups. Fur-

thermore, we hope that the detailed larval descriptions

are also useful for the identification of specimens by cus-

toms.

Acknowledgements. We are grateful to T. Hartmann and D.

Hornes for logistic support in the animal keeping facility; M.

Flecks for the advise on photo adjustments; F. Ihlow for her

advice and the introduction to ArcGIS; U. Bott and C. Etzbauer

for the supply with laboratory equipment; Dr. X. Mengual for

the introduction and the permission to work with a special cam-

era setup and L.M. Carilo Filho, E.M.S. Neto, G. Novaes and

M. Solé for their suggestions in a previous revision. We also

thank two anonymous reviewers for their great suggestions to

improve this article. R.A.R. thanks Coordenadoria de Aperfe-

coamento de Pessoal de Nivel Superior (CAPES) for granting a

©ZFMK

220 Benjamin Klein et al.

doctoral scholarship. This study benefited from multiple grants

of the Alexander Koenig Gesellschaft (AKG).

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APPENDIX I.

Different camera settings (1-4) with regard to light intensities

and ISO-Settings.

Setting 1 2 3 4

Light intensity [%] 50 66 80 100

ISO 1600 1600 1600 100

APPENDIX IL.

A brief description of the natural history of the target

species of this study

Ranitomeya amazonica Schulte (1999) is a poison dart

frog placed in the variabilis group of the genus Rani-

tomeya (Brown et al. 2011). The basic color is black, with

a yellowish orange pattern of medial, dorsolateral and

lateral stripes. Frequently, the black component forms a

“Y” on the back, which begins at the anterior margins of

the eyes and ends at the cloaca (Fig. 1, green color code).

The limbs and the ventral side are teal and dotted with

black spots. Known are two widely separate populations

of R. amazonica: east population, distributed in extreme

southern Guyana; eastern French Guiana; region of the

mouth of the Amazon in Brazil and west population,

distributed in northwestern Amazonian Peru (Loreto),

extreme southeastern Colombia (Amazonas) and expect-

ed in the adjacent borderlands of Brazil (Frost 2006). In

the present study we used data from individuals of the

western population (Fig. 1). They inhabit primary and

secondary rainforests, limited to sparse stands of stunted

Bonn zoological Bulletin 69 (2): 191-223

221

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ters S, Veith M (2003) Convergent evolution of aposematic

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215-226

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K. (2008a) The tadpole of the bamboo-breeding poison frog

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66-68

von May R, Catenazzi A, Angulo A, Brown JL, Carrillo J,

Chavez G, Cordova JH, Curo A, Delgado A, Enciso MA,

Gutiérrez R, Lehr E, Martinez JL, Medina-Miller M, Mi-

randa A, Neira DR, Ochoa JA, Quiroz AJ, Rodriguez DA,

Rodriguez LO, Salas AW, Seimon T, Seinom A, Siu-Ting

K, Suarez J, Torres C, Twomey E (2008b) Current state on

conservation knowledge on threatened amphibian species in

Peru. Tropical Conservation Science 1: 376-396

Waldram M (2008) Breeding biology of Ranitomeya biolat in

the Tambopata region of Amazonian Peru. Journal of Herpe-

tology 42: 232-237

Wells KD (2007) The ecology and behavior of amphibians. The

University of Chicago Press, Chicago & London

trees (Lotters et al. 2007). Clutches of two to six eggs

can be found in water filled leaf axils of those bromeliads

(Lotters et al. 2007). Due to continuous doubts concern-

ing the taxonomic validity of R. amazonica, the extent of

its occurrence as well as the ecological requirements are

unknown. Therefore, the IUCN lists this species as data

deficient IUCN 2015). ]

Ranitomeya benedicta (Brown et al. 2008), also known

as blessed poison frog, is placed within the reticulata

group of the genus Ranitomeya (Brown et al. 2011). The

predominant color is black, covered by a blue reticula-

tion. Except for the black spots surrounding the eyes, the

head region is red and extends posterior to the shoulders

(Fig. 1, light blue color code). In some individuals the

black areas around the eyes are medially fused and ex-

tend to the tympanum, forming a “W”-shaped face mask.

Limbs and the ventral side show the same coloration as

the dorsum, whereas the throat region is covered by a

black marbling. They are distributed throughout the low-

land forests of southern Loreto and eastern San Martin,

Peru (Brown et al. 2011). While they primarily occur in

©ZFMK

222

forests which are located 150 m above sea level, some

individuals have been sighted in areas over 315-405 m

elevation (Brown et al. 2008; von May et al. 2008b).

Clutches consist of two to six eggs and can be found

within the leaf litter covering the forest floor (Brown

et al. 2008). Due to an estimated extent of occurrence of

about 19.000 km7?, declining habitats as well as negative

effects of the international pet trade, the IUCN list this

species as vulnerable (IUCN 2015).

Ranitomeya imitator (Schulte 1986), also known as

mimic poison frog, is placed in the vanzolinii group of the

genus Ranitomeya (Brown et al. 2011). There are three

different forms, whereby the study organism was a high-

land form, which is called the variabilis or “two dots”

type. The ground color of the dorsal side is teal, covered

with large black dots. The nostrils are surrounded by two

black dots, which extends to the snout and therefore are

responsible for the name “two dots”. The ventral side is

grayish blue, while the throat is usually yellowish. The

limbs are teal and covered with irregular small black dots.

The “two dots” or highland form is distributed in Cordil-

lera Oriental, the east of the Departamento San Martin,

Peru, 250—1000 m a.s.]. with temperatures fluctuating be-

tween 22—26 °C (Lotters et al. 2007) (Fig. 1). The frogs

usually inhabit moist premontane primary and secondary

forests, but are also able to live along roads or at the mar-

gins of plantations, usually found in vegetation heights

between 0.5 and 1.5 m above the ground (L6tters et al.

2007). Clutches consist of one to two white eggs, which

are placed in a rolled up leaf (Schulte 1986; Brown et al.

2011). Due to its wide distribution range with many suit-

able habitats and large populations, the IUCN list them as

least concern (IUCN 2015).

Ranitomeya reticulata (Boulenger, 1884) is placed

within the reticulata group of the genus Ranitomeya

(Brown et al. 2011). The head and the back are usually

copper red to reddish brown, while the limbs, the lower

sides and the flanks up to the dorsal and sacral region

are covered with irregular sized black spots on a bluish

background (Fig. 1, yellow color code). The species is

distributed throughout the lowland forests of the Depar-

tamento Loreto, Peru, 150—200 m a.s.I to the province of

Pastaza, Ecuador, 200-340 m a.s.l. (Brown et al. 2011).

In the vicinity of Iquitos, Departamento Loreto, the frogs

occur in syntropy to R. amazonica in the “varillales”.

While R. amazonica is more common in moist environ-

ments, individuals of R. reticulata can be found more fre-

quently in dryer ones, where they perched in vegetation

up to 2 m height. In captivity, clutches of one to five eggs

are deposited in dark and horizontal places (Lotters et al.

2007). Due to its wide distribution with presumable large

populations, the IUCN list them as least concern (IUCN

2015).

Bonn zoological Bulletin 69 (2): 191-223

Benjamin Klein et al.

Ranitomeya sirensis (Aichinger, 1991), also known as

the Sira-poison frog, nowadays comprises the two former

species R. biolat and R. lamasi and is placed in the vanzo-

linii group of the genus Ranitomeya (Brown et al. 2011).

The ground color of our breeding group was black, with

an orange pattern that consists of five thin stripes. The

median and the dorsolateral stripes originate anterior to

the margin of the eyes and end at the cloaca and at the

margin of the thighs respectively, while the two lateral

stripes originate at the tip of the snout in between the nos-

trils and end next to the dorsolateral stripes (Fig. 1, blue

color code). Limbs are sage and covered with black spots.

The species is distributed from the Amazonian Basin in

central eastern and south eastern Peru (Departamentos

Loreto, San Martin, Ucayali, Pasco, Junin, Huanuco, Cus-

co, Madre de Dios) to the southern part of Brazil (State

of Acre) and the northern part of Bolivia (Departamen-

to of Pando) (Brown et al. 2011). They usually inhabit

premontane and montane primary and secondary forests

at elevations between 250-1560 m a.s.l. with an annual

precipitation between 1000-7000 mm (Schulte 1999; von

May et al. 2008b; Brown et al. 2011). Depending on the

elevation, the species inhabits bromeliads or bamboo for-

ests, but also tolerates modulated habitats such as coffee

plantations (Lotters et al. 2007). Due to its wide distri-

bution with presumable large populations in combination

with the fact that many habitats are protected, the IUCN

list this species as least concern (IUCN 2015).

Ranitomeya vanzolinii (Myers, 1982), also known as

the Brazilian poison frog, is a member of the vanzolinii

group of the genus Ranitomeya (Brown et al. 2011). The

basic color is black, covered with irregular yellow spots

which are sometimes fused to lines, especially close to the

eyes and at the flanks, or create a marbled pattern at the

ventral side. Limbs are teal and covered with black spots.

The throat is yellow, whereas a wide dark line crosses the

entire width of the posterior part. The species distribution

ranges from central eastern parts of Peru (Departamentos

Loreto, Huanuco and Pasco) to western Amazonian parts

(Estado Acre) of Brazil (Brown et al. 2011) (Fig. 1). They

usually inhabit primary lowland forests at an elevation

between 200—400 m, except one locality which is situated

in the premontane and moist cloud forests between Rio

Pachitea and Rio Ucayali at an altitude of 1300 m (von

May et al. 2008b, Brown et al. 2011). As a tree-dwelling

species, specimens can be found on trunks, branches and

leaves in heights of up to 4 m, or on the ground (L6tters

et al. 2007). Clutches consist of one to two light colored

eggs which are produced by the same pair that regular-

ly spawns together (Caldwell 1997; Brown et al. 2011).

Although the population trend is decreasing, the IUCN

still list them as least concern, because they are widely

distributed and the populations are presumed to be large

enough (IUCN 2015).

©ZFMK

Larval characterization of six poison-dart frogs 225

APPENDIX III.

Measurements of six different species of the genus Ranitomeya. 1. R. amazonica. 2. R. benedicta. 3. R. imitator. 4. R. reticulata.

5. R. sirensis. 6. R. vanzolinii. Measurements were taken from voucher specimens at stage 41, except R. sirensis which was at

stage 29. All measurements are given in millimeters [mm]. Abbreviations: BL=body length; BWE=body width at eye level;

BWN=body with at nostril level; ED=horizontal eye diameter; END=eye nostril distance, IND=internarial distance; [OD =in-

terorbital distance; MBH=maximum body height, MBW=maximum body width, MTH=maximum tail height, ODW=oral disc

width; TAL=tail length; TMH=tail muscle height at base; TMW=tail muscle width at base; TL=total length; RED=rostro-eye

distance, from tip of snout to the center of the eye in lateral view; RND=rostro-nasal distance, from tip of snout to the center of the

nostril in lateral view; RSD=rostro-spiracle distance.

Species 1 2 3 4 5 6

BL 9.38 9.38 9.69 8.38 6.37 9.00

BWE 57 5.00 5.29 4.58 4.33 4.86

BWN 3.14 2.86 3.43 2.96 3.83 3.14

ED Lis 1.00 0.74 0.80 0.55 0.86

END 13 1.00 1.08 1.20 1.06 1.31

IND LSF 1.43 1.43 Loe 1.05 | ees

IOD 3.00 3:57 3.29 2.93 1.74 3,29)

MBH 4.14 4.29 55 3.48 3.87 4.86

MBW 7.00 FRR) 7.14 5.16 5.47 6.86

MTH 371 4.14 4.43 3.07 3.30 4.00

ODW 1.86 2.14 2.14 2.04 Dahed 1.86

TAL 18.29 19:29 17.14 13.79 12.10 16.86

TMH 2.14 27 2.43 1.64 1.69 2.14

TMW pees. 2.43 2.29 1.87 1.60 Za.

TL 27.67 28.67 26.84 2D WT. 18.47 25.86

RED Dd 1.69 2.08 1.79 L335 2.08

RND 0.92 0.69 1.00 237 0.49 0.77

RSD 6.00 5:23 5.92 5.38 3.40 5.46

MBW/BL 0.75 0.78 0.75 0.62 0.86 0.76

RED/BL 0.23 0.18 0.26 0.28 0.24 0.23

ED/BL 0.12 0.11 0.09 0.09 0.09 0.10

RND/RED 0.43 0.41 0.39 0.40 0.32 0.37

IND/IOD 0.52 0.40 0.46 0.53 0.60 0.48

TMW/MBW 0.33 38 0.34 0.36 0.29 0.33

MBH/MBW 0.59 0.59 0.73 0.68 0.71 0.71

TAL/BL ec ss: 2.06 1.83 1.64 1.90 1.87

TAL/TL 0.66 0.67 0.65 0.62 0.66 0.65

TMH/MTH 0.58 0.62 0.49 O53 0.51 0.54

TMW/MBW 0.33 0.33 0.34 0.36 0.29 0.33

ODW/MBW OF 0.29 0.31 0.40 0.39 0.27

RSD/BL 0.64 0.56 0.56 0.64 0.53 0.61

BWN/BWE 0.56 0.57 0.65 0.65 0.88 0.65

Bonn zoological Bulletin 69 (2): 191-223 ©ZFMK

BHL

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Bonn zoological Bulletin 69 (2): 225-247

2020 - Wagner T.

https://do1.org/10.20363/BZB-2020.69.2.225

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:B7F64F 10-0047-4E2B-86FF-AC61F1B55D26

Revision of Monolepta Chevrolat, 1836 species

from North-East Africa

(Coleoptera: Chrysomelidae: Galerucinae)™

Thomas Wagner" *

' Universitat Koblenz-Landau, Institut fiir Integierte Naturwissenschaften - Biologie, Universitdtsstr. 1,

D-56070 Koblenz, Germany

“Corresponding author: Email: thwagner@uni-koblenz.de

'urn:lsid:zoobank.org:author:6A F65C9C-246B-41CA-B326-2D93C427CCD1

“VII. part of the revision of Afrotropical Monolepta

53. contribution to the taxonomy, phylogeny and biogeography of the Galerucinae

Abstract. Here, the species of Monolepta Chevrolat, 1836 from North-East Africa are taxonomically revised. From this

region, covering the states of Egypt, Sudan, South-Sudan, Ethiopia, Eritrea, Djbouti and Somalia, 15 species are known,

seven of them: M. Jongiuscula Chapuis, 1879; M. postrema Chapuis, 1879; M. euchroma Fairmaire, 1883; M. nigropicta

Laboissiere, 1938; M. marginethoracica Laboissi¢ere, 1940a; M. nigrocruciata Laboissiere, 1940b; and M. gobensis La-

boissiere, 1940b are endemic to the Highlands of Ethiopia and Eritrea. Further eight species occur in the region, but have

wider distribution in Africa: M. cruciata Guérin de Méneville, 1847; . lepida Reiche, 1858; M. vincta Gerstaecker, 1871;

M. vinosa Gerstaecker, 1871; M. ephippiata Gerstaecker, 1871; M. citrinella Jacoby, 1899; M. leuce Weise, 1903; and

M. jeanneli Laboissiere, 1920 with M. kiwuensis Weise, 1924 as new synonym. Some species have been revised before,

and then only additional collecting data are given here. Monolepta longiuscula, M. postrema and M. nigropicta are revised

for the first time. Next to detailed redescription of these species, distribution maps and an identication key are given for

all species.

Key words. Taxonomy, revision, lectotype designation, synonymy, Africa, Afrotropical Region, Ethiopian Highlands,

distribution map, identification key.

INTRODUCTION

In the last catalogue of the Galerucinae (Wilcox 1973),

180 species of Monolepta Chevrolat, 1836 from tropi-

cal Africa were listed. Most of these species have been

described between 1890 and 1950 (Wagner 2017). With

very few exceptions, the descriptions by preceeding au-

thors were based on external characters only. The alloca-

tion to Monolepta and other genera of the “Monoleptites”

(Wilcox 1973) was mostly typological. In an ongoing

revision of this group, the Afrotropical species of Mono-

lepta turned out as polyphyletic, and many species have

to be transferred to other groups in the meantime (Wagner

2004, 2017).

After revision of the generotype of Monolepta, Mono-

lepta bioculata (Fabricius, 1781), and a redefinition of

Monolepta (Wagner 2007a), seven parts on the taxonomic

revision of afrotropical “true” Monolepta have been pub-

lished, six parts according to “coloration types” (Wagner

2000a, b; 2001, 2002, 2003, 2005, 2007b), one with focus

of the specific fauna of Namibia (Wagner 2016).

Received: 21.02.2020

Accepted: 10.09.2020

Another peculiar fauna of these beetles with high en-

demism is found in North-East Africa, in particular in the

Ethiopian Highlands. Seven species are endemic to the

states of Ethiopia and Eritrea, further eight species occur

in both countries and the adjacent states of Egypt, Sudan,

Djibouti and Somalia, but have also a wider distribution

in Africa. Some of these species been already revised in

other parts of the revisions cited above, and here only the

diagnosis and an update of collection and distributional

data are given. Some of the endemic species are revised

here for the first time, including figures on external and

genitalic patterns. An identification key for all Monolepta

species from North-East Africa is given.

MATERIAL AND METHODS

A standard set of figures is given for each species. These

include illustrations of the coloration (dorsal view), in-

cluding the right antenna, where black coloration is indi-

cated by black, yellow coloration by white, and red color-

ation by dot-shading. In polymorphic taxa more than one

Corresponding editor: D. Ahrens

Published: 27.10.2020

226

coloration type is figured. Note that usually also transi-

tions between the given coloration types occur, 1. e., that

only typical and frequently found coloration types are

illustrated, but there might be more in some species. The

basal four antennomeres of usually two different males

and females, dorsal and lateral view of the median lobe

including the endophallic structures, and ventral view of

the median lobe without the endophallic structures (for

classification see Wagner 2000a), the spermathecae of

two (if available) different females, and bursa-sclerites

of one female are figured. Morphometric measurements

were made for external characters. Absolute measure-

ments are: total length from the clypeus to apex of the

elytron, length of elytron, maximal width of both elytra

(usually in the middle or posterior third of the elytra), and

width of pronotum. Relative measurements are: length

to width of pronotum, maximal width of both elytra to

length of elytron, length of second to third antennom-

ere, and length third to fourth antennomere. The number

of specimens measured is given in the description un-

der “total length”. If not stated otherwise, lectotypes are

herein designated in order to fix the species identity and

to preserve the stability of nomenclature in these taxa

according to arcticle 74.7.3. of the Code on Zoological

Nomenclature.

The subsequent redescriptions and descriptions are

based on labelled specimens from the following collec-

tions. Acronyms used and responsible curators in brack-

ets: Bishop Museum, Honolulu (BPBM; A. Samuelson);

Natural History Museum, London (BMNH; M. Geiser,

M. Barclay); Brigham Young University collection, Pro-

vo, Utah (BYUC; Shawn Clark); private collection Ron

Beenen, Nieuwegein, The Netherlands (CBe); private

collection Jan Bezdek, Brno, Czech Republic (CBz); pri-

vate collection Anthony Drane, UK (CDr); private col-

lection Uwe Heinig, Berlin, Germany (CHe); private col-

lection Frantizek Kantner, Budéjovice, Czech Republic

(CKa); private collection Lev Medvedev, Moscow, Rus-

sia (CMe); Hungarian Museum of Natural History, Bu-

dapest (HNHM,; O. Merkl); Institute Royal des Sciences

Naturelle de Belgique, Brussels (IRSN; P. Limbourg);

Museo Civico di Storia Naturale, Genova (MCGD; R.

Poggi); Museo Civico di Storia Naturale, Trieste (MCST;

A. Colla); Museo ed Instituto di Zoologia Sistematica,

Universita di Torino (MIZT; M. Daccordi); Musée Na-

tional d’Histoire Naturelle, Paris (MNHN; A. Mantill-

ier1); Museum ftir Naturkunde, Berlin (MNHB; J. Frisch,

J. Willers); Musée Royal d’Afrique Centrale, Tervuren

(MRAC; M. de Meyer); Museum of Zoology, Helsinki

(MZHF; H. Silfverberg); Museo Zoologico “La Speco-

la”, Firenze (MZUF; L. Bartolozzi); Naturhistorisches

Museum Basel (NHMB; E. Sprecher-Ubersax); Naturhis-

torisches Museum Wien (NHMW; H. Schillhammer);

Naturhistoriska Riksmuseet, Stockholm (NHRS; J. Berg-

sten); Natuurhistorisch Museum Leiden (NNML; R. de

Jong); Senckenberg Deutsches Entomologisches Institut,

Bonn zoological Bulletin 69 (2): 225—247

Thomas Wagner

Eberswalde (SDEI; L. Behne); National Museum of Na-

tional History, Washington (USNM; A. Konstantinov);

Zoologisches Forschungsinstitut und Museum Alexander

Koenig, Bonn (ZFMK; D. Ahrens, K. Ulmen); Zoologi-

cal Institute St. Petersburg (ZISP; A. Kirejtshuk); Zoolo-

gisches Institut und Zoologisches Museum der Universi-

tat, Hamburg (ZMUH; M. Husemann).

RESULTS

Species endemic to Ethiopia and Eritrea

Monolepta longiuscula Chapuis, 1879

(Figs 1—2)

Monolepta longiuscula Chapuis, 1879: 23.

Type material. Ho/otypus. Female, “Abyss., Raffray /

Regione boschiva da Goundet ad Adoua, 1000—2000m,

1873 / 5/8“ (MCGD). There is no information on speci-

men numbers in the original description, and I treat the

only available specimen as holotype.

Further material studied. 9 specimens, 5 findings. Er-

itrea. 2 ex., Asmara, 15.00N/38.56E (IRSN, MNHB):

3 ex., Adi-Caie, 14.50N/39.21E, [X.1902, A. Andreini

(MZUF). — Ethiopia. 2 ex., Abyss., Raffray, coll. G. Al-

lard (MNHN); 2 ex., Adigrat, 14.16N/39.27E, V.1963,

Linnavuori (MZHF).

Redescription. Total length. 4.00-4.80 mm (mean:

4.60 mm; n= 6).

Head. Yellowish-red to red, vertex contrasting black,

labrum red, labial and maxillary palpi yellow. Antennae

entirely yellow to reddish-yellow, last two to three anten-

nomeres more brownish, not contrasting black (Fig. 1A).

Antennomeres slender, second and third in males signifi-

cantly broader (Fig. 2A), second and third antennomeres

usually of same length, length of antennomeres two to

three 1.00-1.14 (mean: 1.07), length of antennomeres

three to four 0.32—0.42 (mean: 0.37).

Thorax. Prothorax entirely yellowish-red (Fig. 1A),

pronotum small and broad, pronotal width 1.10—1.40 mm

(mean: 1.26 mm), pronotal length to width 0.60—0.64

(mean: 0.63), very finely punctured, shining. Elytral col-

oration predominantly yellow, elytral base, humerus, first

third of outer margin including epipleura, and about one

third of suture black, with slight subapical enlargement

of the black sutural patch (Fig. 1A). Elytra very slender,

elytral length 3.00—4.10 mm (mean: 3.60 mm), width of

both elytra 1.90—2.50 mm (mean: 2.23 mm), with width

of both elytra to length of elytron 0.62—0.70 (mean: 0.66).

Scutellum red or black. Meso- and metathorax yellowish,

legs yellow to reddish-yellow.

Abdomen. Black, strong contrasting to the yellowish

underside of thorax (Fig. 1A).

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 227

Fig. 1. Monolepta longiuscula Chapuis, 1879. A. Colour pattern. B. Basal antennomeres, males. C. Dto., females. D. Median lobe,

a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Two different spermathecae. F. Bursa-sclerite, dorsal. G. Dto.,

ventral.

Male genitalia. Median lobe slender, conical, signifi-

cantly narrowed in the apical quarter, with broad and flat

apex (Fig. 1D), straight and sometimes with fine setae

(Fig. 1Da). Tectum broad, pointed at apex (Fig. 1Db),

ventral groove slender, nearly parallel sided (Fig. 1Dc).

Lateral endophallic spiculae short, small and characteris-

tically twisted, median spiculae thin and slender, ventral

spiculae large with one hook (Fig. 1Db, Dc).

Female genitalia. Spermatheca with small spherical

nodulus, slender middle part and long cornu (Fig. 1E).

Dorsal part of bursa sclerites slender, sub-triangular

(Fig. 1F), ventral part slender triangular, outer margin

finely undulate (Fig. 1G).

@ 3

M. euchroma

e@ 1-4

@ 5-15

M. jeanneli

Fig. 2. Distribution of 4 longiuscula, M. euchroma, M. jean-

neli, M. cruciata.

Bonn zoological Bulletin 69 (2): 225—247

Diagnosis. In size and body shape most similar to

M. vincta and M. ephippiata. Monolepta vincta with re-

duced transverse elytral band does not occur in North-

East Africa, while the most dominant coloration type

is with particular broad band (Fig. 15Ac, Ag), median

lobe at apex more broad and flat in M. /ongiuscula, dor-

sal endophallic spiculae of other type (Figs 1D, 15D).

Monolepta ephippiata with somewhat similar dorsal col-

oration (Fig. 13Ab), but than at least with median elytral

spot, median lobe very different with narrow and point-

ed apical part and very different endophallic armature

(Figs 1D, 13D).

Distribution and ecology. An obviuously very rare spe-

cies collected in the surroundings of Asmara in Eritrea

and few adjacent locations of Ethiopia, partly without

detailed location data (Fig. 2).

Monolepta postrema Chapuis, 1879

(Figs 3-4)

Monolepta postrema Chapuis, 1879: 22.

Type material. Lectotype. Male, “Abyss. Raffray /

Monolepta postrema Chap. / additional label (added

later): Regione boschiva da Goundet ad Adoua, 1000—

2000 m, 1893 / Museo Civico di Genova / Lectotypus

Monolepta postrema Chapuis, 1879” (MCGD). This des-

ignation. Chapuis mentioned several specimens in his

original publication without designation of a holotype:

“De Scio; récolée par M. Antinori a Lit Marefia, en Mai,

et a Mahal Uonu en Septembre. Trouvée aussi par M.

Raffray entre Goundet et Adoua”.

©ZFMK

228 Thomas Wagner

Fig. 3. Monolepta postrema Chapuis, 1879. A. Colour pattern, B. Basal antennomeres, males. C. Dto., females. D. Median lobe,

a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Two different spermathecae. F. Bursa-sclerite, dorsal. G. Dto.,

ventral.

Paralectotypes. 1 female, same data as lectotype

(MCGD), 2 females, Scioa, Lit-Marefia, V.1877, Antino-

ri (MCGD).

Further material examined. 260 specimens, 54 find-

ings. Eritrea. 1 ex., Erythree (ZMUH); 1 ex., Asmara,

15.00N/38.56E (MNHN); 1 ex., dto. (HNHM); 2 ex., dto.

(NHMW); 4 ex., dto., Chéren, coll. Clavareau (MRAC);

2 ex., dto., Staudinger, ex coll. J. Weise (MNHB); | ex.,

TX.1905, N. Baccari (MCGD); 4 ex., Umg. Asma-

ra, VII.2001, L. & M. Stalmans (IRSN); 5 ex., Ghin-

da, 15.20N/38.56E (2 ex. MNHB, 1 ex. NMNH, 2 ex.

NHRS); 2 ex., Adi-Ugri, 14.53N/38.49E, VIII.1901,

TX.1902, A. Andreini (MZUF). — Ethiopia. 5 ex., Raffray

(MNHN); 2 ex., coll. Chapuis (IRSN); 3 ex., Bogos, coll.

Duvivier / Kraatz (2 ex. IRSN, 1 ex. SDEI); 7 ex., Ab-

yssinie, 1881, Raffray (MNHN); 2 ex., Abyssinia, 1928,

Mrs. G. McCreag (USNM); 2 ex., Alitiéne, coll. Kraatz

(SDEI); 6 ex., Tigre, 1850, Schimper (MNHN); 2 ex.,

Abyssinia, Tschtscher, VI.1911, Kovacs (HNHM); | ex.,

Das, X.1911, R. J. Storley (BMNH); 2 ex., Scioa, Let.

Marefia, 6.50N/35.56E,1881 / VII.1897, Antinori / Raga-

ZZ1 (MCGD); 3 ex., Addis Abeba, 9.02N/38.42E (ZISP);

6 ex. coll. Le Moult (ZMUH); 33 ex., Dr. Schirhof

(MNHB),; 1 ex., 1899, Sason (ZISP); 1 ex., VI.1905, M.

de Rothschild (MNHN); 1 ex., [X.1926, J. Omer-Coo-

per (BMNH); 32 ex., 1928, Schtirhoff (MNHB); 65 ex.,

1930, Schtirhoff (MNHB); 5 ex., VIT—-IX.1933, L. Saska

(NHRS); 4 ex., X.1948, II.1949, “in flowers of garden

roses”, H. Scott (BMNH); 1 ex., Taddese Bogale, V.1956

(USNM); 12 ex., VIII.1963, P. M. Schroeder (NMNH);

4 ex., 2400 m, II.1967, G. M. Shitaye (BMNH); 5 ex.,

Bonn zoological Bulletin 69 (2): 225—247

11.1972, H. Silfverberg (MZHF); 1 ex., VIII. 1988, L. Med-

vedev (CMe); 1 ex., 2500 m, X.1990, L. N. Medvedev

& E. Samoderzhenkov (CMe); 1 ex., I.1995, Bastianini

(MIZT); 2 ex., near Adis Allem, 9.01N/38.24E, 2600 m,

1X.1926, H. Scott, “cultivated country” (BMNH); 1 ex.,

Djem-Djem Forest, 2800 m, IX.1926, H. Scott “from

grassy open space” (BMNH); 4 ex., Shoa, Wachacha Ra-

vine near Addis Abeba, 2700 m, [X.1926, H. Scott, “from

native shrub” (BMNH); 2 ex., between Djem-Djem and

Wouramboulchi, 3000 m, X.1926, J.O. Cooper (BMNH);

2 ex., Simien, Derasghie, 3200 m, XII.1952, H. Scott,

“from flowering trees & busches” (BMNH); 1 ex., Belle-

ta Forest, 7.32N/36.31E, VI.1963, Linnavuori (MZHF);

1 ex., Agheresalam, 6.29N/38.21E, VI.1963, Linnavuori

Fig. 4. Distribution of M. postrema, M. leuce.

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa

(MZHF); 2 ex., Ambo, 7.32N/36.31E, VI.1977, L. Med-

vedev (CMe); | ex., Akaki River, 8.50N/38.43E, XI.1980,

sweep-netting, A. Demeter (HNHM); | ex., Mt. Menage-

sha, 8.55N/38.35E, X.1980, sweep-netting, A. Deme-

ter (HNHM); 2 ex., Shewa, 6.58N/35.46E, 1986-1990,

Ing. Dedoch (CBz); 1 ex., Debre Zeyt, 10.35N/35.48E,

V.1989, K. Werner (MZUF); 1 ex., Ambo/Guder, 2400 m,

VII.1990, K. Werner (MZUF); 2 ex., Arsi, Wondo Gen-

et, 7.30N/39.30E, 1850 m, VI.1990, K. Werner (MZUF):

5 ex., Ambo, 650 m, XI.—X.1990, L. Medvedev (CMe);

3 ex., Kaffa Pr., 1850 m, 40 km W Bonga, IV.2007, J. Ha-

lada (NME); 1 ex., Amhara Region, Debre Tabor, Debre-

sena, 11.51N/37.59E (BYUC); 2 ex., Oromia reg., Hirna,

9.15N/41.08E, 2315 m, V.2011, V. Hula & Niedobova

(CBz).

Redescription. Total length. 4.80-5.60 mm (mean:

5.20 mm; n= 16).

Head. Labrum and frons yellowish, frons sometimes

brownish, vertex always black (Fig. 3A), labial and max-

illary palpi yellow, terminal palpomeres often brownish.

Antennae yellow, usually only last antennomere with

brownish to black tip (Fig. 3A). Antennomeres slender,

second and third in males significantly broader (Fig. 3B),

second and third antennomeres usually of same length,

length of antennomeres two to three 0.94—-1.15 (mean:

1.02), fourth antommomere usally three times onger than

third, length of antennomeres three to four 0.33-0.42

(mean: 0.37).

Thorax. Prothorax entirely yellow, pronotum pale

yellow, broad, pronotal width 1.40-1.55 mm (mean:

1.48 mm), pronotal length to width 0.58—0.62 (mean:

0.60), very finely punctured, shining. Elytral coloration

characterictic and of constant type, predominantly yel-

low, black at base, black colour elongated about the first

third of the elytra laterally including epipleura and trian-

gle-like along the suture, apical part black (Fig. 3A). Ely-

tral length 3.80—4.40 mm (mean: 4.11 mm), width of both

elytra 2.40—2.80 mm (mean: 2.58 mm), slender, width of

both elytra to length of elytron 0.59-0.67 (mean: 0.63).

Scutellum brownish-red to black. Meso- and metathorax

yellow, as legs.

Abdomen. Entirely yellow in about one third of mate-

rial examined, but mostly yellow with contrasting black

anal-sternite and pygidium, rarely also other abdominal

segments with darker outer margin.

Male genitalia. Median lobe broad, homogenous-

ly conical (Fig. 3Db, Dc), apex slightly bent dorsally

(Fig. 3Da). Tectum small, conical (Fig. 3Db), ventral

groove very broad (Fig. 3Dc). Lateral endophallic spicu-

lae short, broad, claw-like, median spiculae and slender,

ventral spiculae large, comb-like (Fig. 3Db).

Female genitalia. Spermatheca with small spherical

nodulus, broader and long middle part and long cornu

(Fig. E). Dorsal part of bursa sclerites slender, sub-trian-

Bonn zoological Bulletin 69 (2): 225—247

229

gular (Fig. F), ventral part triangular, outer margin finely

undulate (Fig. G).

Diagnosis. Very characteristic by the black basal elyral

coloration that is elongated trianguarly along the suture.

This species shows very low variation in color pattern

and can be only dismissed in this respect with Bicolor-

izea cavidorsis (Fairmaire, 1893), that occur sympatri-

cally and is widely distributed in Ethiopia (Heunemann

et al. 2015). Also the broad conical aedeagus is a rare

pattern in African Monolepta species.

Distribution and ecology. Widely distributed and abun-

dant in Ethiopia and Eritrea, particularly in montane re-

gions, recorded up to 3200 m (Fig. 4).

Monolepta euchroma Fairmaire, 1883

(Figs 2, 5)

Monolepta euchroma Fairmaire, 1883: 111.

Further material examined. Ethiopia. 19 specimens, 4

findings. 2 ex., Addis Abeba, Neri, 1941 (USNM); 15 ex.,

Addis Abeba, 9.01S/38.45E, “roses”, [X.1963, P. M.

Schroeder (USNM); | ex., Bale, 6.40N/39.40E, [X.2000,

P. Leonard (IRSN); 1 ex., Kaffa Pr., 1850 m, 40 km W

Bonga, 7.16N/36.04E, IV.2007, J. Halada (NME).

Remarks. A detailed redescription was published in

Wagner (2007b). Next to the two type specimens from

“Abyssinie A. Raffray Voy. 1881” (MNHN), only ten

specimens have been studied of this obviously rare spe-

cies (Wagner 2007b).

Diagnosis. External and genital characters of this large

species are most similar to M. vinosa which is obviously

phylogenetically closely related. Both species occur sym-

patrically in the Ethiopian Highlands whereas M. vinosa

has a much wider distribution covering most regions of

the Afrotropis. However, there are some constant differ-

ences in detail between both species. The elytral pattern

of M. euchroma is dominated by the black transverse

bands (Fig. 5A), with elytral apex always black but not

red margined like in M. vinosa with similar predominant-

ly black elytra (Fig. 16A). The female genitalic morphol-

ogy (spermathecae and bursa sclerites, Figs SE-G, 16E—

G) of both species are not clearly distinguishable, but the

median lobe of M. euchroma is more slender, the ventral

groove is narrow, and lateral endophallic spiculae have a

small apical enlargement (Fig. 5D), but not hammer-like

as in M. vinosa (Fig. 16D).

Distribution and ecology. Only known from few mon-

tane sites in the Ethiopian Highlands (Fig. 2).

©ZFMK

230 Thomas Wagner

Da Db Dc

Fig. 5. Monolepta euchroma Fairmaire, 1883. A. Colour pattern. B. Basal antennomeres, males. C. Dto., females. D. Median lobe,

a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

Monolepta nigropicta Laboissiére, 1938

(Figs 6-7)

Monolepta nigropicta Laboissiere, 1938: 146.

Type material. Lectotype. Female, “Da Sancurar agli

Amarr, IV.1896, Bottego leg.” (ZMUH); paralectotype:

1 female, “Neghelli, Marzo, 1937; Miss. E. Zavattari nei

Borana A. O. I.” (MCST). This designation. Laboissiere

mentioned two specimens in his original description

without designation of a holotype “Borana Galla: Sancu-

rar (Bottego 1896), un exemplaire, ma collection; Neghe-

Ili, un exemplaire, Zavattari leg. (MCST)*. Type locality:

Ethiopia, Neghelli, 5.30N/39.05E.

Further material examined. Ethiopia. | ex., Ethiopie,

Sidamo Prov., 14/32 km E of Neghelli, 1600 m, V.1974,

R. O. S. Clarke leg. (MRAC).

Redescription Total length. 4.60-5.40 mm (mean:

4.90 mm; n= 3).

Head. Yellow, vertex contrasting black (Fig. 6A), an-

tenna yellow, only terminal antennomere slightly darker,

antennomeres slender, length of antennomeres two to

three 0.83—0.86 (mean: 0.84), length of antennomeres

three to four 0.42—0.50 (mean: 0.45).

Thorax. Prothorax yellow, broad, pronotal width 1.50—

1.65 mm (mean: 1.58 mm), pronotal length to width

0.58—0.62 (mean: 0.60), very finely punctured, shining.

Elytra predominately yellow, with narrow black base, an-

Bonn zoological Bulletin 69 (2): 225—247

terior half of the outer margin, about on ethird along the

suture and he elytral tip black (Fig. 6A). Elytral length

3.60-4.20 mm (mean: 3.83 mm), width of both elytra

2.30—2.50 mm (mean: 2.40 mm), elytra slender, width of

both elytra to length of elytron 0.62—0.68 (mean: 0.63).

Scutellum brown to black. Meso- and metathorax, and

legs yellowd.

Abdomen. Yellow, analsternite and pygidium black.

Male genitalia. Median lobe broad, slightly narrowed

in the apical quarter (Fig. 6Da), apex broad, flat and

straight (Fig. 6Db), tectum broad, ventral groove slender

(Fig. 6Dc). Lateral endophallic spiculae slender, bifur-

cate, median spiculae and slender and bent dorsally, ven-

tral spiculae large with one strong hook (Fig. 6Da, Db).

Female genitalia. Spermatheca with small spherical

nodulus, slender middle part and long cornu (Fig. E).

Dorsal part of bursa sclerites broad, spiny (Fig. F), ven-

tral part slender, outer margin finely serrate (Fig. G).

Diagnosis. In coloration, size and body shape most sim-

ilar to some specimens of M. cruciata (Fig. 9Ab) and

M. nigrocrucita (Fig. 13Ab) but not with completely

black outer margins. Shape of aedeagus, with broad and

flat apical part very different from both other species with

slender and conical apical part (Figs 9D, 13D). Some-

what similar to small 1 euchroma or M. vinosa, but

those species with partly red elytral coloration, slightly

different aedeagus, and very different shape of sperma-

theca which is slender and long in M. nigropicta, and

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 231

Fig. 6. Monolepta nigropicta Laboissiere, 1938. A. Colour pattern. B. Basal antennomere, male. C. Dto., female. D. Median lobe,

a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

broad with short middle part in M. vinosa and M. euchro-

ma (Figs 5E, 16E).

Distribution and ecology. Only three specimens are

known of this obviously very rare species in Ethiopia

(Fig. 7).

M. marginethoracica | *

@® 1-3

@® 4-16

M. mgt

Fig. 7. Distribution of 4 marginethoracica, M. nigropicta,

M. vincta, M. lepida.

Bonn zoological Bulletin 69 (2): 225—247

Monolepta marginethoracica Laboissiére, 1940

(Figs 2, 8)

Monolepta marginethoracica Laboissiere, 1940a: 131.

Remarks. A detailed redescription was published in

Wagner (2007b). Next to lecto-, and paralectotype “Adi

Ugri Eritrea VII / Musée du Congo Erythrée: Adi Ugri

Coll. Clavareau / V. Laboissiere det. 1940: Monolepta

marginethoracica m. Type / R. Det. C 4344” (MRAC),

28 specimens have been revised in Wagner (2007b) and

no further specimens have been found afterwards.

Diagnosis. In coloration, external morphometrics and an-

tennal characters most similar to M. clienta, but M. mar-

ginethoracica is on average larger, and has usually com-

pletely black margined elytra, whereas the elytral apex of

M. clienta is red. Both species are allopatrically distrib-

uted and can be clearly distinguished by the male genital

morphology (Fig. 7D). In size and male genital structures

somewhat similar to M. vinosa, but can be easily distin-

guished by the entirely black margined elytra (Fig. 7A).

Distribution and ecology. Only known from few mon-

tane sites in Eritrea and Ethiopia. Occurs at the type local-

ity together with M. Jongiuscula Chapuis, 1879, M. pos-

trema Chapuis, 1879, and M. nigrocruciata Laboissiere,

1940 (Fig. 2).

©ZFMK

232 Thomas Wagner

Db De

Fig. 8. Monolepta marginethoracica Laboissiere, 1940a. A. Colour pattern. B. Basal antennomere, male. C. Dto., female. D. Medi-

an lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

Monolepta nigrocruciata Laboissiére, 1940

(Figs 9-10)

Monolepta nigrocruciata Laboissiere, 1940b: 7.

= Monolepta varians Weise, in litteris,; Wagner 2007b:

141.

Further material examined. 6 specimens, 2 findings.

Eritrea. 3 ex., Eritrea, Umg. Asmara, VII.2001, L. & M.

Stalmans (IRSN). — Ethiopia. 3 ex., Addis Abeba, En-

tono Hill, 9.05N/38.45E, 2840 m, V.2011, Hula & Nie-

dobova (CBz).

Remarks. A detailed redescription was published in Wag-

ner (2007b). Next to holo-, and 21 paratypes from “Ethi-

opi Goba R. de Meulenaere 1934—1935 / V. Laboissiere

det., 1940: Monolepta nigrocruciata m. Type / Mus. Hist.

Nat. Belg. I.G. 10.738 / cf. Bull. Mus. Hist. Nat. Belg.

XVI. 1940 n° 23, p. 7-8, fig. 1 d“ (RSN), 468 specimens

have been studied in Wagner (2007b).

Diagnosis. Specimens without elytral cross are most sim-

ilar to the sympatric M. gobensis. The latter has a black

pronotum, while specimens of MZ. nigrocruciata without

elytral cross and black pronotum are very rare. Further-

more, M. nigrocruciata has a broader pronotum (pronotal

length to width 0.57-0.63; M. gobensis 0.62—0.67) and

more slender elytra (width of both elytra to length of ely-

tron 0.62-0.69; M. gobensis 0.66—0.71). In any doubtful

cases dissection of median lobes and bursa sclerites al-

low a clear identification of these species in both sexes

Bonn zoological Bulletin 69 (2): 225—247

(Figs 9D-—G, 11D-G). Most similar to M. nigrocruciata

are some specimens of M. cruciata which is also widely

distributed in Ethiopia and Eritrea. Monolepta nigrocru-

ciata 1s significantly more slender than M. cruciata, but

all measured parameters show a more or less wide over-

lap. Specimens with complete elytral cross (Fig. 9Ac,

Ad) should be checked by genital dissection (Figs 9D,

13D-E).

Distribution and ecology. An obviously abundant and

widely distributed species of the Ethiopian Highlands

and surrounding areas in Eritrea and Ethiopia up to

3300 m (Fig. 10).

Monolepta gobensis Laboissiére, 1940

(Figs 11-12)

Monolepta gobensis Laboissiere, 1940b: 8.

Further material examined. 2 specimens, 2 findings.

1 ex., Ethiopia, Arussi Prov., Gobe, 10.VIII.1970, S.

Persson (NHRS); 1 ex., Oromia, Mt. Enkuolo, NE slope,

7.24N/39.22E, XII.2016, J. Schmidt (NME).

Remarks. A detailed redescription was published in

Wagner (2007b). Next to female Holotype “Ethiopie

Goba R. de Meulenaer 1934-1935 / V. Laboissieére det.

1940: Monolepta gobensis m.” (IRSN) Laboissiere des-

ignated 42 paratypes (all IRSN). 62 specimens listed in

Wagner 2007b).

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 233

Fig. 9. Monolepta nigrocruciata Laboissiere, 1940b. A. Four different colour patterns. B. Basal antennomeres, males. C. Dto.,

females. D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal.

G. Dto., ventral.

Fig. 10. Distribution of M. citrinella, M. nigrocruciata.

Bonn zoological Bulletin 69 (2): 225-247

Diagnosis. Colour pattern without elytral black cross is

most similar to M. deleta, in particular to specimens from

the Usambaras with brownish to black prothorax. Both

species occur allopatrically and M. de/eta particularly in

montane regions of Uganda, Kenya and Tanzania. Spec-

imens with elytral cross are very similar to some M. ni-

grocruciata with black prothorax (Fig. 9Ad) that can

occur syntopically in Ethiopia. Male genitalia should be

dissected in specimens with this coloration to ensure a

correct species identification (Figs 9A, 11A).

Distribution and ecology. Restricted to the Ethiopian

Highlands in Eritrea and Ethiopia up to 3500 m altitude

(Fig. 12).

©ZFMK

234 Thomas Wagner

Fig. 11. Monolepta gobensis Laboissiere, 1940b. A. Two different colour patterns. B. Basal antennomeres, males. C. Dto., females.

D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto.,

ventral.

M. ephippiata

e 1-3

@ 4-9

@ 10-13

M. gobensis

Fig. 12. Distribution of M. ephippiata, M. gobensis, M. vinosa.

Species with wider distribution in Nort-East Africa

Monolepta cruciata Guérin de Méneville, 1847

(Figs 2, 13)

Monolepta cruciata Guérin de Méneville, 1847: 331.

= Monolepta puncticeps Chapuis, 1879: 23; Wagner

2007b: 95.

= Monolepta ludicra Weise, 1906: 54; Wagner 2007b:

95.

= Monolepta sternalis Weise, 1909a: 213; Wagner 2007b:

96.

= Monolepta notha Weise, 1927: 21; Wagner 2007b: 96.

Bonn zoological Bulletin 69 (2): 225—247

= Monolepta kivuensis Laboissi¢re, 1929: 152; Wagner

2007b: 96.

= Monolepta missis Laboissiere, 1931la: 405; Wagner

2007b: 96.

= Monolepta carmenta Weise, in litteris: Wagner 2007b:

96.

Further material examined. 42 specimens, 23 find-

ings. Angola. 1 ex. (BMNH). — Botswana. | ex.,

Nata, 20.13S/26.11E, XII.1979, C. R. Owen (USNM).

— Ethiopia. 1 ex., Alemaya, 9.23N/41.56E, VI.1965,

A. B. Gurney (USNM). — Kenya. 1 ex. Lake Nak-

uru, 0.28S/36.07E, XI.1896, Dr. Ansorge (USNM);

7 ex., Nairobi, 1.17S/36.50E, XI.1967, C. V. Reichert

(USNM). — Malawi. | ex., Zomba, Upper Shire Riv.,

15.21S/35.18E, V.1896, Rendall (USNM). — Mocam-

bique. 4 ex., Delagoa Bay, 25.58S/32.35E (USNM);:

1 ex., Beira, 19.49S/34.52E (USNM); 2 ex., Louren-

zo Marques, 25.58S/32.25E, 1.1951, N. L. H. Kraus

(USNM). — South Africa. 2 ex., Durban, 29.51S/31.01E

(USNM),; 4 ex., Port Natal, 28.30S/30.30E (USNM); 1

ex, Wellington, 33.38S/18.59E (USNM); 1 ex., Graha-

mstown, 33.17S/26.32E, X.1899, C le Doux (USNM);:

2 ex., Malvern, 26.12S/28.06E, VII.1897 (USNM); 1 ex.,

Warmbad, 24.55S/28.15E, 1.1968, P. Spangler (USNM);

1 ex., Transvaal, Libertas, X.1979, C. R. Owen (USNM).

— Tanzania. 1 ex., Urambo, 5.04S/32.04E, II.1960, I.

A. D. Robertson (BMNH); 1 ex., N-Mara, X.1958, I.

A. D. Robertson (BMNH); 2 ex., 30-60 km NE Mpi-

ka, 11.40S/31.40E, XI.2004, Snizek (NME). — Ugan-

da. 2 ex., Entebbe, 0.05N/32.29E, [X.1972, H. Falke

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 235

(USNM); 3 ex., Dokulo, 1.36N/33.10E, XI.1967, C. V.

Reichart (USNM). — Zambia. | ex., Hillwood, Ikilenge,

11.16S/24.18E, X.2013, Smith et al. (BMNH); 1 ex., Ly-

angu, Liuwa Plain NPO, 14.46S/22.34E, X1.2013, Smith

et al. (BMNH).

Remarks. A detailed redescription was published in

Wagner (2007b, 2016). Type specimens for the valid

name and of M. puncticeps originated from Ethiopia. A

Neotype was designated for Monolepta cruciata in Wag-

ner (2007b). Insect material of the expedition of Th. Le-

febre to Ethiopia was deposited in the MCGD, but type

material of this species could not be found. The precise

description and the excellent figure given in the original

description made an allocation to this species very likely.

However, since another species, the sometimes very sim-

Db Ea Eb

ilarly coloured M. nigrocruciata occur at the type locality

of M. cruciata, it was reasonable to designate a neotype

to fix the species identity. The lectotype of M. puncti-

ceps “Abyss. Raffray / Regione boschiva da Goundet et

Adoua, 1000-2000 m 1873” (MCGD) was designated as

neotype of M. cruciata. Monolepta cruciata is one of the

most abundant and widely distributed species of Mono-

lepta in Africa. Nearly 3000 specimens out of 465 find-

ings have been studied insofar (Wagner 2007b, 2016).

Diagnosis. Specimens with broad black elytral margins,

suture and median transverse band (like Fig. 13Aa) are

very similar to M. elegans. This species has on average

more slender elytra and antennae (Wagner 2007a) is

abundant only in West Africa, occurs up to Gabon and

Angola, and does not occur in North-East Africa. Most

Fig. 13. Monolepta cruciata Guérin de Méneville, 1847. A. Four different colour patterns. B. Basal antennomeres, males. C. Dto.,

females. D. Median lobe, a. lateral, b. dorsal. E. Dto., variation a. lateral, b. dorsal, c. ventral, without endophallic structures. F.

Spermathecae. G. Bursa-sclerite, dorsal. H. Dto., ventral.

Bonn zoological Bulletin 69 (2): 225-247

©ZFMK

236

specimens of M. cruciata in Ethiopia and Eritrea show

colour pattern like Fig. 13Ac, much rarer like Fig. 13Ab.

Specimens with complete black suture (Fig. 13Ac) show

many similarities to some M. gobensis Laboissicre, 1940

and M. nigrocruciata Laboissiere, 1940. Dissection of

male genitalia (Fig. 9D, 11D, 13D) is sometimes neces-

sary for proper identification.

Distribution and ecology. One of the most abundant

species of Monolepta in Eastern, Central and southern

Africa from Eritrea and Cameroon to the Cape (Fig. 2).

Monolepta lepida Reiche, 1858

(Figs 7, 14)

Monolepta lepida Reiche, 1858: 263.

Further material examined. 40 specimens, 13 find-

ings. 4 ex., “Arab.”, Ehrenb., 30391 (MNHB). — Egypt.

1 ex., Gebel Elba, 22.11N/36.21E, VI.1928, coll. Alfieri

(USNM); 1 ex., Oasis Feiran, 28.45N/33.40E, V.1935,

coll. Alfieri (NHMB); 3 ex., Wadi Feran, I—III.1935

Sinai, W. Wittmer (NHMB); 9 ex., Gebel Elba, 1.1933,

III.1938, H. Priesner (NHMB); | ex., Wadi Isla, Bir Tarfa,

S-Sinai, 32.00N/34.18E, V.1940, coll. Alfieri (USNM). —

Jordan. 6 ex., Wadi Schaib, 200 m, XI.1957, J. Klap-

perich (USNM); 1 ex., 5 km N Mabada, 31.46N/35.48E,

IV.1994, Volkovich (USNM). — Oman. 1 ex., Dhofar,

18.00N/54.00E, X.1979, T. B. Larsen (USNM). — Pal-

estine. 2 ex., Jericho, 31.51N/35.27E, IV.1899, Pic

1899 (MNHN); 4 ex., Wadi Aczajot, Engedi Distr.,

31.27N/35.23E, IV.1994, Volkovich (USNM). — Syria.

2 ex., Baly coll. (BMNH). — Yemen. 5 ex., Jabal al Tark,

16.40N/53.05E, X.2005, M. Rejzek (BMNH).

Thomas Wagner

Remarks. A detailed redescription was published in

Wagner (2005). The holotype originates from Jerusalem

(MNHN). 72 specimens out of 26 findings are listed in

Wagner (2005), and further 58 specimens in 28 findings

in Schlich & Wagner (2010).

Diagnosis. Most similar to M. vincta and both species oc-

cur sympatrically in north-east Africa. Including M. mel-

anogaster from southern Africa, these three species are

most likely a monophyletic group within Monolepta that

can be derived from the similarity in external characters,

coloration, and male genital patterns. In comparison to

M. vincta, M. lepida is on average larger, and has reduced

black elytral coloration (Figs 14-15), while syntopic

M. vincta often have broad transverse black elytral bands

and a black head (Figs.15Ae, 15Ag, type of M. alternata

from Ethiopia similar to 15Ac, but with broader trans-

verse black bands).

Monolepta lepida can be distinguished by the elongated

second and third antennomeres (length of second to third

antennomeres: 0.75—0.88, M. vincta: 0.86—1.00; length

of third to fourth antennomeres: 0.46—-0.54, M. vincta:

0.27—0.35) and the narrow pronotum (pronotal length to

width: 0.63—0.67, M. vincta: 0.57—0.64).

Distribution. Most specimens are known from the Ara-

bian Peninsula and this species is the only one from the

Afrotropical Region that reaches the Palaearctic Region

in Israel, Jordan, and Syria. Further few specimens are

recorded from Eritrea, Somalia, eastern Sudan, and

Egypt (Fig. 7).

Fig. 14. Monolepta lepida Reiche, 1858. A. Two different colour patterns. B. Basal antennomeres, males. C. Dto., females. D. Me-

dian lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

Bonn zoological Bulletin 69 (2): 225—247

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 237

Monolepta vincta Gerstaecker, 1871

(Figs 7, 15)

Monolepta vincta Gerstaecker, 1871: 83.

= Monolepta alternata Chapuis, 1879: 23; Wagner 2005:

263.

= Monolepta insignis Weise 1903: 212; Wagner 2005:

263.

= Monolepta sjéstedti Weise, 1909: 212; Wagner 2005:

263.

= Monolepta ugandaensis Laboissiere, 1920a: 52; Wag-

ner 2005: 263.

= Monolepta lusingensis Laboissicre, 1920b: 98; Wagner

20052263.

= Monolepta bouvieri Laboissiere, 1920b: 98; Wagner

2005: 263.

= Monolepta striola Laboissiere, 1920b: 98; Wagner

2005: 263.

= Monolepta consociata Laboissiére, 1920b: 99; Wagner

2005: 264.

= Monolepta rugifrons Laboissiere, 1920b: 99; Wagner

2005: 264.

= Monolepta femoralis Laboissiere 1940b: 66; Wagner

2005: 263.

Further material examined. 160 specimens, 46 find-

ings. Botswana. | ex., Serowe, 22.54S/26.42E, [X.1987,

malaise trap, P. Forchhammer (USNM). — Ethiopia.

1 ex., Wallo Prov., 11.30N/40.00E, V.1957, J. E. Lane

(USNM); 6 ex., Rock Valley nr. Harar, 9.19N/42.8E,

VI.1965, A. B. Gurney, entirely yellow, brownish abdo-

men, male with narrow brownish elytral base (BMNH).

— Ghana. | ex., Akosombo, 8.16N/3.00E, VI.1973, L.

Knutson (USNM). — Ivory Coast. 7 ex., Tai NP, 174 m,

5.50N/7.20W, canopy light, III.2017, Aristophanous et al.

(BMNH); 6 ex., Mt. Tonkoui peak, 7.27N/7.38W, light,

V.2016, Aristophanous et al. (BMNH); 5 ex., Mt. Nim-

ba camp, 7.35N/8.25W, 823 m, V.2016, Aristophanous

et al. (BMNH); 1 ex., Kromambira vill., 8.30N/3.37W,

220 m, VIII.2016, Aristophanous et al. (BMNH); 23 ex.,

Yeale Village, Mt. Nimba, 7.32N/8.25W, IV.2016, Aris-

topahnous et al. (BMNH). — Kenya. 1 ex., Chuyulu

Hills, 2.35S/37.50E, V1I.1938 (USNM); 1 ex., Malindi,

3.13S/40.07E, V.1940, G. W. Jeffery (USNM); 3 ex., Tsa-

vo NP, Kitani Lodge, 3.05S/38.40E, I.1968, Krombein &

Spangler (USNM); 3 ex., Amboseli GR, 2.38S/37.14E,

1.1968, blacklite, Krombein & Spangler (USNM). — Li-

beria. 1 ex., Mt. Coffee, 6.30N/10.39W, V.1897, coll.

O. F. Cook (USNM); 1 ex., Bendiya, 1940, W. M. Mann

(USNM); 1 ex., Cape Mount, 7.10N/11.00W, 1940, W.

M. Mann (USNM); 1 ex., Reputa, 1940, W. M. Mann

(USNM); | ex., Tropita, [X.1952, on Citrus, coll. Blicken-

staff (USNM). — Nigeria. 3 ex., Olokemeji, 7.20N/4.03E,

IV.1936, van Zwaluwenburg & McGough (USNM); 3 ex.,

Ibadan, 7.23N/3.56E, V.1936, van Zwaluwenburg & Mc-

Gough (USNM); 1 ex., Gindiri, 9.34N/9.14E, XII.1968

(USNM); 1 ex., Samaru Lake, 11.09N/7.41E, I.1978,

Bonn zoological Bulletin 69 (2): 225-247

Don & Mignon Davis (USNM); 1 ex., Gashaka Gundi NP,

7. 19N/11.35E, IV.2010 (BMNH). — Sierra Leone. 5 ex.,

Tiwai Island, 7.33N/11.21W, 120 m, VI2016, Takano

etal. (BMNH); 1 ex., Outambi-Kilimi NP, 9.40N/12.10W,

TX.2009, malaise trap, Takano et al. (BMNH); | ex.,

Njala, 8.00N/10.00W, XI.1916, van Zwaluwenburg

& McGough (USNM); 9 ex., Kambana, Moa Riv-

er, 7.33N/11.05W, VI.2016, light trap, Takano et al.

(BMNH); 5 ex., Tiwai Island, Moa River, 7.33N/11.21W,

VI.2016, light trap, Takano et al. (BMNH); 5 ex., Loma

Mountains, 1050 m, 9.11N/11.05W, VI.2016. light trap,

Takano et al. (BMNH). — South Africa. 3 ex., Nysvley,

24 .29S/28.42E, VI.1976, B. Levey (BMNH). — South

Sudan. | ex., Kajokaji, 3.53E/31.40E, IV.1912, gift ex.

MCZ Dupl. Series (USNM); 1 ex., Gilo, 4.02/32.51E,

X.1979, A. L. Armstrong (USNM). — Tanzania. | ex.,

Lake Manyara, 3.36S/35.56E, 1926, Smithsonian Chrys-

ler Exp. (USNM); 5 ex., Est-Usambara, Amani, [X.2003,

Th. Wagner (ZFMK); 26 ex., Kilimamoja, Kibaone,

3.23S8/35.49E, IV.2012, Light trap, Smith & Takano

(BMNH),; 8 ex., Orekeryan, Mt. Longido, 2.43S/36.43E,

VIII.2012, light trap, Smith et al. (BMNH); 1 ex., Git-

ing, Mt. Hanang, 4.24S/35.24E, 1946 m, XI.2011, Smith

& Takano (BMNH); | ex., Mt. Meru NP; 3.14S/36.50E,

IV.2012, Smith & Takano (BMNH); 1 ex., Ndarak-

wal, 3.01S/36.59E, 1310 m, IV.2012, Smith & Takano

(BMNH); 1 ex., Maskati, Nguru Mits., 6.03S/37.29E,

1759m, X.2010, Smith & Takano (BMNH); 7 ex., Mt.

Hanang, 4.24S/35.24E, 2434 m, V.2012, Smith & Takano

(BMNH). — Uganda. 1 ex., Kampala, 0.19N/32.35E,

VI.1940, A. F. J. Gedye (USNM). — Zambia. 2 ex.,

Kalungu, N. of Isoka, 9.41S/32.43E, 1280 m, XI.2016,

Smith et al. (BMNH); | ex., Lukuli River, Manda NP,

12.15S/30.53E, XI.2012, Smith & Takano (BMNH);

1 ex., Nkwali, S. Lungwa, 13.07S/31.44E, X1.2012,

Smith & Takano (BMNH); 3 ex., Greystone, Kitwe,

12.55S/28.14E, 1179 m, XI.2012, Smith & Takano

(BMNH). — Zimbabwe. 2 ex. Malvern, 26.12S/28.06E,

X.1897 (USNM).

Remarks. A detailed redescription was published in

Wagner (2005, 2016). The type specimen of the val-

id name was described from Mombasa, Kenya. One of

the numerous synonyms, Monolepta alternata, was de-

scribed from Ethiopia. It is characterized by the black

head and broad transversal bands (similar to Fig. 15Ac).

One of the most abundant and wide spread species of

Monolepta in Africa. Up to now (Wagner 2005, 2016)

data on 3112 specimens out of 729 findings were studied.

Diagnosis. Monolepta vincta is most similar and very

closely related to M. melanogaster and M. lepida. Both

Species are on average larger, and thus specimens small-

er than 3.8 mm total length belong mainly to M. vincta.

However, there is a high overlap in body size to M. lepi-

da which is sympatric to M. vincta in North-East Africa.

©ZFMK

238 Thomas Wagner

Da Db Dc

Fig. 15. Monolepta vincta Gerstaecker, 1871. A. Seven different colour patterns. B. Basal antennomeres, males. C. Dto., females.

D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E-F. Dto., variations. G. Spermathecae. H. Bur-

sa-sclerite, dorsal. I. Dto., ventral.

Bonn zoological Bulletin 69 (2): 225—247 ©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 239

Next to the male genitalic patterns (Figs 14D, 15D-—-P),

good diagnostic external characters are the lesser elon-

gated second and third antennomeres and the broader

pronotum in M. vincta (details see diagnosis of M. lep-

ida). Other similar species like 1 melanogaster Wiede-

mann, 1823, M. buquetii Chevrolat, 1836, M. sharonae

Wagner, 2005, or M. ronbeeneni Wagner, 2005 occur

only in southern and western Africa.

Distribution and ecology. This species is widely distrib-

uted and abundant in most parts of tropical Africa, but

with increasing rarity in southern Africa (Fig. 7).

Monolepta vinosa Gerstaecker, 1871

(Figs 12, 16)

Monolepta vinosa Gerstaecker, 1871: 83.

= Monolepta haroldi Chapuis, 1879: 22; Wagner 2007:

106.

= Monolepta buraensis Laboissiere, 1920: 52; Wagner

2007: 106.

= Monolepta melanocta Laboissiere, 1931b: 45; Wagner

2007: 106.

= Monolepta neghellia Laboissicre, 1938: 146; Wagner

2007: 106.

= Monolepta huamboensis Laboissiere, 1939; Wagner

2007: 106.

Further material examined. 27 specimens, 10 findings.

Ivory Coast. 2 ex., 25 km N Bouake, 7.50N/5.00W,

X.1971, black light trap, J. A. Gruwell (USNM). — Ken-

ya. | ex., Rabur, 0.08S/34.49E, XI.1967, C. V. Reich-

art (USNM). — Mocambique. 12 ex., Delagoa Bay,

25.58S/32.25E, F. C. Bowditch, gift ex. MCZ Dupl.

Series (USNM); 1 ex., Beira, 19.49S/34.52E, F. Monros

coll 1959 (USNM). — South Africa. 1 ex., Durban,

29.51S/31.01E, F. C. Bowditch, gift ex. MCZ Dupl.

Series (USNM). — South Sudan. 1 ex., Lado Distr.,

Nimule, 3.36N/32.04E, X.1912 (USNM). — Tanzania.

1 ex., Ukiriguru, 2.43S/33.01E, VI.1969, I. A. D. Robert-

son (BMNH). — Uganda. | ex., ,,Lado Distr.“, Wadalai,

2.50N/32.35E, X.1912 (USNM). — Zambia. | ex., 27 km

E of Solwezi, 12.11S/26.30E, XI.2005 (NME); 6 ex.,

Kalungu, N. of Isoka, 9.41S/32.43E, 1280 m, XI1.2016,

Smith et al. (BMNH).

Remarks. A detailed redescription was published in

Wagner (2007b, 2016). Type specimens for the valid

name originated from Northern Tanzania. Two syn-

onyms, Monolepta haroldi “Regione da boschiva Goudet

ad Adoua 1000—2000 m 1873 / Abyss. Raffray“ (MCGD),

coloration similar to Fig. 16Ab, and Monolepta neghellia

“Cotype / Miss. E. Zavattari nei Borana A. O. I. Moralev.

1937” (ZMUH), coloration similar to Fig. 16Aa but with

entirely black head, were described from Ethiopia. Up

to now 1388 specimens out of 262 findings are revised.

Bonn zoological Bulletin 69 (2): 225-247

Diagnosis. Monolepta vinosa is one of the largest Afri-

can Monolepta species (total length 4.3—7.1 mm), and

most specimens with cross-like elytral pattern longer

than 5.5 mm belong to this species. The colour pattern of

extended black elytral base, entirely red suture, a subapi-

cal black spot that is finely reddish margined (Fig. 16Ac)

is very characteristic and allows an easy differentiation

from all other species. Some specimens with reduced

red suture (Fig. 16Ac) are somewhat similar to very few

large M. cruciata and the syntopic M. euchroma. In those

specimens a dissection of the genitalia in both sexes with

characteristic structures allows a clear differentiation

(Figs 5, 13, 16). For more details for M. euchroma see

there.

Distribution and ecology. One of the most abundant

Afrotropical species of Monolepta, mainly from savan-

nahs but also known from forest regions (Fig. 12).

Monolepta ephippiata Gerstaecker, 1871

(Figs 12, 17)

Monolepta ephippiata Gerstaecker, 1871: 84.

= Monolepta sordida Chapuis, 1879: 23; Wagner 2007:

112.

= Monolepta ephippiata var. keniaensis Laboissiere,

1920: 52; Wagner 2007: 112.

= Monolepta leakeyi Bryant, 1953: 866; Wagner 2007:

eee)

= Monolepta turneri Bryant, 1953: 867; Wagner 2007:

Ih:

Further material examined. 22 specimens, 10 find-

ings. Ethiopia. 1 ex., Oromia reg., Lava fields, nr.

Feto, 8.40N/39.29E, 1367 m, V.2011, V. Hula & Nie-

dobova (CBz); 1 ex., Afar, Metahara, 9.10N/39.51E,

1052 m, V.2011, Hula & Niedobova (CBz). — Ken-

ya. 1 ex., Mt. Elgon, Salt Lake Estate, 1.08N/34.40E,

2100 m, 17.XII.1937, A. Holm (NHRS); 1 ex., Nantuki,

0.01 N/37.04E, II.1968, K. V. Krombeim (USNM); 2 ex.,

Umg. Nairobi, XII.1970, Lichtfang, D. Erber (MNHB);

1 ex., Naro Moru, 0.10S/37.01E, VUI.1978, G. Scudder

(BMNH); 5 ex., Lake Naivasha, 0.45S/36.35E, shrub

margin, X.2005 (BMNH). — Tanzania. 1 ex., Lake

Manyara NP, 3.23S/35.52E, X1.2011, Smith & Takano

(BMNH); 8 ex., Orekeryan, Mt. Longido, 2.43S/36.43E,

VIIL.2012, light trap, Smith et al. (BMNH). — Ugan-

da. 1 ex., Kakamega Forest, 0.21N/34.52E, VII.2002

(MNHB).

Remarks. A detailed redescription on base of 94 speci-

mens out of 45 findings was published in Wagner (2007b).

Type locality of the valid name is Lac Jipe in Northern

Tanzania. One synonym from Ethiopia is M. sordida,

Holotype, #, “Abyss. Raffray / 770 / Monolepta sordida

Chp / Typus Monolepta sordida, 1879 / Regione degli

©ZFMK

240 Thomas Wagner

Da Db De

Fig. 16. Monolepta vinosa Gerstaecker, 1871. A. Three different colour patterns. B. Basal antennomeres, males. C. Dto., females.

D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto.,

ventral.

Agaos XI 1873 Dal fiume Méri Taccazé” (MCGD), col-

oration similar to Fig. 17Ad.

Diagnosis. A small and slender body with peculiar ely-

tral pattern (Fig. 17A) characterizes MM. ephippiata and

Bonn zoological Bulletin 69 (2): 225—247

allow a clear differentiation from all other Afrotropical

Monolepta species. The apical half of the elytra is usu-

ally completely yellow with exception of the elytral tip.

Most similar in coloration is the allopatrically distributed

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 241

Fig. 17. Monolepta ephippiata Gerstaecker, 1871. A. Four different colour patterns. B. Basal antennomeres, males. C. Dto., fe-

males. D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal.

G. Dto., ventral.

M. ephippiatoides Wagner, 2001, which is restricted to

southern Africa. It has a more extended black apical el-

ytral coloration, and a reddish head which is contrasting

to the yellow pronotum. It is not closely related since the

genitalic characters of both sexes are very different from

that of M. ephippiata.

Distribution and ecology. Restricted to montane areas

in East and North-East Africa from Ethiopia through

Kenya towards northern Tanzania and Rwanda (Fig. 12).

Very abundant in the Rift Valley and the Central Province

of Kenya.

Monolepta citrinella Jacoby, 1899

(Figs 10, 18)

Monolepta citrinella Jacoby, 1899: 375.

= Monolepta michaelseni Weise, 1914: 265; Wagner

2016: 424.

= Monolepta eburnea Laboissiere, 1920: 99; Wagner

2016: 424.

= Monolepta poriensis Laboissiere, 1920: 100; Wagner

2016: 424.

Bonn zoological Bulletin 69 (2): 225-247

= Monolepta oryzae Bryant, 1948: 62; Wagner 2016:

424.

Further material examined. 24 specimens, 9 findings.

Botswana. | ex., Mochudi, 24.23S/26.09E, XII.1979, C.

R. Owen (BMNH). — Ethiopia. 2 ex., Rock Valley nr.

Harar, 9.19N/42.08E, VI.1965, A. B. Gurney (USNM).

— Mocambique. | ex., Maputo Special Reserve, West

Gate, 26.30S/32.43E, VI.2017, Aristophanous et. al.

(BMNH). — South Africa. 4 ex., RSA, NW Prov., Kleks-

dorf, 26.52S/26.40E, 1.2001, Snizek (NME). — Tanzania.

7 ex., Ukiriguru, 2.43S/33.01E, [X.1960, I. A. D. Rob-

ertson (USNM); 4 ex., Malya, IV.1960, I. A. D. Robert-

son (USNM); 2 ex., Tarime, 1.21S/34.23E, X.1959, I. A.

D. Robertson (USNM). — Zambia. | ex., Victoria Falls,

17.5S/25.51E, V1.1968, P. Spangler (USNM); 1 ex. Kaf-

ue, XII.1919, Univ. Film ex., H. C. Laven (USNM).

Remarks. A detailed redescription was published in

Wagner (2016), where 1331 specimens out of 225 find-

ings are revised. The type specimen for the valid name

originated from Natal in South Africa.

©ZFMK

242 Thomas Wagner

Da Db Dc

Fig. 18. Monolepta citrinella Jacoby, 1899. A. Colour patterns. B. Basal antennomeres, males. C. Dto., females. D. Median lobe, a.

lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

Diagnosis. Monolepta citrinella is characterized by its

entirely yellow coloration. Some specimens are pale yel-

low, rarely whitish. It 1s the only species with this col-

oration in North-East Africa. Other species with entire

yellow dorsum like M. livingstoni (Jacoby, 1900), M. pi-

menteli Laboissiere, 1939, and M. hiekei Wagner, 2016

are all restricted to southern Africa.

Distribution and ecology. Widely distributed in savan-

nahs and semi-deserts up to desert biomes in tropical Af-

rica (Fig. 10). This almost pan-afrotropical distribution

has resulted in a large number of synonyms. Many spec-

imens were collected by light trapping (some of them in

moth traps, and then completely covered by lepidopteran

scales). The absence of an aposematic pattern and large

eyes are also typical characters of nocturnal beetles.

Monolepta leuce Weise, 1903

(Figs 4, 19)

Monolepta leuce Weise, 1903: 214.

= Monolepta puncticeps var. A. Chapuis, 1879: 24.

Further material examined. 49 specimens, 17 find-

ings. Eritrea. 7 ex., Umg. Asmara, 15.20N/39.00E,

VII.2001, L. & M. Stalmans (IRSN). — Ethiopia. 15 ex.,

Alemaya, 9.24N/42.01E, Bob Hill, Celtis Africana,

VI.1964 (USNM); 1 ex., Wolisso, Ghion, 8.32N/37.58E,

VI.1965, A. B. Gurney (USNM); 5 ex., Rock Valley

nr. Harar, VI.1965, A. B. Gurney (USNM); 5 ex., Ale-

maya, VI.1965, A. B. Gurney (USNM); 2 ex., Jimma,

7. 40N/36.50E, VII.1965, A. B. Gurney (USNM); 3 ex.,

Addis, IV.1971, B. Feinstein (USNM). — Kenya. | ex.,

Bonn zoological Bulletin 69 (2): 225—247

Lombwua, 0.02S/37.35E, Sandb. (NHRS); 1 ex., Mt.

Elgon, V. Clausnitzer (ZFMK); 1 ex., 30 min., NW

Nairobi, I.1968, K. V. Krombein (USNH); 1 ex., Nyeri,

0.25S/36.57E, 11.1968, P. J. Spangler (USNM); 1 ex.,

Gatamayu, 0.58S/36.42E, 2330 m, II.1999, Th. Wagner

(ZMFK); 1 ex., L. Naivasha, 0.23S/36.26E, sweeping

Lake margin, X.2005 (CDr). — Tanzania. | ex., Ngoron-

goro, 3.11S/35.34E, VIHI.1978, G. Scudder (BMNH);

1 ex., Segera Camp am Highway Hotel, 5.19S/38.33E,

325 m, 23.11.2008, U Heinig (CHe); 1 ex., Gonja, Chome

NR, Soth Pare Mts., 4.15S/37.58E, XII.2011, Smith &

Takano (BMNH); 2 ex., Mt. Meru NP; 3.14S/36.50E,

IV.2012, Smith & Takano (BMNH).

Remarks. A detailed redescription was published in

Wagner (2007b) that based on 755 studied specimens.

Next to the female lectotype from Tanzania “Type /

Mombo 7.99 / Monolepta leuce m. / ex. coll. J. Weise”

(MNHB), a ,,variation type“ of Monolepta puncticeps

var. A., a species synonymised with M. cruciata Guérin

de Méneville, 1847 was described from Ethiopia “Abyss.

Raffray / Monolepta puncticeps Chap. Type var.”. The

younger name M. /euce has priority since the older name

is infra-subspecific and thus not available, because a sin-

gle letter as species name is not conform with the ICZN

rules (cf. 11.9.1.).

Diagnosis. Most similar to MZ pauperata which occurs

allopatrically in lowland areas of Western Africa and

can be easily distinguished by completely yellowish-red

underside and the distinct elytral coloration. Monolepta

deleta that is sympatric in Kenyan and Tanzanian High-

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa 243

Da Db Dc

Fig. 19. Monolepta leuce Weise, 1903. A. Colour patterns. B. Basal antennomeres, males. C. Dto., females. D. Median lobe, a.

lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto., ventral.

lands, is on average smaller, elytra are broader and the

pronotum is narrower and more bulged than in M. leuce.

Most evident are the complete black antenna and legs

of M. deleta. There are very few M. cruciata with pale

elytral coloration similar to M. /euce (Figs 13Ad, 19A),

but there is at least at black spot at humerus and black

subhumeral margins.

Distribution and ecology. An abundant species of pre-

dominantely montane areas along the East African Rift

from Eritrea through Ethiopia, Kenya, Tanzania south-

wards to Lake Malawi (Fig. 4).

Monolepta jeanneli Laboissiére, 1920

(Figs 2, 20)

Monolepta jeanneli Laboissiere, 1920: 51.

= Monolepta burgeoni Laboissiere, 1940: 71; Wagner

2000: 230.

= Monolepta seminigra Bryant, 1953: 868; Wagner 2000:

230.

= Monolepta pallipes Bryant, 1953: 867; Wagner 2000:

230.

= Monolepta kiwuensis Weise, 1924; syn. nov.

Type material. New synonymy: Monolepta kiwuensis

Weise, 1924: Holotype, female, ,Ituru omrad. / Kivu

sjon / Monolepta kiwuensis m. / Holotypus Monolepta

kiwuensis Weise, 1924 / Monolepta jeanneli Laboissicre,

1920 Th. Wagner det.“ (NHRS). Holotype by indication

in the original publication ,,;Kiwu See, 1 9“.

Bonn zoological Bulletin 69 (2): 225-247

Further material examined. 26 specimens, 19 findings.

Congo (Democratic Republic). | ex., Parc Nat. Garam-

ba, Mt. Tungu, VI.1952, Miss. H. de Saeger (MRAC):

1 ex., Parc Nat. Albert, Munagana, 1.18S/29.36E,

VIII.1934, G. F. de Witte (IRSN). — Ethiopia. 2 ex.,

Lake Shola, 170 km S of Addis Abeba, 7.40N/38.40E,

XI.1990, Fabaceae, L. Medvedev (CMe). — Kenya. | ex.,

Chyulu Hills, 2.35S/37.50E, V.1976, ca. 1500 m, J. Krik-

ken (NNML); | ex., Mt. Elgon, Kaptega, 1.16N/34.52E,

1980 m, 1.1979, T.-E. Leiler (NHRS); 1 ex., Nairobi,

1.17S/36.50E, 1.1979, T.-E. Leiler (NHRS); 2 ex., Mt.

Elgon, nr. Chepnyalli Cave, dry evergreen montane for-

est, 2500 m, no. 509, at light, 1.1992, O. Merkl & G.

Varkony1 (HNHM),; 3 ex., Hells Gate NP, 0.56S/36,19E,

Tarchonanthus, IV.1998 (CDr); 2 ex., Ol-Njoroma

Gorge, Hells Gate, IV.1997 (CDr); 1 ex., Hells Gate

NP, sweeping Lake margin, X.2005 (CDr). — Tanza-

nia. 1 ex., Morogoro, 6.59S/37.40E, 580 m, light trap,

Ill -IV.1987, Pocs & Sontera (HNHM); 1 ex., Seronera,

XII.1995, lumiere, ex. coll. J. Roggeman (CBe); 1 ex.,

Tanz., 1250 m, 3°50S/30.42E, pr. Igoma, XII.2006, F.

Kantner (CKa); 1 ex., Ngorongoro, Sima camp, 2319 m,

3.13S/35.29E., IV.2012, Light trap, Smith & Takano

(BMNH); 1 ex., Kilimamoja, Kibaone, 3.23S/35.49E,

IV.2012, Light trap, Smith & Takano (BMNH). — Ugan-

da. 1 ex., 0.19N/32.35E, Kampala (ZMUH); 1 ex.,

Kibale Forest, 0.50N/31.06E, Sweep pine, I'V.1984, M.

Nummelin (MZHF); 1 ex., Budongo F,, near Sonso river,

1.45N/31.35E, Th. Wagner (ZFMK); 2 ex., SE of Hoima,

XI.2001, Snizek (NME).

©ZFMK

244 Thomas Wagner

Fig. 20. Monolepta jeanneli Laboissiere, 1920. A. Three different colour patterns. B. Basal antennomeres, males. C. Dto., females.

D. Median lobe, a. lateral, b. dorsal, c. ventral, without endophallic structures. E. Spermathecae. F. Bursa-sclerite, dorsal. G. Dto.,

ventral.

Remarks. A detailed redescription was published in

Wagner (2000), based on 175 specimens out of 93 find-

ings. The type material of the valid name originate from

the Kikuyu Escarpment in Central Kenya.

Diagnosis. Characterized by large, broad size, red elytral

coloration, pale yellow legs and antennae. In Ethiopia

and Eritrea the only Monolepta species with predomi-

nantely red dorsal coloration.

Distribution. Quite common in Central and East Africa

from lowland to monate regions, very rare in northeast

Africa (Fig. 2).

IDENTIFICATION KEY

The following key can be used for all specimens of “true”

Monolepta from North-East Africa, including the states

Egypt, Sudan, South-Sudan, Ethiopia, Eritrea, Djibouti

and Somalia. Up to now, 15 species of Monolepta are

known from this region, seven of them endemic to the

area, mainly from the Ethiopian Highlands.

Bonn zoological Bulletin 69 (2): 225—247

Upperside completely yellow; basal antennomeres

very slender (Fig. 18B, C); total length 4.0—-5.2 mm.

Widely distributed in the Afrotropical Region,

rarely found in North-East Africa (Fig. 10). — N.B:

Several species of galerucines with elongated basi-

metatarsus, possessing an entirely yellow coloration

are known from Africa, some of them originally

described in Monolepta, but do not belong to this

group. Allocation to the genus should be confirmed

by genital dissection in doubtful cases...........0000.000..

pn eee i Mee. ea ee M. citrinella Jacoby, 1899

Elytra carmine red, yellow with reddish outer

margins, or yellow with black markings................. 2

Elytra entirely carmine red (Fig. 20Aa), often with

broad black base (Fig. 20Ab), rarely with additional

black band in the apical third (Fig. 20Ac); large

and broad species, total length 4.50—5.10 mm; ratio

length of elytron to maximal width of both elytra

0.72—0.76. Mainly in wet tropical forests of Central

and East Africa, rarely found in the Ethiopian

Highlands (Fig. 2).....M. jeanneli Laboissiere, 1920

Elytra yellow, with black markings (e.g. Figs 1A, 5A,

9A, 15A), sometimes with red suture (Figs 13Ab,

©ZFMK

Revision of Monolepta Chevrolat, 1836 species from North-East Africa

16A), or with completely red outer margins

(Ete SaliSA Gal AG as. bi aut tensck urokhis tenet Ra eamelccns 3

Elytra black at base, usually as broad band, and

one further transverse black band, rarely reduced

to a smaller spot (Fig. 15Aa, Ac), in the apical third

of elytra; elytral outer margins and apex not black

ORs Fk fod 1 el oye aca ea nee wa amen oe eee Wy Beemer -

Elytra yellow, with black markings (e.g. Figs 1A,

5A, 9A), with or without transverse black band in the

middle, and usually with black elytral tip and outer

margins, sometimes with red suture (Figs 13Ab,

16A), or with completely red outer margins

GFiest SAC sO AS rhea 4:4 howe Won kesh eur es 5

Third antennomere significantly longer than second,

length of second to third antennomere 0.75—0.88

(Fig. 14B—C), and about half as long as fourth

antennomere, length of third to fourth antennomere

0.46—0.54; pronotum comparatively slender, prontal

length to width 0.63-—0.67; larger, total length 3.8-

5.3 mm; apex of median lobe slightly spoon-like

enlarged (Fig. 14D). Abundant in coastal regions

of North-East Africa, the Near East and the Arabian

Peninsula (Fig. 7)................. M. lepida Reiche, 1858

Third antennomere shorter, roughly of same length as

second, length of second to third antennomere 0.86—

1.00, length of third to fourth antennomere 0.28—0.37

(Fig. 15B—C); pronotum broader, pronotal length to

width 0.58—0.65; on average smaller, total length

3.2-4.7 mm; apex of median lobe more slender,

parallel-sided (Fig. 15D—F.); most specimens from

North-East Africa like coloration type Fig. 15Ae.

Abundant species throughout tropical Africa with

exception of the South (Fig. 7)...........0..... M. vincta

Gerstaecker, 1871

Elytra with completely red outer margins (Figs 13Ad,

Elytra at least with significant black base (e.g.

Figs 1A, 6A, 17A), rarely with narrow black outer

margins and suture (Figs 9Aa, 11Aa)..........0.0000. ii

Dorsum reddish to reddish-brown, elytra with

yellow ovate spots in the basal and apical half,

separated by a reddish transverse band (Fig. 19A);

underside and scutellum contrasting black: total

length 3.7—5.3 mm. Restricted to and abundant in the

East African Rift and adjacent areas, predominantely

montane zones from Eritrea and Ethiopia through

Kenya and Tanzania towards Lake Malawi (Fig. 4).

paki ok Ae ee oe M. leuce Weise, 1903

At least with black humeral tip; scutellum and

underside yellow (Fig. 13Ad); rare coloration (see

duplett 8)....M. cruciata Guérin de Méneville, 1849

Bonn zoological Bulletin 69 (2): 225-247

245

Elytra with entirely (Fig. 16Aa, Ac) or partly red

suture (Fies: 5A. ISAbB) TOAD) 21.0.8 hectic legen iines 8

Elytra only yellow with dark brown to black

SHUEY S09 hs a edema NB ot, Os see! Ladd ne seemlcebe 10

Large, total length 4.3—7.1 mm; usually with three

black transverse bands and entirely red suture

(Fig. 16Aa, Ac), or at least subscutellar red sutural

stripe and red scutellum (Fig 5A, 16Ab); basal

antennomeres slender (Figs 5B—C; 16B—C); median

lobe broad lanceolate at apex (Figs 5D, 16D),

spermatheca with large spherical nodulus (Figs 5E,

Smaller, total length 4.1-5.2 mm; cross-like elytral

pattern with narrow black or partly red outer margins

and suture, if suture partly red, subscutellar base

black (Fig. 13Ab); basal antennomeres broader, in

particular in males (Fig. 13B); median lobe narrowed

and slender at apex (Fig. 13D—E), spermatheca with

smaller spherical nodulus (Fig 13F). With exception

of the West, one of the most abundant Monolepta

species in Africa, also frequently found in Ethiopia

(Fig. 2)........ M. cruciata Guérin de Méneville, 1849

Elytra with broad transverse black band, only narrow

red along the basal part of suture and at elytral tip, no

red along uoter suture (Fig. 5A); median lobe more

slender, ventral groove narrow, lateral endophallic

spiculae have a small apical enlargement (Fig. 5D);

rare endemic species of the Ethiopian Highlands

(Ue fh i ee M. euchroma Fairmaire, 1883

Elytral transverse bands usually narrower, suture

entirely red (Fig. 16Aa, Ac) and/or outer elytral

margins partly red (Fig. 16Aa—Ac); median lobe

broader, ventral groove broader in the middle, lateral

endophallic spiculae with hammer-like enlargement

(Fig. 16D); widely distributed and abundant

throughout the Afrotropical Region (Fig. 12)...........

Bae AE POWER a eye eat ON M. vinosa Gerstaecker, 1871

Elytra with entirely black outer margins and suture,

without (Figs 9Aa, 9Ab, 11Aa), or with median

transverse band, given a cross-like pattern (Figs 8A,

SAC: VAC TTAB 3 Aa, SAC)Y Se. sr ies loc cas, 11

Elytra not entirely black at margins, usually only in

the basal half, without median transverse band and

cross-like pattern (Figs 1A, 3 A, 6A, 17A)........... 16

Pronotum red with significant black margins

(Fig. 8A); large, 5.20-5.60 mm; median lobe very

broad (Fig. 8D); restricted to Eritrea, Ethiopia and

SUI AN CRIS LAY eons oot Ree aie eae Mebane Ae nel Re

em Pino a? M. marginethoracica Laboissiere, 1940

Pronotum yellow to reddish-yellow, without black

margins, or entirely black; smaller, 3.90-5.20 mm;

Medial e@besOlOUNe ray Oe, ee Fe ee res 12

246 Thomas Wagner

12 Elytra with black suture and margins only, without

transverse band (Figs 9Aa, 9Ab, 11Aa)................ 13

— Elytra with cross-like pattern due to four yellow

spots (Figs 9Ac, 9Ad, 11Ab, 13Aa, 13Ac)........... 14

13 Pronotum broad, pronotal length to width 0.57—0.63

(Fig. 9A), yellow or black; total length at least

3.9 mm, apex of median lobe very slender, parallel-

sided (Fig. 9D); abundant and endemic in the

Ethiopian Highlands (Fig. 10)....... M. nigrocruciata

Laboissiére, 1940

— Pronotum more slender, pronotal length to width

0.62-0.67 (Fig. 11A), black; smaller, total ength

3.54.7 mm, apex of median lobe broad, spoon-like

(Fig. 11D); abundant and endemic in the Ethiopian

Highlands (Fig. 12) ..M. gobensis Laboissiere, 1940

14 Elytra relatively broad, width of both elytra to length

of elytron 0.66—0.74; apical part of median lobe

slender, conical (Fig. 13D—E); head and pronotum

usually yellow (Fig. 13Ac), if pronotum red, at least

base yellow (Fig. 13Aa, Ab) (see duplett 8)..............

golzmita dente! M. cruciata Guérin de Méneville, 1849

— Elytra more slender, width of both elytra to length

of elytron 0.62—0.70; apical part of median lobe

slender, but more parallel-sided (Fig. 9D) or broad

at apex (Fig. 11D); head and pronotum entirely red

(Fig. 9Aa—9Ac) or black (Figs 9Ad, 11Ab) ......... LS

15 Apex of median lobe very slender, parallel-sided

CE1g-291D) (SECU PSL UG en. Sirs nn Ranss etree etagutclen Riise

amide asing Settnad teat M. nigrocruciata Laboissiere, 1940

— Apex of median lobe broad, spoon-like (Fig. 11D)

(sceduplett-13)x. 7: M. gobensis Laboissiere, 1940

16 Elytra with broad black base, triangularly enlarged

along suture (Fig. 3A); large 4.8-5.6 mm; median

lobe broad conical towards apex (Fig. 3D); very

abundant endemic in the Ethiopian Highlands

(Figen ye ak Monolepta postrema Chapuis, 1879

— Elytra narrow black at base (Figs 1A, 3A, 16A);

usually smaller 3.6—5.4 mm; median lobe different..

BF olen acces 1 Ve eente RENE eee ee Sonpee Amel 120, ge Aon ee 17

17 Elytra with saddle-like black coloration (Fig. 17A);

small, total length: 3.6—4.8 mm; median lobe dorso-

ventrally compressed, conical, pointed at apex

(Fig. 17D); restricted to montane areas of Ethiopia,

Uganda, Kenya, Rwanda and northern Tanzania

CEs" 105) Peon ae M. ephippiata Gerstaecker, 1871

— Basal half of elytra with narrow black base and

margin, along suture somewhat enlarged towards the

middle (Figs 1A, 6A); same size or larger; median

lobe enlarged at apex (Figs 1D, 6D) ..........00......... 18

Bonn zoological Bulletin 69 (2): 225—247

18 Smaller, 4.0-4.8 mm; elytra more slender, width of

both elytra to length of elytron 0.62—0.70; pronotum

red (Fig. 1A); median lobe slender, lateral spiculae

twisted (Fig. 1D); rare endemic species of the

Bihio pian Highlands: (Pig 2) scree ots ame es

Aa achanadeceea tad Monolepta longiuscula Chapuis, 1879

— Larger, 4.6-5.4 mm; elytra slightly broader, width of

both elytra to length of elytron 0.62—0.68; pronotum

yellow (Fig. 6A); median lobe broader, lateral

spiculae straight (Fig. 6D); rare endemic species of

the Ethiopian Highlands (Fig. 2)...

Be eh an Monolepta nigropicta Laboissiere, 1938

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BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (2): 249-261

2020 - Romanowski J. et al.

https://do1.org/10.20363/BZB-2020.69.2.249

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:3 1 20B9BF-7510-4874-8C3B-E93425A65544

The Coccinellidae (Coleoptera) from El Hierro, Canary Islands

Jerzy Romanowski'’, Piotr Ceryngier’, Christian Zmuda’*, Jaroslav Vétrovec’ & Karol Szawaryn*

'2.3 Institute of Biological Sciences, Cardinal Stefan Wyszynski University, Woycickiego 1/3, 01-938 Warsaw, Poland

*Buzulucka 1105, Hradec Krdlové, Czech Republic

> Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679, Warsaw, Poland

“Corresponding author: Email: j.romanowski@uksw.edu.pl

'urn:|sid:zoobank.org:author: DBA7DF8E-27C 1-4600-8632-1316D994940C

> urn:|sid:zoobank.org:author: 1345CB63-OBE2-447B-ADB0O-CACCF74D 1616

3urn:Isid:zoobank.org:author: FFE2BF31-198A-418D-9BB2-17447A325E9D

*urn:Isid:zoobank.org:author:ADA36F 13-ECF6-4B09-B6B7-2E96CA 945E0F

>urn:Isid:zoobank.org:author:D741C759-6CDD-4B61-BE93-3ECC2918A73F

Abstract. In this study, Coccinellidae were collected and observed at 42 sites located on El Hierro (Spain), the western-

most island of the Canary archipelago, during 2017 and 2019 excursions. A total of 1553 specimens belonging to 18 spe-

cies were recorded, of which four species are newly reported from El Hierro. The total number of ladybird species so far

documented to inhabit El Hierro is 22. After examination of the morphological features Scymnus cercyonides Wollaston,

1864 is transferred from the subgenus Pul//us Mulsant, 1846 to Mimopullus Firsch, 1987. Chilocorus canariensis Crotch,

1874 and Novius canariensis Korschefsky, 1935 are confirmed to be valid species.

Key words. Spain, West Palaearctic, ladybird beetles, new records, endemic species.

INTRODUCTION

The Canary Islands are situated in the northeast Atlantic

Ocean near the African coast and belong to the Mediter-

ranean Basin biodiversity hotspot (Myers et al. 2000).

They have a subtropical climate strongly influenced by

the humid trade winds, with temperatures showing little

seasonal variation: mean temperature in winter is 18 °C

and in summer 24 °C (Juan et al. 2000; Espadaler 2007).

The fauna of the Canary Islands is characterized by a high

level of endemism. For example, among the Canarian in-

vertebrates endemism is estimated at about 50% (Juan

et al. 2000).

The fauna of Coccinellidae of the Canary Islands has

a long history of exploration pioneered by Wollaston

(1864) and summarized by Eizaguirre (2007) and Oromi

et al. (2010). More than 50 species of ladybird beetles

were reported from the archipelago. The highest num-

bers of species were reported from Gran Canaria (42) and

Tenerife (41) (Eizaguirre 2007; Oromi et al. 2010; Su-

arez et al. 2018, Romanowski et al. 2020a), large islands,

well-known for their concentration of endemic diversity

(Reyes-Betancort et al. 2008). However, Coccinellidae

were not deeply investigated on all islands of the archi-

pelago, and only 18 species have so far been reported

from El Hierro (Franz 1995; Oromi et al. 2010). Recent

study by Romanowski et al. (2018, 2019) nearly doubled

Received: 19.03.2020

Accepted: 10.09.2020

number of ladybird species reported from Fuerteventura

and indicated that this eastern island of the Canary archi-

pelago was less prospected than central islands such as

Tenerife and Gran Canaria. This study aims to provide

new information on species richness of ladybird beetles

of El Hierro.

MATERIAL AND METHODS

El Hierro is the westernmost and also the smallest

(269 km?) and geologically youngest island of the Canary

archipelago, formed by volcanic eruptions approximately

1.1 million years ago (Fernandez-Palacios & Whittaker

2008). A wide range of natural habitats can be found on

the island (Fig. 1) along with decorative plants sustained

by irrigation that grow in parks, hotel grounds and gar-

dens. Due to a well-preserved biological diversity, since

2000 EI Hierro has the status of a biosphere reserve.

Coccinellidae were collected and observed at 42 sites

on El Hierro between 28 January and 2 February 2017

and between 6 and 12 April 2019. Study sites were lo-

cated along the coast and inland of the island (Table 1).

The beetles were mostly shaken down from various trees

and shrubs on a 1 m x | m white beating sheet and were

swept from ground cover with a net. Some ladybirds

were picked from vegetation after direct observation.

Corresponding editor: D. Ahrens

Published: 27.10.2020

250 Jerzy Romanowski et al.

Fig. 1. Habitats surveyed for ladybird beetles on El Hierro. A. Halophile vegetation. B. Junipers Juniperus sp. in Sabinar. C. Pine

forest. D. Agricultural land.

The voucher specimens collected by J. Romanowski and

C. Zmuda are stored in the insect collection at the Insti-

tute of Biological Sciences, Cardinal Stefan Wyszynski

University in Warsaw and those collected by J. Kratky

and J. Pelikan are deposited in private collection of Ja-

roslav Vétrovec.

The nomenclature of ladybird beetles, unless specif-

ically discussed, follows Kovar (2007), and systematic

arrangement follows Slipinski (2007) and Seago et al.

(2011). List of synonyms is provided only for species

which were not mentioned in the previous works (Roma-

nowski et al. 2019; Romanowski et al. 2020b).

RESULTS

During the research, a total of 1553 Coccinellidae spec-

imens (1545 imagines, 3 pupae, and 5 larvae) belonging

to 18 species were recorded, of which four are new to El

Hierro. Below, the data on the recorded species are pro-

vided together with supplementary photographic infor-

Bonn zoological Bulletin 69 (2): 249-261

mation on the identification of several species of special

interest.

List of taxa found on El Hierro during this study

Coccinellinae Latreille, 1807

Chilocorini Mulsant, 1846

Chilocorus canariensis Crotch, 1874

Fig. 2A—F

Material examined. Valverde (30.1.2017), 1 ex. (leg. J.

Kratky); Las Puntas (29.1.2017), 2 exx. (leg. J. Kratky);

El Chirgo (29.1.2017), 1 ex. (leg. J. Pelikan); Tamaduste

(30.11.2017), 1 ex. (leg. J. Kratky); Arbol Garoé, Eche-

do, El Juan, El Mocanal, Guarazoca, Hoya del Morcil-

lo, La Caleta, La Dehesa, Las Playas, Mirador de Isora,

Montafia de la Casilla, Pozo de las Calcosas, Punto de la

Dehesa, Sabinar, Tigaday, Valverde (6—12.IV.2019), total

of 57 exx. (55 adults, 2 larvae) collected from various

©ZFMK

Coccinellidae from El Hierro ny |

Table 1. Collecting sites of ladybird beetles on El Hierro.

0 MN DN FWN YH [ZF

io)

HB FS BPW WWW WwwwwowNnN NN NN WN NN NV N YR eR FRR FR

No RF OO DN WDNA FW N YK DU AN HD FPWNRK TD OU HAN DN fF WN YF CO

Location

Arbol Garoé

Camino de Jinama

Charco Menso

Cueva de Don Juste

Echedo

El Chirgo

El Gretime

El Juan

El Mocanal

El Pinar

El Sabinal

El Tifior

El Tomillar

Eremita de San Salvador

Guarazoca

Hoya del Morcillo

Isora

La Caleta

La Dehesa

La Restinga

Las Playas

Las Puntas

Malpaso

Mirador de Isora

Mirador de Jinama

Mirador de las Playas

Montafia de Cascaja

Montafia de la Casilla

Montafia de Masilva

Montafia de Mercadel

Montafia del Gajo

Montafia del Lajura

Pista del Derrabado

Pozo de la Salud

Pozo de las Calcosas

Punto de la Dehesa

Sabinar

Sabinosa

San Andres

Tamaduste

Tigaday

Valverde

Coordinates

27°47’ 22”N 17°56°35”W

27°45’ 12”N 17°59°28"°W

27°50’52”N 17°55’24”"°W

27°38'°54’"N 17°59°31"°W

27°50’03”N 17°55’22”W

27°45°04’"N 18°03’06”W

27°44’22”N 18°04’56”W

27°42’46”N 18°02753”W

27°49 14"N 17°56°41°W

27°41°43”N 17°58°35”°W

27°43’°48"N 18°07°14"°W

27°47°21”"N 17°56’03”W

27°43’28"N 18°06’23”W

27°43’56”N 18°00’37”°W

27°48°35"N 17°58’24"°W

27°42’51”N 17°59°49°W

27°45’09"N 17°56’51”W

27°48’03”N 17°53’14"°W

27°43°47°N 18°08’30”W

27°38’29"N 17°58’°55”°W

27°43’°04’"N 17°57731°W

27°47°31"N 17°59°29"°W

27°43’43”N 18°02’26”"W

27°44°19"N 17°57°04°W

27°45°46"N 17°58’50”W

27°43’°57°N 17°58’22”W

27°47 24°N 17°58°21°W

27°43’15”N 17°58’50”°W

27°43’°51”N 17°59°31°W

27°42’39"N 18°01717”"W

27°43°44"N 17°59°29”"W

27°40°41"N 17°58°48"°W

27°44’27"N 18°03°51°W

27°45’22”N 18°06714"°W

27°50’23”N 17°56°48"°W

27°45’59”"N 18°07°48"°W

27°44’°55”N 18°07°37"°W

27°44’51”N 18°05°51”°W

27°46’°06”N 17°57°53”W

27°49’30’N 17°53’44°W

27°45’°06”N 18°01°36”W

27°48°38"N 17°54’°52”W

Bonn zoological Bulletin 69 (2): 249-261

plants, including Yucca sp., Euphorbia sp., Juniperus sp.,

Nerium oleander L. (leg. J. Romanowski and C. Zmuda).

Distribution. Endemic Canarian species.

Remarks. Wollaston (1864) examined specimens of this

species from the Canary Islands and stated that they be-

long to the common European species Ch. renipustulatus

(Scriba, 1790). However, Crotch (1874) in his revision

of the ladybird beetles of the world, recognized it as a

separate species. Since that time various authors treat-

ed it as a subspecies of Ch. renipustulatus (Franz 1995;

Eizaguirre 2007; Nicolas 2010; Nicolas & Rae 2012) or

as a distinct species (Kovar 2007; Hernandez et al. 2009).

To confirm the status of the Canarian specimens we com-

pared the genitalia of both sexes with those of Ch. re-

nipustulatus collected in Poland (Fig. 2G—K). Without

a doubt, Ch. canariensis should be treated as a distinct,

endemic Canarian species, and Ch. renipustulatus should

be excluded from the list of ladybird beetles of the Ca-

nary Islands.

Differential diagnosis. Chilocorus canariensis can be

separated externally from Ch. renipustulatus by the shape

of red maculae on elytra (Fig. 2A). In Ch. canariensis el-

ytral maculae form a transverse band in the central part

of each elytron, while in Ch. renipustulatus maculae are

almost rounded with a regular border. Differences in

male genitalia: in Ch. canariensis penis guide asymmet-

rical (Fig. 2D—E), about as long as parameres, parameres

shortly setose, apex of penis with screw-shaped carina

with more dense coils (Fig. 2F); in Ch. renipustulatus pe-

nis guide symmetrical (Fig. 2I—J), distinctly shorter than

parameres, parameres with longer setae, apex of penis

with screw-shaped carina more loose (Fig. 2K). Differ-

ences in female genitalia: in Ch. canariensis (Fig. 2C)

spermatheca with apical projection more sclerotized and

twice longer than in Ch. renipustulatus (Fig. 2H).

Parexochomus nigripennis (Erichson, 1843)

Material examined. Las Puntas (29.1.2017), 1 ex. (leg.

J. Kratky).

Distribution. Reported from all islands of the Canary ar-

chipelago excluding La Palma (Eizaguirre 2007; Oromi

et al. 2010). Outside of the Canary Islands known from

Algeria, Egypt, Libya, Tunisia, Morocco, Iran, Italy, Por-

tugal, Spain, Saudi Arabia, United Arab Emirates, Iran,

Pakistan and India (Poorani 2002; Kovar 2007; Biran-

vand et al. 2017; Abied et al. 2018; Lakhal et al. 2018).

©ZFMK

252 Jerzy Romanowski et al.

Fig.2. A-F. Chilocorus canariensis Wollaston. A. Habitus. B. Abdomen, male. C. Spermatheca, spermduct and accessory gland.

D. Tegmen, lateral. E. Tegmen, inner. F. Penis, lateral. G—K. Chilocorus renipustulatus (Scriba). G. Abdomen, male. H. Sper-

matheca, spermduct and accessory gland. I. Tegmen, lateral. J. Tegmen, inner. K. Penis, lateral.

Bonn zoological Bulletin 69 (2): 249-261 ©ZFMK

Coccinellidae from El Hierro 253

Coccidulini Mulsant, 1846

Cryptolaemus montrouzieri Mulsant, 1853

Material examined. Echedo (12.1V.2019), 1 ex. on N.

oleander, Tamaduste (11.IV.2019), 1 ex. on Bougainvil-

lea sp. (leg. J. Romanowski and C. Zmuda).

Distribution. An Australian species spread throughout

the world (Kairo et al. 2013). Reported from all Canary

Islands (Eizaguirre 2007; Oromi et al. 2010; Romanows-

ki et al. 2019, 2020b).

Nephus flavopictus (Wollaston, 1854)

Fig. 3G

Material examined. Pozo de la Salud (28.1.2017), 1 ex.

(leg. J. Kratky); El Pinar (31.1.2017), 1 ex. (leg. J. Pe-

likan) from Euphorbia sp.; El Tifior (1.11.2017), 1 ex.

(leg. J. Pelikan); Pozo de las Calcosas, Charco Menso,

Cueva de Don Juste, El Mocanal, El Tomillar. Guaraz-

oca, Isora, La Caleta , La Restinga, Pozo de la Salud,

Sabinar, Tamaduste, Tigaday, Valverde (7—12.IV.2019),

total of 96 exx. collected from various plants, including

Euphorbia sp., Juniperus sp., Yucca sp., N. oleander,

Pistacia lentiscus L. and Bougainvillea sp. (leg. J. Ro-

manowski and C. Zmuda).

Distribution. Endemic Macaronesian species, reported

from the Canary Islands (Fursch 1987; Eizaguirre 2007;

Oromi etal. 2010), the Azores (Fursch 1966, 1987; Soares

et al. 2003a) and Madeira (Bielawski 1963; Fursch 1987;

Soares et al. 2003b).

Remarks. Two N. flavopictus specimens collected at El

Monacal have a distinct color form depicted in Fig. 3G.

In this form the black markings on the light area of the

elytra are missing (for comparison with typically colored

individuals see fig. 5K in Romanowski et al. 2019).

Nephus (Nephus) incisus (Har. Lindberg, 1950)

Material examined. La Restinga (8.IV.2019), 11 exx.

on N. oleander and Hibiscus sp.; Montafia del Lajura

(8.IV.2019), 2 exx. on Euphorbia sp.; Tamaduste (11.

IV.2019), 1 ex. on Euphorbia sp. (leg. J. Romanowski

and C. Zmuda).

Distribution. Endemic Canarian species (Oromi et al.

2010; Romanowski et al. 2019, 2020). By some authors

(Fursch 1987; Eizaguirre 2007; Nicolas 2010) erroneous-

ly reported under the name Nephus peyerimhoffi (Sicard,

1923) (Romanowski et al. 2019). New to EI Hierro.

Bonn zoological Bulletin 69 (2): 249-261

Rhyzobius litura (Fabricius, 1787)

Material examined. Sabinar (8.IV.2019), 1 ex. on Juni-

perus sp. (leg. J. Romanowski and C. Zmuda).

Distribution. Palaearctic species (Kovar 2007), report-

ed from all the Canary Islands (Eizaguirre 2007; Oromi

et al. 2010).

Rhyzobius lophanthae (Blaisdell, 1892)

Material examined. El Mocanal (9.IV.2019), 1 ex.;

El Tomillar (7.1V.2019), 1 ex.; Guarazoca (9.IV.2019),

20 exx.; Las Playas (12.1V.2019), 2 exx.; La Restinga

(8.I1V.2019), 1 ex.; Mirador de Isora (12.IV.2019), 2 exx.;

Tigaday (07.IV.2019), 1 ex., collected mostly from Cy-

cas sp., Phoenix canariensis H. Wildpret, Hibiscus sp.

and Yucca sp. (leg. J. Romanowski and C. Zmuda).

Distribution. Widely distributed species of Australian

origin, known from all Canarian Islands (Eizaguirre,

2007).

Scymnus (Pullus) canariensis Wollaston, 1864

Big 3F

Material examined. Pozo de la Salud (28.1.2017),

6 exx. (leg. J. Kratky), 2 exx. (leg. J. Pelikan); Sabinosa

(28.1.2017), 2 exx. (leg. J. Kratky); Pista del Derrabado

(23.1.2017), 1 ex. (leg. J. Kratky); El Chirgo (28.1.2017),

6 exx. (leg. J. Kratky), (29.1.2017), 7 exx. (leg. J. Pe-

likan); Las Playas (1.11.2017), 2 exx. (leg. J. Kratky);

Tamaduste (30.1.2017), 1 ex. (leg. J. Kratky), Camino de

Jinama (31.1.2017), 1 ex. (leg. J. Pelikan); Cueva de Don

Juste, Echedo, El Juan, El Mocanal, El Sabinal, El To-

millar, Guarazoca, Hoya del Morcillo, Isora, La Caleta,

La Dehesa, La Restinga, Las Playas, Mirador de Isora,

Montafia de la Casilla, Montafia del Lajura, Pozo de la

Salud, Pozo de las Calcosas, Punto de la Dehesa, Sabi-

nar, Tamaduste, Tigaday, Valverde (7—12.IV.2019), total

of 901 exx. collected from various plants including Pinus

canariensis C. Smith, Juniperus sp., N. oleander, Prunus

dulcis (Mill.) D.A.Webb, Casuarina equisetifolia L., Hi-

biscus sp., Ph. canariensis, Euphorbia sp., Hedera sp.

and Yucca sp. (leg. J. Romanowski and C. Zmuda).

Distribution. Scymnus canariensis has been considered

an endemic Canarian species, known from all islands of

the archipelago (Eizaguirre 2007). However, recently it

was also reported from Sao Tomé and Principe, and Sen-

egal (Hounkpati et al. 2020).

Remarks. On El Hierro, S. canariensis has a distinct

color form, which is depicted on Fig. 3F. It was already

emphasized by Wollaston (1864) that the occurrence of

this form (named by him S. canarensis var. f) is limited

©ZFMK

254 Jerzy Romanowski et al.

Fig. 3. A-C. Coccinella miranda Wollaston. A. Tegmen, inner. B. Tegmen, lateral. C. Penis, lateral. D. Pharoscymnus decempla-

giatus (Wollaston), habitus of untypically colored specimen from El Hierro. E. Coccinella miranda Wollaston, habitus. F. Scymnus

canariensis Wollaston, habitus of El Hierro color form. G. Nephus flavopictus (Wollaston), habitus of untypically colored specimen

from El Hierro.

Bonn zoological Bulletin 69 (2): 249-261 ©ZFMK

Coccinellidae from El Hierro 255

to El Hierro. Male genitalia in this form agree with those

of S. canariensis from other islands of the archipelago

(e.g., Romanowski et al. 2019).

Scymnus (Mimopullus) cercyonides Wollaston, 1864

new combination

Fig. 4A-I

Material examined. E] Chirgo (28.1.2017), 5 exx. (leg.

J. Kratky) from Euphorbia sp., 1 ex. (leg. J. Pelikan);

Sabinosa (29.1.2017), 2 exx. (leg. J. Kratky), 1 ex. (leg.

J. Pelikan); Eremita de San Salvador (31.1.2017), 1 ex.

(leg. J. Kratky) from Laurus sp.; El Mocanal (9.IV.2019),

1 ex. from Hibiscus sp.; El Tomillar (7.1V.2019), 1 ex.

from Ficus carica L.; Sabinar (8.IV.2019), 1 ex. from Ju-

niperus sp. (leg. J. Romanowski and C. Zmuda).

Distribution. The species reported from western and

central Canary Islands (Eizaguirre 2007; Oromi et al.

2010).

Remarks. Male genitalia of our specimens (Fig. 4D—F)

are identical with the lectotype drawn by Fursch (1987).

Species frequently misidentified with Scymnus marinus

Mulsant, 1850. So far it was assigned to the subgenus

Pullus Mulsant, 1846. However, based on the short ca-

rinae on prosternal process, complete and recurved post-

coxal abdominal lines (Fig. 4A), and antennae consisting

of 11 antennomeres, with a club composed of 4 antenno-

meres (Fig. 4H), we transfer this species to the subgenus

Mimopullus Firsch, 1987.

Scymnus (Scymnus) nubilus Mulsant, 1850

Material examined. Sabinosa (28.1.2017), 1 ex. (leg. J.

Kratky); Las Playas (12.IV.2019), 5 exx. on N. oleander

(leg. J. Romanowski and C. Zmuda).

Distribution. Reported from all the islands of the Canary

archipelago except La Palma (Oromi et al. 2010; Roma-

nowski et al. 2019, 2020b). Species widely distributed

in the Mediterranean and Middle Eastern regions (Kovar

2007). Recorded also in Pakistan (Gilgit-Baltistan) (Ash-

faque et al. 2015), India (Poorani & Lalitha 2018) and

Nepal (Bielawski 1972).

Stethorus tenerifensis Fiirsch, 1987

Material examined. Eremita de San Salvador

(31.1.2017), 1 ex. (leg. J. Pelikan); Echedo, El Mocanal,

El Sabinal, El Tomillar, Isora, La Caleta, La Dehesa,

La Restinga, Las Playas, Mirador de Isora, Pozo de las

Calcosas, Sabinar, Tamaduste, Tigaday, Valverde (7-12.

IV.2019), total of 132 exx. collected from various plants

Bonn zoological Bulletin 69 (2): 249-261

including Juniperus sp., P. canariensis, Euphorbia sp.,

N. oleander, Ph. canariensis, Yucca sp., Punica grana-

tum L. and F: carica L. (leg. J. Romanowski and C. Zmu-

da).

Distribution. Endemic species, known from all Canarian

Islands (Eizaguirre 2007; Oromi et al. 2010; Romanows-

ki 2020b).

Coccinellini Latreille, 1807

Coccinella miranda Wollaston, 1864

Fig. 3A-C, E

Material examined. E] Gretime (29.1.2017), 1 ex. (leg.

J. Kratky); Montafia del Gajo (30.1.2017), 2 exx. (leg.

J. Kratky); El Pinar (30.1.2017), 1 ex. (leg. J. Kratky);

El Tomillar, Malpaso, Mirador de las Playas, Montafia

de la Casilla, Montafia de Masilva, Montafia de Mer-

cadel, Pozo de la Salud, Sabinar (6—11.I'V.2019), total of

99 exx. (98 adults, 1 larva) collected from P. canariensis

(leg. J. Romanowski and C. Zmuda).

Distribution. Endemic Canarian species, reported from

Tenerife, La Gomera, La Palma, Gran Canaria and

Fuerteventura (Eizaguirre 2007; Oromi et al. 2010). The

occurrence on Fuerteventura was not confirmed in a re-

cent study (Romanowski et al. 2019). New to EI Hierro.

Coccinella septempunctata algerica Kovar, 1977

Material examined. El Pinar (30.1.2017), 2 exx. (leg. J.

Kratky); El Juan, El Mocanal, Hoya del Morcillo, Isora,

Las Playas, Mirador de Isora, Mirador de Jinama, Mon-

tafia de la Casilla, Pozo de la Salud, San Andres (06-12.

IV.2019), total of 67 exx. (66 adults, 1 larva) collected

from P. canariensis, Tamarix sp., N. oleander and herba-

ceous plants (leg. J. Romanowski and C. Zmuda).

Distribution. This Palaearctic species inhabits all seven

Canarian islands (Eizaguirre 2007; Oromi et al. 2010).

Myrrha octodecimguttata (Linnaeus, 1758)

Material examined. Arbol Garoé (9.IV.2019), 2 exx.

from P. canariensis; El Tomillar (7.1V.2019), 1 ex. from

P. canariensis (leg. J. Romanowski and C. Zmuda).

Distribution. Palaearctic species (Kovar 2007), reported

so far from two Canarian islands, La Gomera (Eizaguirre

2007; Oromi et al. 2010) and Gran Canaria (Romanows-

ki et al. 2020a). New to El Hierro.

©ZFMK

256 Jerzy Romanowski et al.

Fig. 4. Scymnus (Mimopullus) cercyonides Wollaston. A. Abdomen, male. B. Spermatheca. C. Female genitalia, bursa copulatrix,

spermduct and spermathecal. D. Tegmen, inner. E. Penis, lateral. F. Tegmen, lateral. G. Habitus. H. Antenna. I. Male abdominal

segments [IX and X.

Hippodamia variegata (Goeze, 1777)

Material examined. Isora (12.IV.2019), 1 ex. from

P. granatum, Montafia de Cascaja (9.IV.2019), 1 ex. from

herbaceous vegetation; Pozo de la Salud (7.IV.2019),

4 exx. (3 pupae and | larva) from herbaceous vegetation:

San Andres (11.IV.2019), 1 ex. from herbaceous vegeta-

tion (leg. J. Romanowski and C. Zmuda).

Distribution. The species is widely distributed in the Pa-

laearctic, Afrotropical and Oriental regions, and inhabits

all seven Canarian islands (Eizaguirre 2007; Oromi et al.

2010).

Noviini Mulsant, 1846

Novius canariensis Korschefsky, 1935

Fig. SA-F, L

Bonn zoological Bulletin 69 (2): 249-261

Material examined. Arbol Garoé (9.IV.2019), 1 ex.

from Juniperus sp.; El Sabinal (7.[V.2019), 1 ex. from

Juniperus sp.,; Mirador de Isora (12.1V.2019), 3 exx. from

Euphorbia sp.;, Tigaday (7.1V.2019), 1 ex. from Junipe-

rus sp. (leg. J. Romanowski and C. Zmuda).

Distribution. Endemic Canarian species, known from

Tenerife and Gran Canaria (Eizaguirre 2007; Oromi et al.

2010). New to El Hierro.

Remarks. There were some doubts about the validi-

ty of this species. Forrester (2008) wrote that she was

unable to find and examine the type series of N. canar-

iensis collected on Gran Canaria. However, Korschefsky

(1935) drew the habitus of that species, which perfectly

fits to our specimens collected on El Hierro (Fig. SL). To

check, whether N. canariensis is a distinct species, its

male genitalia were compared with the genitalia of main-

land N. cruentatus (Mulsant, 1846) collected in Poland

©ZFMK

Coccinellidae from El Hierro 257.

Fig. 5. A-F. Novius canariensis Korshefsky. A. Abdomen, male. B. Spermatheca. C. Female genitalia and bursa copulatrix. D.

Penis, lateral. E. Tegmen, inner. F. Tegmen, lateral. G-J. Novius cruentatus (Mulsant). G. Abdomen, male. H. Penis, lateral. I. Teg-

men, inner. J. Tegmen, lateral. K. Novius cruentatus, habitus. L. Novius canariensis, habitus.

Bonn zoological Bulletin 69 (2): 249-261 ©ZFMK

258

(Fig. 5G—K). Our investigation confirms that the Canari-

an species is clearly different from N. cruentatus.

Differential diagnosis. Novius canariensis (Fig. 5L) can

be separated externally from N. cruentatus (Fig. 5K) by

the shape of red maculae on elytra. In N. canariensis the

central part of elytra is occupied by a complete transverse

band, whereas in N. cruentatus there are two small red,

rounded maculae on each elytron, one close to the later-

al margin, second close to sutural line. Sometimes these

maculae are larger but they never form complete trans-

verse band. Differences in male genitalia: in N. canar-

iensis tegminal strut short, penis guide with blunt apex

(Fig. 5E), in lateral view regularly curved (Fig. 5F), in

N. cruentatus tegminal strut long, penis guide pointed

(Fig. 51) , in lateral view sinusoidal (Fig. 5J).

Novius cardinalis (Mulsant, 1850)

Material examined. El Gretime (29.1.2017), 3 exx. (leg.

J. Kratky); Camino de Jinama (31.1.2017), 1 ex. (leg.

J. Kratky); Valverde (30.1.2017), 1 ex. (leg. J. Kratky);

Montafia del Gajo (30.1.2017), 1 ex. (leg. J. Kratky);

Cueva de Don Juste (8.1V.2019), 1 ex. from succulents;

El Sabinal (7.IV.2019), 1 ex. from Juniperus sp.; El To-

millar (7.1V.2019), 6 exx. from F; carica; Hoya del Mor-

cillo (6.[V.2019), 1 ex. from P. canariensis; La Restinga

(8.1V.2019), 2 exx. from Hibiscus sp.; Mirador de Iso-

ra (12.1V.2019), 4 exx. from P. dulcis; Tamaduste (12.

IV.2019), 2 exx. from P. lentiscus, Tigaday (7.1V.2019),

8 exx. from herbaceous plants (leg. J. Romanowski and

C. Zmuda).

Distribution. This species, native to Australia, 1s cur-

rently widely distributed in warmer regions throughout

the world (Kovar 2007; Michaud 2012). Reported from

all islands of the Canary archipelago (Oromi et al. 2010;

Romanowski et al. 2019).

Remarks. This species has for a long time been placed in

the genus Rodolia Mulsant, 1850. However, Rodolia was

recently synonymized with Novius Mulsant, 1846 (Pang

et al. 2020).

Sticholotidini Pope, 1962

Pharoscymnus decemplagiatus (Wollaston, 1857)

Fig. 3D

Material examined. Tamaduste (30.1.2017), 1 ex. (leg.

J. Kratky); El Mocanal (9.TV.2019), 4 exx. from Ficus sp.

and Hibiscus sp.; La Caleta (10.IV.2019), 11 exx. from

Euphorbia sp., Ficus sp. and Hibiscus sp.; La Restinga

(8.1V.2019), 1 ex. from Hibiscus sp.; Las Playas (12.

IV.2019), 2 exx. from N. oleander, Montafia del La-

jura (8.IV.2019), 5 exx. from P. canariensis,; Sabinar

Bonn zoological Bulletin 69 (2): 249-261

Jerzy Romanowski et al.

(8.I1V.2019), 5 exx. from Juniperus sp.; Tamaduste (11.

IV.2019), 8 exx. from Yucca sp.; Tigaday (8.IV.2019),

9 exx. from Juniperus sp. and Ph. Canariensis (leg.

J. Romanowski and C. Zmuda).

Distribution. Species reported from all islands of the

Canary archipelago (Oromi et al. 2010; Romanowski

et al. 2019) and from Madeira (Wollaston 1857).

Remarks. One of the specimens of P. decemplagiatus

collected in this study has a distinct color form depict-

ed in Fig. 3D. It is entirely black, without yellow elytral

spots found in typically colored specimens (for compari-

son see fig. 9B in Romanowski et al. 2019).

DISCUSSION

In this study we recorded the occurrence on El Hierro

of 18 species of Coccinellidae, of which four have not

previously been reported from the island (Table 2). On

the other hand, we failed to find four species reported by

other authors: Scymnus (Mimopullus) marinus Mulsant,

1850, S. (Scymnus) rufipennis Wollaston, 1864, Stethorus

wollastoni Kapur, 1948 and Novius cruentatus (Mulsant,

1846). The total number of ladybird species so far doc-

umented to inhabit El Hierro is thus 22. However, the

status of the species not recorded in this study (S. mari-

nus, S. rufipennis, S. wollastoni and N. cruentatus) needs

further investigation. Of the species newly reported for

EI Hierro, three (Nephus incisus Novius canariensis and

Coccinella miranda) are the Canarian endemics, and the

fourth (Myrrha octodecimguttata) is widely distributed

in the Palaearctic region (Kovar 2007).

Although the number of ladybird species known from

El Hierro increased slightly as a result of our survey, it

is still the lowest among the main seven islands of the

archipelago. Not much higher numbers were record-

ed on Lanzarote (Romanowski et al. 2020b) and La

Gomera (Oromi et al. 2010) (23 species on each island),

as well as on La Palma (Oromi et al. 2010) (25 species),

while clearly higher on Gran Canaria (Romanowski et

al. 2020a) (42 species) and Tenerife (Eizaguirre 2007;

Oromi et al. 2010; Suarez et al. 2018) (41 species). The

low ladybird species richness on El Hierro may be relat-

ed to the island’s small size, low age and long distance

from the African continent. On the other hand, relatively

few alien species have so far been recorded on El Hi-

erro. Those include three widely distributed Australian

species: Cryptolaemus montrouzieri, Rhyzobius lophan-

thae and Novius cardinalis. In contrast, on Lanzarote,

apart from these three Australian species, the American

Delphastus catalinae (Horn, 1895) and Olla v-nigrum

(Mulsant, 1866) as well as the Asiatic Pharoscymnus

flexibilis (Mulsant, 1853) have been found (Romanowski

et al. 2020b). The latter two species probably arrived to

©ZFMK

Coccinellidae from El Hierro

259

Table 2. The list of Coccinellidae recorded on El Hierro in this study and reported in previous papers. Question mark after a refer-

ence number means that the presence of a given species on El Hierro was questioned by the author(s) of the quoted paper. Species

new to El Hierro in bold print.

No. Species

1 Chilocorus canariensis Crotch, 1874

2 Parexochomus nigripennis (Erichson, 1843)

3 Cryptolaemus montrouzieri Mulsant, 1853

4 Nephus flavopictus (Wollaston, 1854)

5 Nephus incisus (Lindberg, 1950)

6 Rhyzobius litura (Fabricius, 1787)

7 Rhyzobius lophanthae (Blaisdell, 1892)

8 Scymnus (Pullus) canariensis Wollaston, 1864

9 Scymnus (Mimopullus) cercyonides Wollaston, 1864

10 Scymnus (Mimopullus) marinus Mulsant, 1850

11 Scymnus (Scymnus) rufipennis Wollaston 1864

12 Scymnus (Scymnus) nubilus Mulsant, 1850

3 Stethorus tenerifensis Fursch, 1987

14 Stethorus wollastoni Kapur, 1948

15 Coccinella miranda Wollaston 1864

16 Coccinella septempunctata algerica Kovat, 1977

17 Mpyrrha octodecimguttata (Linnaeus, 1758)

18 Hippodamia variegata (Goeze, 1777)

19 Novius canariensis Korschefsky, 1935

20 Novius cruentatus (Mulsant, 1846)

ZA Rodolia cardinalis (Mulsant, 1850)

22 Pharoscymnus decemplagiatus (Wollaston, 1857)

' reported as Exhochomus (sic!) flavipes

> reported as Nephus fractus Wollaston

> reported as Pullus pallidivestis Muls.

This study Literature data

+ 15286. 2708; 10. 12

1; 2,6,-7, 8,9!

1,7,8

27, 3, 4, 6, 8

2 Oz7 b,09 UL cb2

2,6, 7,8

1, 2, 6, 7, 8, 10, 11, 12

2.3 Oh. Ole

1322 ORO Tn

1, 4, 6, 7, 8

1. 27467, 7-8

153336; FB

_ 100k 8. LIPS sb?

+ + + + + + + 4

2 SO ore, 9, Nl TD

+ + + + +

1,2, 6?, 7,8

4, 6,77, 8

1,4,6,7,8

“reported as Scymnus levaillandi (sic!) Muls. (2) and S. levaillanti Mulsant, 1850 (6)

> reported by Wollaston as Scymnus minimus (Rossi), a synonymic name of Stethorus pusillus (Herbst, 1797). Later Kapur (1948)

included the specimens collected by Wollaston in a newly described S. wollastoni.

References: 1 — Eizaguirre (2007), 2 — Franz (1995), 3 — Furrsch (1987), 4 — Israelson et al. (1982), 5 — Kovar (1977), 6 — Machado &

Oromi (2000), 7 — Nicolas (2010), 8 — Oromi et al. (2010), 9 — Torres del Castillo et al. (1992), 10 — Uyttenboogaart (1935), 11 —

Wollaston (1864), 12 — Wollaston (1865)

the Canary Islands very recently: O. v-nigrum was first

time recorded in the archipelago in 2014 (Tenerife and

La Palma) (as Harmonia axyridis (Pallas, 1773), see Ro-

manowski et al. 2020a) and P. flexibilis in 2016 (Fuerte-

ventura) (Romanowski et al. 2018). It can be assumed

that in the near future these newcomers will also reach

the western islands of the Canary archipelago, including

El Hierro.

Acknowledgments. We thank Jifi Kratky and Jan Pelikan for

providing specimens used in this study. Weronika Romanows-

ka assisted in collecting specimens, Matgorzata Grochowska

assisted in laboratory work.

Bonn zoological Bulletin 69 (2): 249-261

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Bonn zoological Bulletin 69 (2): 263-274

2020 - Sinclair B.J. et al.

https://do1.org/10.20363/BZB-2020.69.2.263

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org: pub: BDS9F89E-3684-47A D-BB67-446E34FO0ASC

Revision of the aquatic dance flies (Diptera: Empididae: Clinocerinae)

described by F. Vaillant in two 1960 publications

Bradley J. Sinclair’’, Igor V. Shamshev? & Jean-Luc Gattolliat?

'Canadian National Collection of Insects & Canadian Food Inspection Agency, OPL-Entomology, K.W. Neatby

Bldg., C_E.F,, 960 Carling Ave., Ottawa, ON, KIA 0C6, Canada

?Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, RU-199034, Russia

3Musée Cantonal de Zoologie, Palais de Rumine, 1015 Lausanne, Switzerland; Department of Ecology and Evolu-

tion, Biophore, University of Lausanne, CH-1015 Lausanne, Switzerland

* Corresponding author: Email: bradley.sinclair@canada.ca

'urn:Isid:zoobank.org:author:45 16327F-B73E-456C-927F- 1 8EFBOB9E08B

2urn:Isid:zoobank.org:author:569F41CC-EC2B-4CF0-802A-8D7056C72C93

3urn:lsid:zoobank.org: author: 9F2CBF71-33B8-4CD7-88D3-85D7ES528AEA5

Abstract. The specimens from two 1960 publications by Frang¢ois Vaillant on aquatic empidids (Diptera: Empididae:

Clinocerinae) are examined. Lectotypes are designated for Atalanta minutissima Vaillant, 1960, A. orientalis Vaillant,

1965, A. stackelbergi Vaillant, 1960, Oreothalia rupestris Vaillant, 1960, Wiedemannia bicolorata Vaillant, 1960, W. fo-

liacea Vaillant, 1960, W. fumosa Vaillant, 1960, W. saltans Vaillant, 1960, W. similis Vaillant, 1960, Seguyella rostrata

Vaillant, 1960 and S. tadjikistana Vaillant, 1960. The following taxonomic changes are proposed: Atalanta nigra orientalis

Vaillant, 1965 is now Clinocera orientalis (Vaillant, 1965), stat. rev. and Clinocera vaillantiana sp. nov. is named for

Atalanta (Atalanta) rufipes sensu Vaillant.

Key words. Palaearctic, Nearctic, new species, lectotypes, aquatic dance flies.

INTRODUCTION

The French entomologist Frangois Vaillant (1920— )

described a series of new species of aquatic empidids

(Clinocerinae) in two 1960 publications. Vaillant (1960a)

listed new distribution records and described three new

species from specimens he collected in Tennessee, USA

and later Vaillant (1960b) published new species records,

a new genus and eight new species from Kazakhstan,

Tajikistan and Turkmenistan from specimens borrowed

from the Zoological Institute of Russian Academy of Sci-

ences in St. Petersburg. In the latter publication, a portion

of the specimens upon which these species were based

were retained in his private collection and most of the

loaned material was returned. Unfortunately, the material

that was returned was inadequately labelled and determi-

nation of the type status was hindered by the inability to

assemble the entire type series for each species.

Between 2010 and 2013, the private Diptera, Cole-

optera and Trichoptera collections of Fran¢ois Vaillant,

representing around 12,000 slides and numerous pinned

specimens, were donated to the Musée cantonal de zool-

ogie, Lausanne, Switzerland (MZLS). Among this valu-

able collection were around 1,300 slides of Empididae

including type material for about 70 species. This study

Received: 18.08.2020

Accepted: 24.09.2020

of the Clinocerinae specimens from the 1960 publications

was initiated to answer several long outstanding questions

for BJS and IVS and represents only a small portion of

the aquatic dance fly collection. This is a follow-up study

to Sinclair & Shamshev (2019) which investigated only

a short series of specimens determined as Wiedemannia

lota Walker, 1851. Much work remains in identifying all

the type specimens from this vast donation.

MATERIAL AND METHODS

This study is based on material housed in the Musée can-

tonal de zoologie, Lausanne, Switzerland (MZLS) and

the Zoological Institute of the Russian Academy of Sci-

ences, St. Petersburg, Russia (ZIN).

The label data for type specimens are cited verbatim

and listed beginning with the top label continuing to the

bottom label. Data on labels are listed within quotation

marks, with a change in label represented by a semico-

lon. A new line on a label is indicated by a slash (/). Any

additional information not found on the labels is given in

square brackets.

The status of the type material of the new species de-

scribed in Vaillant (1960a, b) was not distinctly outlined.

Corresponding editor: X. Mengual

Published: 27.10.2020

264

For several species there was no statement concerning

name-bearing types and in these cases all specimens list-

ed are treated as syntypes according to the International

Code of Zoological Nomenclature (ICZN 1999) Article

73.2.1. In most cases, Vaillant (1960a, b) used the ex-

pression “type choisi du ...” to indicate either the type

locality or the collection locality of a type specimen, and

in our opinion this was not an explicit statement of type

fixation. The identification of the name-bearing specimen

was further inhibited by the lack of explicit labelling.

Although all specimens examined by us bear Vaillant’s

determination label, no “type” labels were attached. The

ICZN (1999) Article 73.1.1 states: “If an author when

establishing a new nominal species-group taxon states

in the original publication that one specimen, and only

one, 1s the holotype, or “the type” [French version of

ICZN: “le type’], or uses some equivalent expression,

that specimen is the holotype fixed by original designa-

tion”. On the basis of the use of the above expression by

Vaillant without a definite article, in combination with

the absence of type labelling, we interpret that a particu-

lar name-bearing specimen was not established in these

publications. All specimens listed by Vaillant under ma-

terial examined sections are treated as syntypes. A simi-

lar interpretation of type material status was discussed by

Richet et al. (2013).

RESULTS

Material from Vaillant (1960a)

During a visit to Tennessee (USA) in August 1955, Vail-

lant collected aquatic insects from streams and waterfalls

in Great Smoky Mountains National Park of Tennessee

and North Carolina (USA). This material later formed the

basis of several publications on Thaumaleidae (Vaillant

1959a), Psychodidae (Vaillant 1959b) and Clinocerinae

(Empididae) (Vaillant 1960a). In the latter publication,

Vaillant (1960a) described three new species. The fol-

lowing species were listed in this publication and all

specimens associated with his identifications were stud-

ied if available. All material was poorly labelled in terms

of type material and the depository of the types was not

specified in the publication. Fortunately, Vaillant’s de-

scriptions and illustrations have readily facilitated spe-

cies identification by subsequent taxonomists without the

need for direct comparisons with type specimens.

Bonn zoological Bulletin 69 (2): 263-274

Bradley J. Sinclair et al.

Clinocera sp.

Atalanta (Hydrodromia) sp.: Vaillant, 1960a: 119.

Material. Le Comte, 10.vili.1955 (1 9).

Remarks. The genus name Atalanta Meigen, 1800 was

suppressed by the ICZN (1963) and Sinclair (1995) listed

the subgenus Hydrodromia Macquart, 1835 as a junior

synonym of Clinocera Meigen, 1803.

The single female specimen listed by Vaillant (1960a)

was not found among the donated collection.

Roederiodes recurvatus Chillcott, 1961

(Fig. 1)

Roederiodes recurvatus Chillcott, 1961: 424. Type local-

ity: Old Chelsea, Quebec, Canada.

R. recurvatus: Melander, 1965: 468 (catalogue); Wilder,

1981a: 419 (review); Sinclair, 1995: 698 (checklist).

Roederiodes junctus Coquillett, 1901: Vaillant, 1960a:

117 (not Coquillett) (Wilder 1981a: 419).

Material examined. USA. Tennessee: Roaring Fork

Creek [near Gatlinburg, 600 mJ], 20.vili.1955, F. Vail-

lant (slides: GBIFCH00606816: 1 3, 2 99; GBIF-

CH00606817: 1 3; GBIFCH00606818: 2 4; pinned:

GBIFCH00654925: 1 ?¢ [abdomen missing]; all MZLS).

Remarks. Vaillant (1960a) identified and labelled the

above material as Roederiodes junctus (Fig. 1). This was

a misidentification of R. recurvatus (see Chillcott 1961:

fig. 17).

Oreothalia rupestris Vaillant, 1960

(Fig. 2)

Oreothalia rupestris Vaillant, 1960a: 118. Type locality

(by lectotype designation): Laurel Falls, Tennessee,

USA.

O. rupestris: Melander, 1965: 467 (catalogue); Wilder,

1981b: 463 (revision); Sinclair, 1995: 696 (checklist).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

(Fig. 2): “GBIFCH/ 00606820”; “LECTOTYPE/ Oreo-

thalia rupestris/ Vaillant, 1960// des. Sinclair,/ Sham-

shev, Gattolliat/ 2020 [red label]; “Oreothalia rupes-

tris/ VAILLANT/ Laurel Falls/ Appalachian Mountains/

28. VIII.1955, F. VAILLANT” (MZLS, slide). PARA-

LECTOTYPES: USA. Tennessee: same data as lec-

totype except, GBIFCH00606821 (1 3, MZLS, slide);

same data except, GBIFCH00606822 (1 3, MZLS, slide);

same data except, GBIFCH00606823 (1 3, 1 9, MZLS,

slide); same data except, GBIFCH00606824 (1 4, 1 9,

MZLS, slide); same data except, GBIFCH00606825

©ZFMK

Revision of the aquatic dance flies described by F. Vaillant in two 1960 publications 265

GBIFCH Bae a: ar

s GBIFCH Be

00606820 90606830

GBIFCH

00606817

GBIFCH §/EGR

00606828 Bs

GBIFCH Re

00606816

Reederiosdes juncta

COQuictetr

ee |

| tris

Roaring fork Creeh , VAILLANT

Agpelachian Nounterns rel Falls

| eeeeaents lachian Movntains

| 2o0-vans 1955

| UB Man 198s

| F. VAILLANT hate Ae .

F. VAILLANT

—_—-

a — ee

- GBIFCH

~ 00854926

GBIFCH PS + 2 GBIFCH oi GBIFCH ge

oosose4o Kime? & = 0684 | on6o6e42

) eumeait

WE yee state.

Figs 1—6. Specimens from Vaillant (1960a). 1. Roederiodes junctus (=R. recurvatus Chillcott), three slides. 2. Oreothalia rupestris

Vaillant, lectotype and two paralectotype slides. 3. O. rupestris Vaillant, pinned males. 4. O. rupestris Vaillant, labels on pin. 5. Wie-

demannia fumosa Vaillant (=Trichoclinocera fumosa), lectotype and two paralectotype slides. 6. Wiedemannia saltans Vaillant

(=Trichoclinocera hamifera (Melander)), lectotype and two paralectotype slides.

Bonn zoological Bulletin 69 (2): 263-274 ©ZFMK

266

(1 3, 1 2, MZLS, slide); same data except, GBIF-

CH00606826 (1 3, MZLS, slide); same data except,

GBIFCH00606827 (1 3, 1 2, MZLS, slide); Gatlinburg

to Clingmans Dome Rd., 900 m, 28.viii1.1955, F. Vaillant

(slides: GBIFCH00606828: 4 299°, GBIFCH00606829:

1 3, GBIFCH00606830: 1 3, 1 9; all MZLS); Mt. Le

Conte, 10.vii1.1955, 1950 m, F. Vaillant (slide: GBIF-

CH00606831: 1 4, MZLS).

Additional material. USA. Tennessee: Laurel Falls,

28.vili.1955, F. Vaillant (pinned: GBIFCH00654926:

8 63, GBIFCH00654927: 9 29, MZLS; 3 empty pins

without specimens, ZIN).

Remarks. Vaillant (1960a) designated Laurel Falls as

the type locality (8 males and 4 females) and all speci-

mens were found mounted on slides, but the collection

date was published as 20 August instead of 28 August as

stated on the labels (Fig. 2). The pinned specimens from

Laurel Falls (Figs 3, 4) listed under Additional material

were not reported among the material examined by Vail-

lant (1960a) and are not considered part of the original

syntype series. Vaillant donated some specimens to ZIN

but we found only empty pins.

Oreothalia rupestris 1s the only described species of

this endemic Nearctic genus in the East, occurring only

in the Great Smoky Mountains (Wilder 1981b; Sinclair

unpubl. data). There is a probable undescribed species

based on a single female specimen from Gainesville,

Florida, distinguished from O. rupestris on the basis of

wing venation, pleural colouration and chaetotaxy (Sin-

clair 1995).

Trichoclinocera fumosa (Vaillant, 1960)

(Fig. 5)

Wiedemannia (Roederella) fumosa Vaillant, 1960a: 119.

Type locality (by lectotype designation): Roaring Fork

Creek, Great Smoky Mountains, Tennessee, USA.

W. (Roederella) fumosa: Melander, 1965: 469 (cata-

logue).

Seguyella fumosa (Vaillant): Vaillant, 1960b: 180 (new

combination).

Trichoclinocera fumosa (Vaillant): Sinclair, 1994: 1029

(new combination, revision).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

(Fig. 5): “GBIFCH/ 00606832”; “LECTOTYPE/ Wie-

demannia/ (Roederella) fumosa/ Vaillant, 1960/ des./

Sinclair, Shamshev,/ Gattolliat 2020 [red label]; “Se-

guyella fumosa/ VAILLANT/ Roaring Fork Creek/ Ap-

palachian Mountains [Great Smoky Mountains National

Park]/ 20. VIII.1955/ F. VAILLANT” (MZLS, upper left

specimen). PARALECTOTYPES: USA. Tennessee:

on same slide as lectotype (1 4, 2 29, MZLS, slide);

Bonn zoological Bulletin 69 (2): 263-274

Bradley J. Sinclair et al.

same data except, GBIFCH00606833 (3 do, MZLS,

slide); same data except, GBIFCH00606834 (1 3, 2 29,

MZLS, slide); same data except, GBIFCH00606835

(1 6, 2 99, MZLS, slide); same data except, GBIF-

CH00606836 (2 33’, 3 92, MZLS, slide); Little River,

3000 ft [1100 m, F. Vaillant], GBIFCH00654928 (1 3,

1 2, MZLS, pinned together on single mount).

Remarks. Vaillant (1960a) designated Roaring Fork

Creek as the type locality (16 males and 24 females) and

10 males and 8 females were located for this study.

Vaillant (1960b) transferred Wiedemannia fumosa to

a new genus, Seguyella Vaillant, 1960b, which 1s now

classified as a junior synonym of Trichoclinocera Col-

lin, 1941 (Sinclair 1994). This species was transferred

to Trichoclinocera and redescribed by Sinclair (1994),

where the species was shown to occur primarily in the

southern Appalachian Mountains from Virginia to north-

ern Georgia.

Trichoclinocera hamifera (Melander, 1928)

(Fig. 6)

Wiedemannia (Chamaedipsia) hamifera Melander, 1928:

233. Type locality: Beaverkill, New York, USA.

Wiedemannia (Roederella) saltans Vaillant, 1960a: 122.

Type locality (by lectotype designation): near Gatlin-

burg, Tennessee, USA.

Wiedemannia (Chamaedipsia) saltans: Melander, 1965:

469 (catalogue).

Seguyella saltans (Vaillant): Vaillant, 1960b: 180 (new

combination).

Trichoclinocera hamifera (Melander): Sinclair, 1994:

1030 (new synonym, revision).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

(Fig. 6): “GBIFCH/ 00606840’ 1 4”; “LECTOTYPE/

Wiedemannial/ (Roederella) saltans/ Vaillant, 1960/ des./

Sinclair, Shamshev,/ Gattolliat 2020 [red label]”; “Se-

guyella saltans/ VAILLANT/ Between Gatlinburg and

headquarters [Great Smoky Mountains National Park]/

Appalachian Mountains/ 21.VIII.1955/ F. VAILLANT”

(MZLS, slide). PARALECTOTYPES: USA. Tennes-

see: same data as lectotype except, GBIFCH00606841

(3 99, MZLS, slide); same data except, 22.vili.1955,

GBIFCH00606842 (1 , MZLS, slide); Greenbrier

Cove [600 m], 17.vi.1955, F. Vaillant (slides: GBIF-

CH00606837: 3 99; GBIFCH00606838: 1 4; GBIF-

CH00606839: 2 29, all MZLS).

Remarks. Vaillant (1960a) designated “between Gatlin-

burg, Tennessee and the headquarters of the Great Smoky

Mountains National Park” (3 males, 3 females) as the

type locality and 2 males and 3 females were located for

this study.

©ZFMK

Revision of the aquatic dance flies described by F. Vaillant in two 1960 publications 267

Vaillant (1960b) transferred Wiedemannia saltans to

the new genus Seguyella. This genus is a junior synonym

of Trichoclinocera Collin and S. saltans is a junior syn-

onym of Trichoclinocera hamifera (Sinclair 1994).

Trichoclinocera sp.

Wiedemannia (Philolutra) sp.: Vaillant, 1960a: 123.

Material. Between Gatlinburg and National Park head-

quarters, 22.viil.1955 (7 9).

Remarks. The seven female specimens identified by

Vaillant were not found among the donated collection.

The genus Wiedemannia Zetterstedt, 1838 does not occur

in the southern Appalachians and we assume that these

specimens belong to Trichoclinocera. There are at least

four species of 7richoclinocera present in the southern

Appalachian Mountains including 7. falcata Sinclair,

1994 and T. minor (Melander, 1928), in addition to the

two species above (Sinclair 1994).

Material from Vaillant (1960b)

Vaillant (1960b) borrowed a series of Clinocerinae spec-

imens collected in central Asia from A.A. Stackelberg

(ZIN). Vaillant (1960b) described eight new species,

identified four additional species of Clinocerinae and de-

scribed a new genus, Seguyella. Vaillant returned a por-

tion of the original loan and retained an unknown number

of specimens from his study for his private collection.

All material was poorly labelled in terms of type material

and the depository of the types was not specified. Fortu-

nately, Vaillant’s descriptions and illustrates have readily

facilitated species identification by subsequent taxono-

mists without the need for direct comparisons with type

specimens.

Clinocera minutissima (Vaillant, 1960)

(Fig. 15)

Atalanta (Atalanta) minutissima Vaillant, 1960b: 172.

Type locality (by lectotype designation): Khorog on

Gunt River (37°29'N 71°33'E), Tajikistan.

Clinocera minutissima (Vaillant): Chvala & Wagner,

1989: 330 (catalogue); Sinclair, 1995: 693 (checklist).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

(Fig. 15): [printed in Cyrillic] [Tajikistan]: “Khorog on

r. [=reka, river] Gunt/ Shugnan, 25.1x.[1]943./ Stackel-

berg”; “LECTOTYPE/ Atalanta (Atalanta)/ minutissima/

Vaillant, 1960/ des. Sinclair, Shamshev,/ Gattolliat 2020

[red label]; “GBIFCH/ 00596473”; “Atalanta/ (Atalan-

ta)/ minutissima VAILLANT </ Khorog, Pamir/ occi-

dental. Tadzikistan/ 25.1X.1943/ A.A. STACKELBERG

Bonn zoological Bulletin 69 (2): 263-274

coll./ F. VAILLANT [hand-written by Vaillant]” (1 3,

MZLS). PARALECTOTYPES: same data as lectotype

(2 53, MZLS, slides; 1 9, ZIN, pinned).

Remarks. Vaillant (1960b) designated the locality

“Khorog” as the type locality, which included two males

and two females. We identified three males and one fe-

male from the type series. Vaillant (1960b) also listed a

single female from “Kondara’”, but this specimen was not

found in either MZLS or ZIN.

Sinclair (1995) assigned this species to the C. lineata

group on the basis of the form of the surstylus (Sinclair

2008). Many species in this group, including C. minu-

tissima, possess facial setulae (defining feature of genus

Kowarzia Mik, 1882), but the male terminalia clearly

identify them as belonging to the genus Clinocera.

Clinocera orientalis (Vaillant, 1965) stat. rev.

(Figs 7-10)

Clinocera nigra Meigen, 1804: Vaillant, 1960b: 174 (as

Atalanta (Atalanta)).

Atalanta nigra orientalis Vaillant, 1965: 148. Type local-

ity (by lectotype designation): Kondara Canyon, valley

of Varzob River (38°48'N 68°48'E), Tajikistan.

Clinocera nigra orientalis (Vaillant): Sinclair, 1995: 693

(checklist).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled:

“Tprinted in Cyrillic] [Tajikistan] Atalanta/ (Atalanta)/

nigra (Meigen)/ 3 [hand-written by Vaillant, yellow la-

bel]”; “usch. [=uschelje, canyon] Kondara, dol. [=doli-

na, valley]/ r. [=reka, river] Varzob, Taj. [=Tajikistan]/

Stackelberg 6.x1.[1]944”; “Lectotypus/ Atalanta/ nigra

orientalis Vaillant, 1965/ design. Sinclair, Shamshev,

Gattolliat 2020” (ZIN, INS_DIP_ 0000606). PARALEC-

TOTYPE: same data as lectotype, GBIFCH00596472

(1 3, slide, MZLS).

Remarks. Vaillant (1960b) initially identified nine speci-

mens from Tajikistan as C. nigra Meigen. Vaillant (1965)

later re-evaluated his decision and concluded that these

Central Asian specimens differed in the male genitalia

and named a new subspecies (as A. (A). nigra orientalis)

for these specimens. No type or type locality was des-

ignated for this new subspecies. We consider the male

genitalia of C. nigra orientalis (see Vaillant 1965: figs 11,

1m) are sufficiently different from C. nigra to warrant

elevation to species. Only two of nine specimens listed in

Vaillant (1960b) could be found of this species.

©ZFMK

268 Bradley J. Sinclair et al.

| m. Ko BRApa, 01.

bs 3 4 ol

is |

Figs 7-10. Clinocera orientalis (Vaillant) stat. rev., male paralectotype. 7. Slide. 8. Terminalia. 9. Habitus. 10. wing.

Clinocera stackelbergi (Vaillant, 1960)

(Fig. 16)

Atalanta (Kowarzia) stackelbergi Vaillant, 1960b: 174.

Type locality (by lectotype designation): Khorog on

river Gunt (37°29'N 71°33’'E), Tajikistan.

Clinocera (Kowarzia) stackelbergi (Vaillant): Chvala &

Wagner, 1989: 334 (catalogue).

Clinocera stackelbergi (Vaillant): Sinclair, 1995: 693

(checklist).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

(Fig. 16): “Atalanta/ (Kowarzia)/ stackelbergi/ VAIL-

LANT/ 4/F. VAILLANT det. [yellow label, hand-written

by Vaillant]”; “[printed in Cyrillic] Khorog nar. [na reke,

=on river] Gunt/ Shugnan 25.1x.[1]943, Stackelberg”:

“LECTOTYPUS/ Atalanta (Kowarzia)/ stackelbergi

Vaillant, 1960/ des. Sinclair, Shamshev, Gattolliat/ 2020

[red label]” (ZIN, INS DIP 0000607). PARALEC-

TOTYPES: Tajikistan: same data as lectotype (2 33,

1 2, ZIN; GBIFCH00602303:1 <4, MZLS, slide); same

data as lectotype except, 26.ix1943 (1 6, ZIN); Kondara

Canyon, valley of river Varzob, Stackelberg, 6.x1.1944,

GBIFCH00602304 (1 3', MZLS, slide).

Remarks. Vaillant (1960b) did not designate a type spec-

imen or type locality for this species. A total of six male

and two female syntypes were listed, and six male and

one female syntypes were found during this study.

Bonn zoological Bulletin 69 (2): 263-274

Despite the presence of facial setulae, a defining char-

acter of the genus Kowarzia, Sinclair (1995) transferred

this species to Clinocera and assigned it to the C. /ineata

group on the basis of male terminalia.

Clinocera stagnalis (Haliday, 1833)

Heleodromia stagnalis Haliday, 1833: 159. Type locali-

ty: Holywood, Downshire, Ireland.

Material examined. Tajikistan: Stalinabad [=Dushan-

be] valley of Gulbisty River, 20.iv.1943 (1 3, ZIN);

Stalinabad [=Dushanbe], loess hills, 24.1v.1943, Stackel-

berg (1 Q, ZIN), 5.iv.1944 (1 9, ZIN); Stalinabad [=Du-

shanbe], foothils, 18.iv.1943, Goussakovsky (1 9, ZIN);

Tavil-dara, N slope of Darvazskiy Ridge, 10.x.1942 (1 3,

ZIN); Viskharvi on Pyandzh River, 21.x.1942, Stackel-

berg (1 4, ZIN).

Remarks. This is a very widespread species, found

across the Palaearctic Region and the arctic and Rocky

Mountains of the Nearctic Region (Sinclair 2008).

Clinocera vaillantiana sp. nov.

(Figs 11-14)

Atalanta (Atalanta) rufipes Vaillant, 1960b: 174 (not

Bezzi).

Type material examined. HOLOTYPE <}, labelled

(Fig. 11): “[printed in Cyrillic] [Tajikistan] usch. [=us-

©ZFMK

Revision of the aquatic dance flies described by F. Vaillant in two 1960 publications

ym. Kouqapa, qon.

p06 ke i

AeOe|

i Se —_—

} Atalanta (Atalanta)

| ufipes | ‘Bezzi

Catton de Kondaca

Masné da Hoar |

Tadaihistan , 2OWwl9ue

pele as TSHSUB ERG. coll-

oBIECH wane , .

~ 00596474 Pa fh

269

Figs 11-14. Clinocera vaillantiana sp. nov., male holotype. 11. Slide. 12. Terminalia. 13. Habitus. 14. wing.

chelje, canyon] Kondara, dol. [=dolina, valley]/r. [=reka,

river] Varzob, Taj. [=Tajikistan]/ Stackelberg 20.1Vv.

[19]44”; “HOLOTYPE/ Clinocera vaillantiana/ Sin-

clair, Shamshev,/ Gattolliat, 2020”; “Atalanta (Atalanta)/

rufipes Bezzi 4/ Cafion de Kondata/ Massif de Hissar/

Tadzikistan, 20.[V.1944/ A.A. STACKELBERG coll./ F.

VAILLANT”; “GBIFCH/ 00596471” (MZLS, slide).

Description. Male. Head with broad face; ocellar seta

3/4 length of scutal setae; postpedicel short ovate; aris-

ta-like stylus slender. Scutum with long setae; subequal

in length with scutellar setae; 1 postpronotal seta weaker

than notopleural setae; 1 presutural postalar seta; 2 no-

topleural setae; 1 postsutural postalar seta; 6 dorsocentral

setae. Legs with coxae and femora pale brown (Fig. 13);

remaining legs dark brown; fore femur with biserial row

of ventral setae, setae half as long as width of femur; fore

tibia with erect ventral setae. Wing infuscate (Fig. 14),

lacking spots or clouding; pterostigma absent; auxiliary

crossveins absent; cell dm produced distally; halter pale

brown.

Male terminalia (Fig. 12; Vaillant 1960b: figs 2c—f):

Clasping cercus oval, strongly tapered apically. Surstylus

digitiform with sharply pointed subapical process. Phal-

lus slightly sinuous, not expanded apically; distiphallus

slender and arched.

Etymology. This species is a patronym in honour of

Francois Vaillant in recognition of his efforts to describe

the diversity of aquatic empidids and he will be 100 years

of age in 2020.

Bonn zoological Bulletin 69 (2): 263-274

Remarks. Vaillant (1960b: figs 2c—f) considered the sin-

gle specimen he identified as Atalanta (Atalanta) rufipes

(Bezzi, 1899) to be significantly different from C. nigra

rufipes [originally Atalanta (Atalanta) nigra rufipes| and

consequently elevated rufipes sensu Vaillant to species

level. Sinclair (2007) examined syntype specimens of

C. rufipes Bezzi and proposed this species as a junior

synonym of C. nigra. On the basis of the illustration of

the male genitalia of C. rufipes in Sinclair (2007: fig. 1),

the male genitalia of this Central Asian specimen (Vail-

lant 1960b: figs 2c—f; Fig. 12) is clearly not conspecific,

and represents a new species described herein.

Trichoclinocera cyanescens (Vaillant, 1960)

(Fig. 17)

Seguyella cyanescens Vaillant, 1960b: 180. Type local-

ity: “Tavil) Dara” [= Tavildara] (38°41'N 70°29'E),

Tajikistan.

Seguyella cyanescens. Chvala & Wagner, 1989: 322 (cat-

alogue).

Trichoclinocera cyanescens (Vaillant): Sinclair, 1994:

1015 (new combination).

Type material examined. HOLOTYPE <j, labelled

(Fig. 17) [printed in Cyrillic] [Tajikistan]: “Tavil-dara

[=Tavildara, 38°41'N 70°29’E], N/ skl. [=sklon, slope]

Darvaz. [=Darvazskiy] khr. [=khrebet, ridge] 9,x/ Stack-

elberg [1]942”; “GBIFCH/ 00606848”; “HOLOTYPE/

Seguyella cyanescens/ Vaillant, 1960”; “Seguyella cya-

nescens/ VAILLANT </ Tavilj Dara, Massif de/ Darvaz.

©ZFMK

270

Tadzikistan/ 9.X.1942/ A.A. STACKELBERG coll./ F.

VAILLANT” (MZLS, slide).

Remarks. This species was described on the basis of a

single male specimen. Vaillant removed this specimen

from the pin and made a slide mount, including the orig-

inal locality label. A holotype label has been attached.

Bradley J. Sinclair et al.

Trichoclinocera rostrata (Vaillant, 1960)

(Fig. 18)

Seguyella rostrata Vaillant, 1960b: 181. Type locality (by

lectotype designation): Kondara Canyon, valley of riv-

er Varzob (38°48'N 68°48'E), Tajikistan.

Seguyella rostrata: Chvala & Wagner, 1989: 322 (cata-

logue).

Trichoclinocera rostrata (Vaillant): Sinclair, 1994: 1016

(new combination).

—s«GBIFCH ESE

00596475

GBIFCH

00596474

‘GBIFCH =f

es 00596473

Atalanta (

minutissima .

Khereg ’ Pamir « ial

Sccicental. Tadzihistan

2511x1943

A‘A'STACKELBERG call.

F. VAILLANT

GBIFCH

in 00606848

GBIFCH

00606849

Seqeyetla costrats

ae VATCCAIT OF

| Bedile de Kondarca . Masntl

de Wissac, Tadzikistan,

2O+IV 194g i

_ A*ASTACRELBERG coll

F. VAILLANT

Xopor na p. [yur

Iyruan 25.)x.943

Timareavbeps

Zoological Institute

| St. Petersburg

INS_DIP_0000607

Figs 15-19. Specimens from Vaillant (1960b). 15. Clinocera minutissima (Vaillant), lectotype and two paralectotype slides.

16. Clinocera stackelbergi (Vaillant), lectotype and labels. 17. Seguyella cyanescens Vaillant (=Trichoclinocera cyanescens), holo-

type slide. 18. Seguyella rostrata Vaillant (=Trichoclinocera rostrata), two paralectotype slides. 19. Seguyella tadjikistana Vaillant

(= Trichoclinocera tadjikistana), paralectotype slide.

Bonn zoological Bulletin 69 (2): 263-274

©ZFMK

Revision of the aquatic dance flies described by F. Vaillant in two 1960 publications 201

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

[printed in Cyrillic] [Tajikistan]: “Seguyella/ rostra-

ta/ VAILLANT/ 6/ F. VAILLANT det. [yellow label,

hand-written by Vaillant]’; “usch. [=uschelje, canyon]

Kondara, dol. [=dolina, valley]/ r. [reka, river] Varzob,

Tadj. [=Tajikistan]/ Stackelberg 20.iv.[19]44”’; “Tricho-

clinocera/ rostrata/ det. BJ. Sinclair 1993”; “LEC-

TOTYPUS/ Seguyella/ rostrata Vaillant/ des. Sinclair,

Shamshev, Gattolliat 2020 [red label]” (ZIN, INS_

DIP_0000608). PARALECTOTYPES: Tajikistan:

same data as lectotype (2 Jo, 7 92, ZIN); same data

as lectotype (Fig. 18) (slides: GBIFCH00606849: 1 2;

GBIFCH00606850: 1 @; pinned: GBIFCH00654933:

1 2; GBIFCH00654934: 1 9; GBIFCH00654935: 1 2;

all MZLS).

Remarks. Vaillant (1960b) did not designate a type spec-

imen for this species and examined a total of six male and

11 female specimens (= syntypes), of which six males

and nine females were found during this study. Sinclair

(1994) transferred this species to the genus 7richoclino-

cera after studying two male and two female syntype

specimens borrowed from ZIN, but a lectotype was not

designated by Sinclair (1994).

Trichoclinocera tadjikistana (Vaillant, 1960)

(Fig. 19)

Seguyella tadjikistana Vaillant, 1960b: 184. Type locality

(by lectotype designation): Dushanbe, Tajikistan.

Seguyella tadjikistana: Chvala & Wagner, 1989: 322 (ca-

talogue).

Trichoclinocera tadjikistana (Vaillant): Sinclair, 1994:

1016 (new combination).

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

[printed in Cyrillic]: “Seguyella/ tadjikistana/ VAIL-

LANT/ #m/ F. Vaillant dét. [yellow label]”; “Stalinabad

[= Dushanbe]/ Tajik. [= Tajikistan] predgorja [= foot-

hills], Goussakovsky 18.iv.[19]43,”; “Trichoclinocera/

tadjikistana/ Det. B.J. Sinclair 1993”; “LECTOTYPUS/

Seguyella/ tadjikistana Vaillant/ des. Sinclair, Shamshev,

Gattolliat 2020 [red label]” (ZIN, INS DIP 0000609).

PARALECTOTYPES: Tajikistan: same data as lecto-

type (1 9, ZIN); Viskharvi on Pyandzh River, Tajikistan,

21.x.1942, Stackelberg (1 9, ZIN); Tavil-dara, N slope of

Darvazskiy Ridge, 7-11.x.1942, A.A. Stackelberg (1 3,

4 29, ZIN: 3 examined and dissected by B.J. Sinclair);

same data except, GBIFCH00606851 (Fig. 19) (1 2,

MZLS, slide).

Remarks. Vaillant (1960b) designated Viskharvi as the

type locality, which was represented by one male and

one female specimen. Only the female specimen was

Bonn zoological Bulletin 69 (2): 263-274

found and the male specimen appears to be lost. We have

chosen a lectotype male from Dushanbe, which is some

200 km east of Viskharvi.

Sinclair (1994) transferred this species to the genus

Trichoclinocera after studying two male and two female

syntype specimens borrowed from ZIN, but did not des-

ignate a lectotype.

Wiedemannia bicolorata Vaillant, 1960

(Fig. 20)

Wiedemannia (Chamaedipsia) bicolorata Vaillant,

1960b: 175. Type locality (by lectotype designation):

Kondara Canyon, valley of Varzob River, Tajikistan.

Wiedemannia (Chamaedipsia) bicolorata. Chvala &

Wagner, 1989: 325 (catalogue); Sinclair, 1995: 713.

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

[printed in Cyrillic]: “Wiedemannia/ (Chamaedipsia)/ bi-

colorata/ VAILLANT/ 2/ F. Vaillant dét. [yellow label]’”;

“usch. [=uschelje, canyon] Kondara, dol./ r. [= dolina

reki, valley of river] Varzob, Taj. [= Tajikistan]/ Stackel-

berg 7.x1.[1]944”; “LECTOTYPUS/ Wiedemannia (Cha-

maedipsia)/ bicolorata Vaillant/ des. Sinclair, Shamshev,

Gattolliat 2020 [red label]” (ZIN, INS_DIP_0000610).

PARALECTOTYPES: Tajikistan: same data as lecto-

type (1 &, 3 2, ZIN; including 1 3 and 1 @ on one

pin); Rakhaty, Gissarskaya valley, 5.vii.1943, Stackel-

berg (3 99, ZIN, pinned); Tavil-dara, N slope of Dar-

vazskiy Ridge, 7.x.1942, Stackelberg (1 3’, ZIN, pinned);

Viskharvi on Pyandzh River, 21.x.1942, A.A. Stackel-

berg, GBIFCH00606843 (1 <4; MZLA, slide); same data

except, GBIFCH00606844 (1 6, MZLS, slide); same

data except, GBIFCH00654930 (1 4, MZLS, pinned);

Kovron, near Kalay-khumb, 20.x.1942, A.A. Stackel-

berg, GBIFCH00654929 (1 9, MZLS, pinned; 1 9, ZIN).

Remarks. Vaillant (1960b) designated “Canon de Kond-

ara” as type locality and he studied three males and four

females, of which two male and three female specimens

were found during this study. Several pairs of facial setae

are present on a number of specimens.

Wiedemannia fallaciosa (Loew, 1873)

Clinocera fallaciosa Loew, 1873: 44. Type locality:

“Pannonia inferiori et in confinibus Daciae regionibus

(Kowarz)” ex titulo [Herculesbad, Romania].

Material examined. Kazakhstan: Alma-Ata, Pogan-

ka River, on stones, 8—24.vi1.1942, A.A. Stackelberg

(3 3S, 1 9, ZIN). Tajikistan: Tavil-dara, N slope of

Darvazskiy Ridge, 7 and 9.x.1942, A.A. Stackelberg

(2 92, MZLS; 13 43, 12 29, ZIN); Kalai-khumb, Dar-

vaz, 21.viii.1943, A.A. Stackelberg (2 J, MZLS; 4 99,

©ZFMK

2t2 Bradley J. Sinclair et al.

ZIN); Stalinabad [=Dushanbe], foothills, 18.1v.1943,

V.V. Gussakovskij (1 4, MZLS).

Remarks. Some pinned specimens (MZLS) were found

partially destroyed by dermestids.

Wiedemannia foliacea Vaillant, 1960

(Fig. 21)

Wiedemannia (Chamaedipsia) foliacea Vaillant, 1960b:

176. Type locality (by lectotype designation): Dushan-

be, valley of Dushanbinka River, Tajikistan.

Wiedemannia (Chamaedipsia) foliacea. Chvala & Wag-

ner, 1989: 325 (catalogue); Sinclair, 1995: 714.

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), 3 labelled

[printed in Cyrillic] [Tajikistan]: “Wiedemannia/ (Cha-

maedipsia)/ foliacea/ VAILLANT/ <@/ F. Vaillant dét.

[yellow label]”; “Stalinabad [now Dushanbe],/ dol.

[=dolina, valley]/ Dyushambinka [=Dushanbinka, a

river|/ Stackelberg 13.v.[19]43”; “LECTOTYPUS/

Wiedemannia (Chamaedipsia)/ foliacea Vaillant/ des.

Sinclair, Shamshev, Gattolliat 2020 [red label] (ZIN,

INS_DIP_0000611). PARALECTOTYPES: Tajiki-

stan: same data as lectotype, GBIFCH00606845 [in-

correctly interpreted as “Vallée du ruisseau Goulbista’’|

(1 4, MZLS, slide); same data as lectotype, GBIF-

CH00654932 (1 3, MZLS, pinned); same data as lecto-

type (1 3, 2 2, ZIN, pinned); Stalinabad [=Dushanbe],

foothills, 18.iv.1943, V.V. Goussakovsky (2 99, ZIN);

Stalinabad [=Dushanbe], foothills, 27.vu.1945, V.V.

GBIFCH

00606843

Goussakovsky, GBIFCH00606846 (1 4, MZLS, slide);

Viskharvi on Pyandzh River, 21.x.1942, A.A. Stackel-

berg, GBIFCH00654931 (1 9°, MZLS, pinned).

Additional material examined. Tajikistan: Stalinabad

[=Dushanbe], Botanical garden, 13.v.1943, Stackelberg

(1 9, ZIN).

Remarks. Vaillant (1960b) did not designate a type spec-

imen for this species. Vaillant (1960b) listed a total of

seven male and five female syntypes, of which five males

and five females were found for this study. Additional

material of this species has been identified in ZIN, which

was not included in the original loan to Vaillant.

Wiedemannia lota Walker, 1851

Wiedemannia lota Walker, 1851: 107. Type locality:

Wicklow County, Ireland.

Atalanta (Philolutra) astigmatica Stackelberg, 1937:

123. Type locality: “Kara-Kala” (= Magtymguly,

38°26'N 56°18'E), Turkmenistan.

Atalanta astigmatica: Sinclair & Shamshev, 2019: 163

(lectotype designation, new synonym).

Material examined. Turkmenistan: Kara-kala [now

Magtymguly], Syumy, viii.1931, P.A. Petristsheva (1 3,

MZLS; Sinclair & Shamshev 2019, fig. 3), ix.1931 (233,

ZIN (Sinclair & Shamshev 2019, figs 1, 2), 1 4, MZLS).

Tajikistan: Stalinabad [=Dushanbe], valley of Gulbista

River, 20.iv.1943, A.A. Stackelberg (1 4, ZIN; 1 3, on

slide GBIFCH00606855, 1 2, MZLS); Stalinabad [=Du-

foliacea Vaillant, two paralectotype slides. 22. Wiedemannia similis Vaillant, lectotype slide.

Bonn zoological Bulletin 69 (2): 263-274

©ZFMK

Revision of the aquatic dance flies described by F. Vaillant in two 1960 publications 273

shanbe], foothills, 18.iv.1943, V.V. Gussakovsk] (1 9,

MZLS); Rakhaty, Gissarskaya valley, 5.vi1.1943 (1 9,

ZIN); Tavil-dara, N slope of Darvazskiy Ridge, 7.x.1942,

A.A. Stackelberg (2 99°, ZIN).

Additional material examined. Tajikistan: Stalinabad

[=Dushanbe], valley of river Dyushambinka [=Dushan-

binka], 13.v.1943, Stackelberg (2 3, ZIN); Stalinabad

[=Dushanbe], valley of river Gulbista, 20.iv.1943, Stack-

elberg (1 4, ZIN).

Remarks. The specimens from Turkmenistan were dis-

covered to be the type specimens for Atalanta astigmati-

ca Stackelberg (Sinclair & Shamshev 2019).

Wiedemannia similis Vaillant, 1960

(Fig. 22)

Wiedemannia (Wiedemannia) similis Vaillant, 1960b:

178. Type locality (by lectotype designation): Viskhar-

vi, River Pyandzh, Tajikistan.

Wiedemannia (Wiedemannia) similis: Chvala & Wagner,

1989: 324 (catalogue); Sinclair, 1995: 716.

Type material examined. LECTOTYPE (here desig-

nated in order to fix identity of the species), labelled

(Fig. 22) [printed in Cyrillic] [Tajikistan]: “Viskharvi on

r. [=reka, river|/ Pyandzh, Taj. [=Tayjikistan]/ 21.x.[1]942,

Stackelberg”; “LECTOTYPE/ Wiedemannia/ (Wiede-

mannia) similis/ Vaillant, 1960/ des. Sinclair, Shamshev,/

Gattolliat 2020 [red label]”; “Wiedemannia (Wiedeman-

nia)/ similis VAILLANT 37/ Défilé de Viskharvi, Mas-

sif/ de Darvaz, Tadzikistan./ 21.X.1942/ A.A. STACK-

ELBERG coll./ F. VAILLANT”; “GBIFCH/ 00606847”

(MZLS, slide). PARALECTOTYPES: Tajikistan:

same data as lectotype (2 99, ZIN); Tavil-dara, N slope

of Darvazskiy Ridge, 9.x.1942, A.A. Stackelberg (2 99,

ZIN).

Remarks. Vaillant (1960b) did not designate a type spec-

imen for this species. He listed one male and five female

syntypes, of which one male and four females were found

during this study.

Acknowledgements. Christophe Daugeron (Paris Muse-

um) is thanked for directing the search by BJS and IVS for

the types of Vaillant to Lausanne. Jim O’ Hara (Ottawa),

Patrice Bouchard (Ottawa) and Neal Evenhuis (Honolu-

lu) are thanked for discussions concerning type material

status. Ian Quintas and Maud Liégeois (MZLS) greatly

contributed to this study by inventorying and digitaliz-

ing the 1300 slides of the Empididae collection deposited

by Francois Vaillant at MZLS. Alexey Kovalev helped

to take photos in ZIN. The study of IVS was performed

in the frames of the Russian State Research Project no.

Bonn zoological Bulletin 69 (2): 263-274

AAAA-A19-119020690101-—6. Marija Ivkovic¢ and an

anonymous reviewer kindly reviewed the manuscript.

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©ZFMK

Bonn zoological Bulletin 69 (2): 275-291

2020 - Kefelioglu H. et al.

https://do1.org/10.20363/BZB-2020.69.2.275

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub: EA017B83-DD67-45CA-9555-6DB9D261 A40D

Taxonomic revision of the Levant moles of Turkey

(Mammalia: Talpidae)

Haluk Kefelioglu', Boris KryStufek?, Ahmet Yesari Selcuk*®, Rainer Hutterer** & Jonas J. Astrin*

"3 Department of Biology, Faculty of Science, Ondokuz Mayis University, Samsun, Turkey

? Slovenian Museum of Natural History, Presernova 20, SI-1000 Ljubljana, Slovenia

*+° Zoologisches Forschungsmuseum Alexander Koenig, Leibniz-Institut fiir Biodiversitat der Tiere, Adenauerallee 160,

D-53113 Bonn, Germany

* Corresponding author: Email: R. Hutterer@leibniz-zfmk.de

'urn:|Isid:zoobank. org: author:592452A F-02D3-4DC3-A350-ODFCE829A 3F5

?urn:lsid:zoobank.org:author: FB4835B1-61 8E-4A0E-8917-078A90328D97

3urn:|sid:zoobank. org:author:2F906968-32C8-4359-AC96-76049F6E229B

4urn:lsid:zoobank.org: author: 16023337-0832-4490-89A9-846AC3925DD8

>urn:Isid:zoobank.org:author:50661540-FD30-4A BA-8415-6B3069105E93

Abstract. This paper examines the distribution and the morphological and genetic variation of 7Zalpa levantis. Previous

records from Thrace were re-identified as 7a/pa martinorum, restricting the range of 7alpa levantis to northern Asia Minor

and the Caucasus in Georgia, Armenia and Russia. Within 7a/pa levantis, we found three moderately distinct populations

in western, central, and eastern Turkey. While the central one is 7: /. Jevantis and the eastern one 7! /. transcaucasica, the

western subspecies had not been recognized before and is therefore named as a new subspecies.

Key words. Cytochrome 5, molecular taxonomy, morphology, phylogeography, subspecies, 7alpa levantis, Talpa marti-

norum.

INTRODUCTION

Mammalian systematics is dynamic and new species are

continuously being recognized. The number of mammal

species, estimated at 5,416 in 2005 (Wilson & Reeder

2005) increased to 6,495 just 13 years later (Burgin et al.

2018), an astonishing 20% increase. This progress was

at least partly generated by a wide application of new re-

search tools, above all the highly effective DNA-based

methods which are capable of delimiting morphological-

ly cryptic species (Baker & Bradley 2006).

Our focus in this study is the evolutionary divergence,

taxonomy and species richness of the Eurasian mole ge-

nus 7alpa Linnaeus, 1758 in Turkey. The genus is endem-

ic to the western Palaearctic region and is well known

to the lay public for its distinctive external appearance

and the characteristic heaps of soil, mole-hills, which

are abundant in temperate zone meadows. Less known

to the public is the fact that species delimitation in 7al-

pa has been progressing very slowly and continuing dis-

agreements among experts over the number of species

exist (KryStufek & Motokawa 2018). Strong selective

pressures for a semifossorial life blur the phylogenetic

signal in morphological structures and convergences/

Received: 06.07.2020

Accepted: 07.10.2020

parallelisms are overwhelming. Traditional taxonomy

therefore heavily underestimated the species richness of

moles. The state of knowledge progressed only when the

information in nucleotide sequences was combined with

a wide taxonomic sampling (Bannikova et al. 2015). Be-

tween 2005 and 2020, the number of recognized species

in the genus 7a/pa increased from nine (Hutterer 2005) to

fourteen (KryStufek & Motokawa 2018, KryS8tufek et al.

2018a, Demirtas et al. 2020), an increase of 56%.

Bannikova et al. (2015) pointed out several unresolved

taxonomic problems, which required further attention.

One of these problems concerns the Levant mole Zalpa

levantis Thomas, 1906, which displays a very high intra-

specific genetic divergence. Earlier on, the Levant mole

was thought to range from the south-eastern Balkans

across northern Turkey into the Caucasus and the Cas-

pian coast of Iran. It was subsequently shown that the

western-most populations represent a species new to sci-

ence (Zalpa martinorum Krystufek et al. 2018), that those

from the Caspian coast are identical with 7: talyschensis

Vereschchagin, 1945, and that the rest can be split into the

western 7! /evantis proper, and the eastern 7. transcauca-

sica Dahl, 1945 (Demurtas et al. 2020). In this paper we

are re-addressing the geographical variability of Levant

Corresponding editor: J. Decher

Published: 27.10.2020

276 Haluk Kefelioglu et al.

moles occupying Turkey by combining, for the first time,

molecular evidence with morphological data. Our aim

was to gain a more holistic view on the taxonomic struc-

ture of the Levant mole.

MATERIAL & METHODS

Specimens. We studied small blind moles from through-

out Turkey (Fig. 1, Appendix I) which were earlier classi-

fied as T. /evantis. The European material was taken into

consideration because it had so far not been screened ge-

netically and because Demirtas et al. (2020) suggested

these populations to be conspecific to those occupying

Tissue samples for DNA analysis were placed in

non-denaturated 96% ethanol and subsequently refrig-

erated. The cytochrome b (Cyt b) gene was sequenced

for 20 Levant moles and these new sequences were ana-

lyzed together with 17 additional Levant mole sequences

from Turkey and the Caucasus region. Furthermore, we

downloaded from the GenBank database 23 sequences

of 10 Zalpa species, and an outgroup Talpinae sequence

(Urotrichus talpoides). Collecting data associated with

the new sequences and all GenBank numbers for Levant

moles are given in Table 1 [sequences submitted to Gen-

Bank]; for the remaining GenBank numbers see Table 1.

Specimen vouchers (skins and skulls) are deposited

in the following collections (acronyms in parentheses):

Anatolia. National Museum of Natural History, Washington D. C.

28, 33,34 A i

A 31,32 Nas LA)

44/45

Nw 4 172,73

WW al hon

54 |57-59

48-51 56

Central

West

Fig. 1. Sample locations of Talpa levantis and T: martinorum. Symbols: © Talpa levantis dogramacii ssp. nov.; A T. levantis le-

vantis, 0 T. I. transcaucasica, ¢ T: levantis ssp.; @ T! martinorum. Symbols correspond to those in Fig. 1 and Table 1. Tentative

range of Zalpa levantis is shaded grey and tentative longitudinal ranges of lineages are shown by left-right arrows. Downwards

arrows show contact points between the sublineages of Western (W1, W2) and Central (C1, C2) lineages. Population near Lake

Van (pt. 74) is presumably an isolate of unknown genetic identity, known from a single locality. Bulgaria: 1-Kondolovo. Turkey:

2-Kirklareli, Dupnisa; 3—Tekirda’, Corlu; 4—Istanbul, Catalca; 5—Istanbul, Bahcekoy, Belgrad Ormani; 6—Canakkale; 7—Kapidaz,

Balikesir; 8—Balikesir, Manyas; 9—Balikesir, Bandirma; 10—Bursa, Karacabey; 11—Bursa, Uludag; 12—Bursa, Kirazlryayla, Uludag;

13—-istanbul, Mahmutsevketpasa; 14—Istanbul, Sile; 15—-Izmit; 16—-Izmit, Kandira; 17—Adapazari, Kazimpasa, Alandtizii koyii;

18—Diizce; 19—Bolu, Abant; 20—Kocaman forestry, half was between Akcakoca and Alapli; 21—Bolu, Seben; 22—Bolu, Karadere;

23—-Zonguldak, Uzungtiney Koyti; 24—Zonguldak, Caycuma; 25—Zonguldak, Alapli; 26—between Zonguldak and Bolu; 27—Zongul-

dak, between Sefercik and Filyos; 28—Tosya, Kastamonu; 29-Sinop, Abali Koyu; 30—Sinop, Gerze; 31—Amasya; 32—Amasya, Tat-

licak koyt; 33—Samsun, Bafra; 34—Samsun, Kizilirmak delta, Bafra; 35—Samsun, Erikli K6yt; 36-Samsun, Ondokuzmayls, Der-

ekoy; 37—Tasova District, Borabay Lake; 38—Samsun, Karakavuk; 39-Samsun, Incesu Koyti; 40-Samsun; 41—Samsun, Kurupelit:

42—Samsun, Tekkekoy; 43—Samsun, 3 km south Carsamba; 44—Ordu, Fatsa; 45—Ordu, Fatsa, Geyikceli Koyii; 46—Ordu, Ulubey;

47-Ordu; 48—-Giresun, Yavuzkemal; 49-—Giresun, Batlama Deresi; 50—Giresun, Kttmbet; 51—Giresun, Dereli; 52—Giresun;

53—Giresun, Ulper; 54—Trabzon, Mereyem Ana; 55—Giresun, Gorele; 56—Ordu, Torul, Gimiishane; 57—Trabzon, Macka; 58—Tra-

bzon, Macka, Altindere; 59-Trabzon, Macka, Stmela Manastir1; 60—Trabzon; 61—Trabzon, Khotz; 62—Trabzon, Ozdil; 63—Trab-

zon, Oymalitepe; 64—Trabzon, Yomra; 65—Rize, Ovit, Ovit Yaylasi1; 66—Rize, Ardesen; 67—Ayder, Ilicasi; 68—Artvin, Hopa, Sug6-

renkoyu; 69—Artvin, Hopa 8 km east; 70—Artvin; 71—Artvin, Ardanug; 72—Artvin, Yalnizcamgecidi; 73—Ardahan, Cam Ge¢idi;

74-Bitlis, Tatvan, Lake Van. Armenia: 75—Margahovit;, 76—Fioletovo. Russia: 77—Kabardino-Balkaria, Nalchik; 78—Adygea.

Bonn zoological Bulletin 69 (2): 275-291 ©ZFMK

Taxonomic revision of the Levant moles of Turkey 2a7

Table 1. Details of sample localities (mapped in Figure 1) for Levant moles s. lat. and cytochrome b haplotypes found within them.

ey Country Locality pas Voucher No. ela pepe References

e 7martinorum

1 Turkey Kirklareli, Dupnisa TR13 MT738563 This study

2 Bulgaria Mt. Strandzha, Kondolovo ZFMK-MAM-2017.1151 MH093595 Krystufek et al. 2018a

4 Turkey Istanbul, Catalca TRI5 MT738565 This study

f Turkey Kapidag, Balikesir TRI8 OMU 1346 MT738568 This study

11 Bursa, Uludag TR6 OMU 1350 MT738556 This study

TR7 OMU 1352 MT738557 This study

TR8 OMU 1353 MT738558 This study

PMS 10650 FN640571 Colangelo et al. 2010

2S Zonguldak, Uzungtiney Koyt KP717336 Bannikova et al. 2015

2 Diuizce TRI16 OMU 1344 MT738566 This study

TR17 OMU 1345 MT738567 This study

in Zonguldak, Caycuma KP717338 Bannikova et al. 2015

A T. levantis Central

20 Zonguldak, Alapli KP717340 Bannikova et al. 2015

26 Bolu-Zonguldak TRI9 OMU 1343 MT738569 This study

28 Zonguldak, Sefercik — Filyos KP717339 Bannikova et al. 2015

KP717343 Bannikova et al. 2015

33 Amasya TRI14 MT738564 This study

42 Samsun TRI1 MT738561 This study

PMS 10299 FN640572 Colangelo et al. 2010

46 Ordu, Fatsa TRO MT738559 This study

49 Ordu TR20 MT738570 This study

TR12 MT738562 This study

51 Giresun TRIO OMU 1349 MT738560 This study

32 Giresun, Ulper TR20 OMU 1340 MT738552 This study

= Giresun, Ktimbet TRS MT738555 This study

59 Trabzon, Macka TRI OMU 1354 MT738551 This study

64 Trabzon, Ozdil TR4 OMU 1351 MT738554 This study

65 Trabzon, Oymalitepe TR3 OMU 1347 MT738553 This study

T. levantis East

76 Turkey Ardahan, Cam Gegidi PMS 21658 FN640570 Colangelo et al. 2010

fe: Armenia Margahovit KP717335 Bannikova et al. 2015

78 Fioletovo KP717337 Bannikova et al. 2015

KP717342 Bannikova et al. 2015

79 Russia Kabardino-Balkaria, Nalchik KP717334 Bannikova et al. 2015

KP717341 Bannikova et al. 2015

Kabardino-Balkaria FN640573 Colangelo et al. 2010

FN640574 Colangelo et al. 2010

80 Russia Adygea KP717344 Bannikova et al. 2015

KP717345 Bannikova et al. 2015

KP717346 Bannikova et al. 2015

Bonn zoological Bulletin 69 (2): 275-291

©ZFMK

278 Haluk Kefelioglu et al.

(NMNH), Natural History Museum London (BMNH),

Naturhistorisches Museum Wien, Vienna (NMW), Zo-

ologische Staatssammlung Munchen, Munich (ZSM),

Mammal Collection in the Ondokuz Mayis University,

Samsun (OMU), and Slovenian Museum of Natural His-

tory, Ljubljana (PMS). Vouchers in OMU, PMS and ZSM

were examined by us in December 2019 and February

2020. Material from the remaining collections was exam-

ined by BK prior to this study and records were compiled

to contain measurement data, drawings and photographs.

All field procedures involving handling of animals in

this study were in compliance with guidelines approved

AB037602

KP717356

100" KP717360

1007 MHO093595

- TR13

by the American Society of Mammalogists (Sikes et al.

2011). Recent collecting was carried out under permit

B.30.2.0DM.0.20.09.00-050.04-09 issued on February

14, 2014, by the Ethic Committee at the Ondokuz Mayis

University.

Molecular protocols. Total genomic DNA was extracted

from ethanol-preserved muscle tissue using silica mem-

brane columns of the Blood and Tissue kit by Qiagen

(Hilden, Germany). DNA extracts are available from

the ZFMK Biobank, Bonn (DNA voucher IDs are list-

ed in Table 1). For PCR amplifications of the mitochon-

EU918371 ~Urotrichus talpoides

Talpa altaica

Talpa ognevi

KP717367

| Talpa martinorum @&

Talpa davidiana

99 TR15

400 FJ688089

77 FJ688098

64 100 KP717348 Talpa stankovici

FJ688094

67" KP717347

oa - HQ233501 Talpa romana

72 100 DQ630425

KP717333 Talpa caeca

99 FN640560

54 FN640561

74 53 KU189723 Talpa occidentalis

KF801510 Ss,

Too + KU189595 i Talpa aquitania

57 83 ZFMK-MAM-2013 595

700] | KF801574 7

KU189429 alpa europaea

FJ688085

KP717322

FN640570

99 go KP717345

KP717344

KP717346

KP717337

) Kkp717342 East [|

98] pKP717335

FN640573

99] }FN640574

KP717334

KP717341

85 sae TR16

TR17

KP717336 W2

100¢ KP7 17338

FN640571 West O

ToT TR18

60 TRO6 W1

TRO7

100

87 TRO8

TRO1

100 TRO3 |c2

77* TRO4

99-— TRO2 7

88 TRO5

78 TROY

oy (Ure A

Tab C1 Central

FN640572

TR11

1 LTR14

0.08 59 KP717340

TR19

100], KP717339

KP717343

Fig 2. 50% Majority Rule Bayesian tree inferred from 1043 bp of the mitochondrial cytochrome 5 gene for 11 species of the genus

Talpa. Posterior probability values are shown on the nodes. The tree is rooted with Urotrichus talpoides. Symbols correspond to

those in Fig. 1 and Table 1.

Bonn zoological Bulletin 69 (2): 275-291

©ZFMK

Taxonomic revision of the Levant moles of Turkey 279

drial Cytochrome b (Cyt 5) gene, we used the Qiagen

Multiplex PCR kit, following the manufacturer’s speci-

fications and based on 2 ul undiluted DNA template in

20ul total reaction volumes. DNA fragments of 1043 bp

were amplified with an Applied Biosystems GeneAmp

PCR System 2700 (Life Technologies), applying the

primers L14724ag (5’-ATGATATGAAAAACCATC-

GTTG-3’) and HI1591l5ag (5’-TTTCCNTTTCTG-

GTTTACAAGAC-3’; Guillén-Servent & Francis 2006).

PCR routine followed a ‘touch-down’ protocol: Taq

activation: 15 min at 95°C; first cycle set (15 repeats):

35 s denaturation at 94°C, 90 s annealing at 60°C (-1°C

per cycle) and 90 s extension at 72°C. Second cycle set

(25 repeats): 35 s denaturation at 94°C, 90 s annealing at

50°C, and 90 s extension at 72°C.

After enzymatic clean-up, all PCR products were

Sanger-sequenced at Macrogen, Europe’s commercial

Sanger sequencing service (Amsterdam, NL). Sequences

were assembled, inspected and aligned using Geneious

vers. R7 (Biomatters, Auckland, New Zealand).

Bayesian analyses were conducted using MrBayes

vers. 3.2 (Ronquist & Huelsenbeck 2003). Specific

parameters for a GTR+G model were equated by the

program. GTR+G is a typical substitution model that

includes sufficient degrees of freedom and factors in het-

erogeneity of substitution rates among sites, but avoids

Overparameterization as potentially induced by modelling

invariable sites (Jia et al. 2014 showed the irrelevance of

including invariable site assumptions in datasets below

species level). Parameters were unlinked between the 3rd

versus Ist plus 2nd codon positions, based on the fact

that third codon ‘wobble’ positions are less influenced by

selective pressure and much less conserved then Ist and

2nd positions, hence requiring separate parameter calcu-

lation. MrBayes was run for 20 million generations and

using the default number of chains. Every 1000th tree

was sampled. Negative log-likelihood score stabilization

was determined in a separate visualization. Accordingly,

we retained 39,960 trees, which were used for building a

50%-majority rule consensus tree with posterior proba-

bilities (Fig. 2).

Morphological analyses. Our study was based on visual

examination of museum specimens, both macroscopical-

ly and under a stereomicroscope at different magnifica-

tions. Skull morphology was quantified by means of five

cranial variables, which were scored using a Vernier calli-

per with accuracy to the nearest 0.1 mm (acronyms in pa-

rentheses): condylobasal length of skull (CbL), length of

maxillary tooth-row (MxT; canine to 3 molar), breadth

of braincase (BcB), breadth of rostrum over canines

(RoC), and breadth of rostrum over molars (RoM). The

length of the posterior part of bratncase was measured on

printed skull photographs. External measurements were

obtained from specimen tags: body mass (BWt), length

of head and body (H&B), length of tail (TL), and length

Bonn zoological Bulletin 69 (2): 275-291

of hind foot (HfL). Body mass is given in grams and the

remaining measurements in millimetres.

Based on molecular results, the specimens were

grouped into three operational taxonomic groups (OTUs),

which were essentially identical to phylogenetic lineag-

es. Because molecular characters were not known for all

museum specimens, we presumed that the lineages are

allopatric and classified skulls on this basis. Specimens

from the zone of overlap between the Western and the

Central lineages were excluded, while specimens from

the little-known contact zone between the Central and

the Eastern lineages were assigned to the group using

classification criteria derived from a discriminant func-

tion analysis based on securely identified vouchers. We

used the same labels for denomination of phylogenetic

lineages and morphological OTUs (Western, Central and

Eastern). Moles from Lake Van (pt. 74 in Fig. 1) are tra-

ditionally classified as 7 /evantis although they are an

isolate with unknown molecular identity. We used mor-

phometric analysis to compare this sample with the three

OTUs of 7. levantis.

Heterogeneity between OTUs was evaluated in one-

way or two-way analyses of variance (Anova). To char-

acterize the craniometric variation among samples and to

find patterns in our high-dimensional data, we performed

a principal components analysis (PCA) and a discrimi-

nant function analysis (DFA) on log, ,-transformed crani-

al variables. Rates of correct classification of a priori de-

fined species were evaluated in a discriminant analysis.

To evaluate the performance of the DFA and avoid the

risk of overfitting the data, all analyses were cross-val-

idated using the jack-knife procedure, in which each

specimen is classified into a group using the discriminant

function derived from all specimens except the specimen

being classified. Relative length of maxillary tooth row

(MxT%) and relative breadth of rostrum over molars

(RoM%) were expressed as quotients with the condy-

lobasal length of skull and multiplied by 100. Because

of undesirable statistical properties of ratios, we did not

use them in multivariate analyses. Statistical tests were

run in Statistica 7.0 (StatSoft Inc., OK, USA) and SPSS

Statistics 2012 (IBM Analytics, NY).

RESULTS

Molecular results. Sequencing of the new Turkish sam-

ples resulted in 19 haplotypes of the length 1043 bp (one

sequence missing one base, another three). A further se-

quence that showed a clear (and accordingly trimmed)

read for only 403 bp was integrated in the dataset (sam-

ple TRO9 from Fatsa Ordu). Overall, the dataset includ-

ed 6 ambiguous positions in individual sequences (see

attached alignment in Appendix II).

In the Bayesian tree (Fig. 2), haplotypes clustered ac-

cording to the earlier results of Bannikova et al. (2015),

©ZFMK

280 Haluk Kefelioglu et al.

although tree topologies differed in some minor respects.

Moderate nodal supports prevent us from discussing the

deeper branching topology (outside 7. /evantis) in detail.

Turkish samples grouped into four clusters. The only

two haplotypes from European Turkey (TR13, TR1I5)

aligned with the reference sequence of 7? martinorum

from Bulgaria. Levant mole haplotypes grouped into

three lineages, which showed strong geographic associ-

ations and were designated as the Western, Central and

Eastern lineage. The Eastern lineage holds a moderately

supported basal position with regard to the Western and

Central lineages. The collecting sites of specimens asso-

ciated genetically with the Central and Eastern lineages

were separated by a distance of about 225 km, without

any genetically screened samples in-between. On the

other hand, the ranges of the Western and Central lineag-

es overlapped to the east of the city of Zonguldak for a

distance of at least 30 km in west-to-east direction. Be-

sides this, the Western and Central lineages were further

sub-structured, each into two allopatric sub-lineages. In

11.0

9.0

Length of braincase

7.0

8.0 9.0

the Western lineage, the sublineages W1 and W2 were

tentatively delimited by Sakarya, while the sub-lineages

Cl and C2 of the Central lineage had a contact between

Rize and Trabzon. The C2 sublineage occupies the ma-

jority of the range of Levant moles in Turkey by stretch-

ing along the Black Sea coast in west-to-east direction

for ca. 650 km.

Within the Levant moles of Anatolia, the Cyt 5 di-

vergence was highest between the Eastern and the Cen-

tral lineages (highest pairwise p-distance at 8.0%), and

amounted to 5.9% between the Central and the West-

ern lineages. Genetic variation within the lineages was

highest in the Central lineage (mean p-distance of 2.0%,

highest pair-wise p-distance 3.4%), closely followed by

the Western lineage (mean 1.7%, highest 2.9%), and was

lowestin the Western lineage (mean 1.0%, highest 2.6%).

In our dataset, the lowest p-distance among lineages was

between the Central and Western lineages, with 3.5%.

Central

10.0

RoM

11.0

12.0

Fig. 3. Bivariate plot of length of neurocranium (see the left upper inset) against breadth of rostrum across molars (RoM) for three

operational taxonomic units of Zalpa levantis. Symbols are same as in Fig. 1.

Bonn zoological Bulletin 69 (2): 275-291

©ZFMK

Taxonomic revision of the Levant moles of Turkey 281

Morphology. Moles from Turkish Thrace lack the para-

style on the anterior upper molars and were therefore

classified as 7. martinorum (cf. Kry8tufek et al. 2018a).

The parastyle is present in the majority of Anatolian in-

dividuals, as long as their molars are still comparatively

unworn. Visual examination of skulls retrieved no quanti-

tative cranial or dental traits among the 7? /evantis OTUs.

In the results of a two-way Anova, the major source of

morphometric variation was the OTU and not the sex-

ual category (Table 2). Therefore, five variables (H&B,

HfL, CbL, MxT, RoM) showed significant heterogeneity

among the OTUs and only three traits (BWt, H&B, BcB)

were also sexually dimorphic. With the exception of the

length of tail, there was no interaction between these two

factors. Out of 27 pairwise comparisons, only ten showed

significant differences in the Fisher LSD test. Six of them

fell between the Central and Eastern OTUs, while two

comparisons were significant between the Western and

Central OTUs, and further two between the Western and

Eastern OTUs, respectively. Males were more prone to

the heterogeneity among OTUs (7 significant pairwise

comparisons) than females (3 significant comparisons).

The two quotients (MxT% and ROM%) showed a similar

pattern as the linear measurements (Table 2).

100 x RoM/ CbL (%)

35 37

When inspecting skulls macroscopically, we spotted

slight differences in their shape and proportion. There-

fore, in the Western OTU, the posterior outline of the

braincase was less bowed than in the Central OTU, the

overlap however was considerable (Fig. 3). Furthermore,

the relative length of the maxillary tooth-row (MxT%)

and the width of rostrum across molars (ROM%) showed

a steady increase from the Eastern OTU to the Western

OTU; the Central OTU was intermediate in both cas-

es. Again, the overlap among the OTUs was sizeable

(Fig. 4). We therefore tested our data set for possible

longitudinal trends. Two external traits (BWt, TL), three

craniodental variables (MxT, RoC, RoM) and both quo-

tients (MxT% and RoM%) showed significant trends of

a west-to-east decline (Table S1). The remaining traits

(H&B, HfL, CbL, BcB) showed extremely low F-val-

ues (F<0.30, p>0.59). Moles in the west were therefore

the heaviest, with longer tails, absolutely and relatively

longer maxillary tooth-rows, relatively and absolutely

broader rostra and less bowed posterior braincases. The

eastern moles showed the lowest values for all these in-

dices, while geographically intermediate moles were also

transitional in these traits.

Central

39 41

100 x MxT / CbL (%)

Fig. 4. Bivariate plot of breadth of rostrum across molars (RoM) against length of maxillary tooth-row (MxT), both expressed as

quotients of the condylobasal length of skull and multiplied by 100, for three operational taxonomic units of Talpa levantis and the

sample from Lake Van. Symbols are same as in Fig. 1.

Bonn zoological Bulletin 69 (2): 275-291

©ZFMK

282 Haluk Kefelioglu et al.

Table 2. Descriptive statistics (mean and standard error) for three operational taxonomic units (OTUs) of Talpa levantis. Results of

two-way Anova (sex and OTU as factors) and Fisher LSD test between the OTUs (W—Western; C—Central; E—Eastern) are shown

in four columns on the right-hand side.

Trait West Central East Two-Way Anova Scheffé test

N Mean SE N Mean SE N Mean SE F-value p

BWt males 26 5488 1448 25 5532 1477 6 £51.25 3.014 OTU 1.18 0.311

females 13 52.00 2.048 29 4763 1.371 7 £44914 2.791 Sex 5.90 0.017

Interaction 1.47 0.236

H&B males 29, 12241 1.244 34 12609 1.149 14 121,57 1.791 OTU 4.27 0.015 W-C, C-E

females 13 11954 1.859 29 12210 1.244 10 11850 2.119 Sex 6.33 0.013

Interaction 0.09 0.912

TL males 29, 27.90 0469 34 2732 0433 14 2800 0675 OTU 231 0.098

females 13 2862 0.700 29 2831 0469 9 25.56 0.842 Sex 0.24 0.626

Interaction 3.94 0.022

HfL males 29, 18.76 0.245 34 1912 0227 14 1794 0354 OTU 3.93 0.022 C-E

females 13 1854 0366 29 1900 0246 10 1842 0418 Sex 0.03 0.861

Interaction 0.58 0.563

CbL males 29, 31.15 0.229 32 31.76 0218 14 3063 0330 OTU 11.68 0.00002 C-E

females 13 3044 0343 27 4.3135 0238 9 2964 0412 Sex 7.96 0.006 W-C, C-E

Interaction 0.49 0.62

MxT males 30.)=6« 11.95 0.095 35 1209 0084 14 11.51 0133 OTU 12.60 0.00001 W-E, C-E

females 14 11.75 O.133 28 1201 0094 9 11.36 0.166 Sex 1.99 0.161 C-E

Interaction 0.19 0.824

BcB males 29, 15.25 0.089 33 1546 0.083 14 15.29 0.128 OTU 2.40 0.091

females 13 1496 0.133 29 15.17 0.089 9 15.02 0.160 Sex 8.70 0.004

Interaction 0.00 0.996

RoC males 30 ©6461 0.181 35 4.23 0.168 14 3.96 0.265 OTU 1.03 0.361

females 14 414 0.265 28 4.23 0.188 9 404 0331 Sex 0.45 0.504

Interaction 0.83 0.439

RoM males 30. «8.830.097 35 8.60 0.089 14 831 0141 OTU 4.31 0.016 W-E

females 14 870 0.141 29 8.72 0.098 9 8.40 0.176 Sex 0.09 0.770

Interaction 0.74 0.481

Quo-

tiens

MxT% males 28 3842 0.159 32 3819 0.148 14 37.55 0.225 OTU 7.50 0.0007 W-E,C-E

females 13 38.62 0.234 27 3827 0.162 8 3767 0298 Sex 0.90 0345 W-E

Interaction 0.00 0.984

RoM% males 29 28.34 0.222 32 27.04 0211 14 27.11 0319 OTU 9,08 0.0002 W-C.W-E

females 13 2853 0.331 27 27.74 0.230 8 27.83 0.422 Sex 4.82 0.030

Interaction 0.59 0.556

Bonn zoological Bulletin 69 (2): 275-291 ©ZFMK

Taxonomic revision of the Levant moles of Turkey 283

DF2 (31.5%)

DF1 (54.7%)

Fig. 5. The 95% confidence ellipses for dispersion of scores of

four operational taxonomic units of Zalpa levantis onto the first

two discriminant axes derived from discriminant factor anal-

yses of log, ,-transformed cranial variables. The proportion of

variance explained by an axis is in parentheses. The ellipse for

the Lake Van sample is shown by a dashed line.

The principal components analysis was run on a cor-

relation matrix of all five cranial traits. One-way Anova

retrieved significant heterogeneity among OTUs in four

principal components (pc) out of a total of five. Quite re-

markably, the highest F-values were by pc3 and pcS, L.e.

two components which explained only a small proportion

of variance (=10.4%) in the original data set (Table S2).

Projection of specimen scores onto these components re-

vealed a high overlap among OTUs and moles from Lake

Van overlapped with all three OTUs (not shown).

Forward stepwise discriminant analysis on five cra-

nial variables and with four groups (three OTUs and

sample from Lake Van) as classification factor resulted

in a moderately high Wilk’s lambda (=0.587, p<0.001).

All variables were included into the analysis, except for

the braincase width (F-to-enter=2.255, p=0.85). Condy-

lobasal length of the skull and maxillary tooth-row length

had the highest F-to-remove values (10.656 and 8.175,

respectively; p<0.00005) and therefore contributed most

to a discrimination between groups. Putting aside the

Lake Van sample, the Mahalanobis squared distance (D’)

was high between the Western and the Eastern OTUs

(D?=2.125), moderate between the Western and the Cen-

tral OTUs (D?=1.667) and low between the Central and

the Eastern OTU (D7=1.355; all significant at p<0.002;

F>4.5). The Lake Van sample was most similar to the

Eastern sample (D?=1.690, p=0.046), followed by the

Central OTU (D’?=2.006, p=0.006) and the Western OTU

(D?=2.759, p=0.001). Predictability of classification was

rather low and only 54.7% of cases were allocated into

the actual group; this ranged from 80.0% of correct clas-

sifications for the Van sample, across 56.8% for the West-

Bonn zoological Bulletin 69 (2): 275-291

ern OTU and 52.9% for the Eastern OTU, to 45.8% in

the Eastern OTU. Cross-validation of classification with

leave-one-out yielded very similar results with 52.0% of

individuals being allocated to the actual group. The over-

lap between groups was therefore considerable and was

evident also from the projection of specimen scores onto

the first two discriminant axes, explaining 86.2% of vari-

ance in the original data set (Fig. 5). On the other hand,

the cross-validation of classification results showed that

we avoided the risk of overfitting data in our DFA. We

therefore conclude that differences between the groups

are slight but genuine.

DISCUSSION

Survival in Pleistocene refugia. There is a deep genea-

logical divergence among the three main Cyt 5 lineages

of the Levant mole and such a pattern is a clear indication

that these lineages originated from an allopatric fragmen-

tation event (Avise 2000). The most ancient divergence in

the Levant mole, which is between the Western + Central

and the Eastern lineages, is estimated to have occurred at

ca. 1.91 Mya (Demirtas et al. 2020). The current phylo-

geographic pattern of the Levant mole is therefore clearly

the legacy of climatic changes during the glacial-inter-

glacial cycles of the Pleistocene when the newly emerged

biogeographic barriers created by novel climatic condi-

tions fragmented populations, prevented gene flow and

triggered divergence in isolation.

Contrary to Europe where periodic expansion of ice

sheets and the consequent cooling of temperatures pro-

foundly impacted the survival of temperate biota through-

out the Pleistocene (Hewitt 2000), the Quaternary envi-

ronments in Anatolia were different in many respects.

Glaciers persisted only at elevations above 2200 m (Erin¢

1978) while the lowlands were affected by aridificaton

(Webb & Bartlein 1992). In a highly diverse landscape of

Anatolia, the endurance of temperate taxa was facilitated

along the altitudinal gradient in a network of mountain

refugia which provided moist conditions at intermediate

elevations (Ansell et al. 2011). Fossorial moles are highly

sensitive to soil humidity, which supports prey consisting

primarily of earthworms (Krystufek & Motokawa 2018).

It is therefore feasible to presume that during the Pleis-

tocene the progressing aridification pushed the Levant

moles to higher elevations where they endured in humid

enclaves. This fragmented the mole’s range, just as an

expansion of glaciers and tundra habitats repeatedly frag-

mented continuous distributions of numerous temperate

taxa in Europe (Hewitt 2000). A combination of Anato-

lian topography and climatic history may have promot-

ed a long-term local survival of the Levant mole in the

Black-Sea (Pontic) Mountains, and simultaneously facil-

itated the independent evolutionary divergence of vicari-

ant populations. At least five refugia can be deduced from

©ZFMK

284 Haluk Kefelioglu et al.

the topology of Cyt 5 trees (Demirtas et al. 2020, and

this study), which matches a spatially explicit picture of a

wider pattern of endemism in Anatolia (e.g., Roces-Diaz

et al. 2018). The Marmara region, which emerged in our

study as an important refugial area for the Western lin-

eage, has been identified by mammalogists as part of a

permeable corridor for faunal exchanges between Europe

and south-western Asia (Hosey 1982) but was never con-

sidered as being of particular importance for mammalian

endemism.

The phylogeographic structuring of the Levant mole

cannot be attributed to the external barriers. Demirtas

et al. (2020) stressed this for the Eastern part of the Pon-

tic Mts. where no obvious obstacles separate the Central

and the Eastern lineages. The situation is even more puz-

zling on the western end of the range where the Central

haplotypes are parapatric with the Western ones.

Demurtas et al. (2020) suggested for the Levant mole

to occupy both sides of the Marmara and Bosporus (also

called the Turkish) straits. The idea of the intermittent

continental bridge at the Turkish strait dates back to times

of classical zoogeography (Kosswig 1955, Hosey 1982).

As confirmed by recent phylogeographic studies, mam-

mals crossed the Turkish straits moving from Europe to

Anatolia (e.g., Glis glis; Helvaci et al. 2012), from Ana-

tolia to Europe (e.g., Microtus hartingi;,; Krystufek et al.

2018b) or in both directions (e.g., Crocidura leucodon,

Dubey et al. 2007). The Levant mole, however, was ob-

viously not such a transcontinental migrant. As already

suggested by KryStufek et al. (2018a) and confirmed in

this study, the small blind moles from European Turkey

are conspecific with 7. martinorum from Bulgarian Thra-

ce. Talpa levantis is therefore a species endemic to the

Caucasus and the Pontic Mts. of south-western Asia.

Species delimitation in Levant moles. One of the cen-

tral aims of our study was a translation of phylogenetic

results into taxonomy. In the interpretation of Demurtas

et al. (2020) the Cyt b K2P divergence by 7.28% (8.0%

maximum uncorrected distance in our results, 6.4% as a

median) between their eastern and western sublineages

(identical to Eastern and Western + Central lineages in

this study) justify their ranking as distinct species, namely

Talpa levantis s. str. and T. transcaucasica. Given that the

K2P value of 7.28% is the lowest interspecific distance

in the genus 7a/pa, Demurtas et al. (2020) justified their

taxonomic split by pointing on a “robust and geographi-

cally coherent” topology of their phylogenetic tree. Fur-

thermore, they stressed that subterranean mammals are

“morphologically constrained” which makes traditional

delineation between species “intrinsically difficult”. In-

deed, at least one newly recognized species of 7alpa, 1.e.

T: ognevi, was elevated to the rank of species in its own

right (KryStufek & Motokawa 2018) entirely on the basis

of genetic distances provided by Bannikova et al. (2015).

On the other hand, two recent studies established new

Bonn zoological Bulletin 69 (2): 275-291

species of Talpa (T. aquitania and T: martinorum) on the

basis of both, genetic distances and unique craniodental

traits (Nicolas et al. 2017, Kry8tufek et al. 2018a) and the

independent species status for 7 talyschensis was pro-

posed on morphological evidence (Zaytsev et al. 2014)

before this was revealed by nucleotide sequences (Ban-

nikova et al. 2015).

While ranking the three Cyt 5 lineages of Levant moles,

we had the following tn mind:

1.Genetic distances between the lineages’ of

the Levant mole are below the lowest inter-

Specific pairwise distance in the genus Talpa.

2.Craniometric distances calculated in our study do not

match the genetic distances. Genetically the most dis-

tinct were the Central and the Eastern lineages, while

the greatest Mahalanobis squared D2 distance was

retrieved between the Western and Central OTUs.

3.Univariate and multivariate analyses of morpho-

metric variables displayed a pattern of a gradual

longitudinal cline with no evidence of discontinul-

ty on the contact zones of the three lineages. Such

a smooth transition may not be due to a putative

gene flow but can equally well indicate morpholog-

ical response to the environment, which frequently

changes gradually and was not tested in our study.

4 Our study retrieved a wide zone of overlap between

the Western and Eastern lineages, which is most

likely due to a secondary admixture of allopatrical-

ly evolved populations (Avise 2000). The Cyt 5 evi-

dence on its own unfortunately does not allow a con-

clusion regarding gene flow, or lack of it, between

the two lineages. Consulting more and nuclear mark-

ers would help future investigations on the topic.

We suggest a polytypic species concept as the appro-

priate taxonomic solution for the observed pattern of

variation in the Levant mole. Subsequently we classify

the three lineages as distinct subspecies. Subspecies are

usually defined as allopatric groups of populations with

independent histories, which are definable by geograph-

ically structured attributes, be they either, or both, mor-

phological and molecular characteristics (Patton & Con-

roy 2017). As long as they are part of one and the same

species, subspecies are by definition inter-fertile. Our hy-

pothesis of three reproductively compatible, rather than

reproductively isolated groups of populations of Levant

moles can be falsified and is therefore testable. This hy-

pothesis can be tested on the contacts of divergent phy-

logeographic lineages. We urge for further field sampling

and molecular screening of moles in the zone of overlap

between the Western and the Central lineages around the

city of Zonguldak and to the west of it, and between Tra-

bzon and Rize, where one can expect the Central and the

Eastern lineages to meet.

©ZFMK

Taxonomic revision of the Levant moles of Turkey 285

Taxonomy of Talpa levantis

Talpa levantis Thomas, 1906

Diagnosis. Distinguishable from all other species of the

genus Jalpa by nuclear and mitochondrial DNA sequenc-

es (Bannikova et al. 2015, Demurtas et al. 2020).

Description. 7: /evantis is a smaller mole (H&B=103—

149 mm, CbL=28.6—33.5 mm) with eyelids sealed and

the eyes covered by a transparent skin. External mor-

phology shows no peculiarities. Skull is of average shape

(KryStufek et al. 2018a): relative width (as a percentage

of CbL) of rostrum over canines is 11.8—14.9% and width

of rostrum over molars is 24.7—31.0%. The maxillary

tooth-row is comparatively short (MxT%=35.6—-38.9%).

However, the 1* upper molar has a parastyle, which

shows heavy tooth-wear. The pelvis is of the caecoidal

type, i.e., with the 4" sacral foramen opened posteriorly

(Dogramaci 1989b). Diploid number of chromosomes

is 2n = 34 and the fundamental number of autosomal

arms is NFa = 64. All subspecies were karyotyped and

no variation was reported (Sokolov & Tembotov 1989,

Kefelioglu & Gengoglu 1996; Sevindik 2013, Selcuk &

Kefelioglu 2017).

Comparisons. 7: /evantis can be separated by mor-

phological and karyological characteristics from other

moles occupying Turkey (Kefelioglu & Gencoglu 1996,

KryStufek & Vohralik 2001, Kry8tufek et al. 201 8a).

7. ognevi is larger (CbL= 33.6—35.9 mm) and has a high-

er diploid number (2n = 38; Selcuk & Kefelioglu 2017).

T. davidiana has a more robust skull with a comparative-

ly wider rostrum; the breadth across canines accounts

for 12.1-14.5% of the condylobasal length in 7. /evan-

tis as opposed to 14.9-17.3% in T. davidiana. T: levan-

tis is smaller than 7’ europaea from European Turkey

(CbL=32.4—37.0 mm) and has eyelids grown together,

while they are free in 7! europaea. T: levantis has a para-

style on the 1*t upper molar while 7. martinorum lacks it.

Overall comparison of cranial shape in Turkish species of

Talpa is summarised in Selcuk et al. (2017).

Distribution. Range embraces the coast and mountains

in northern Turkey along the Sea of Marmara and the

Fig. 6. Ventral cranium of subspecies of 7alpa levantis. a. T: 1. dogramacii ssp. nov. PMS 10650 (paratype; condylobasal length of

skull = 30.2 mm). b. 7! /. levantis PMS 10299 (31.3 mm). ec. 7. 1. transcaucasica PMS 21658 (30.3 mm).

Bonn zoological Bulletin 69 (2): 275-291

©ZFMK

286

Black Sea (Fig. 1) and the Caucasus in Georgia, Armenia

(as far south as Lake Sevan), and Russia (south of Kuban

and Sulok rivers in Krasnodar, Adygea, Karachay-Cher-

kessia, Ingushetia, Chechnya, and Dagestan; Sokolov &

Tembotov 1989). A population in the Lake Van area is

obviously an isolate (KryStufek & Motokawa 2018).

Miscellaneous. Reviewed by KryStufek & Motokawa

(2018); Sokolov & Tembotov (1989) provided a detailed

review of the Caucasian populations. We subsequently

list three subspecies (Fig. 6). The population from Lake

Van was not assigned to any of them and requires a mo-

lecular screening.

Talpa levantis levantis Thomas, 1906

(Fig. 5b)

Talpa caeca levantis Thomas, 1906:416. Type locality

is “Scalita, S. of Trebizond”, now “Altindere, south of

Trabzon, Turkey” (KryStufek & Vohralik 2001:100).

The type 1s a skin and skull in the Natural History Mu-

seum London (No. 6.3.6.5); type was seen.

Talpa levantis: Spitzenberger, 1973 (in Felten et al.

1973:229). First use of current name combination.

Diagnosis. Identical to the Central lineage of Zalpa le-

vantis as retrieved in the phylogenetic analysis of the

mitochondrial Cyt b gene. In our dataset, the subspecies

levantis has unique mutations in comparison with se-

quences of both ssp. transcaucasica and T: 1. dogramacii

new subspecies at 6 positions of our Cyt 5 alignment

(see Appendix IT): 150:C, 447:T, 852:G, 933:G, 990:T,

1020:T.

Description and comparison. Similar to the remain-

ing subspecies and the differences are on average. The

nominotypical subspecies differs significantly from ssp.

transcaucasica in four linear variables (H&B, HfL, CbL,

MxT) and both quotients (MxT%, RoM%) in males

and in two linear variables (CbL, MxT) in females. The

nominotypical subspecies attained higher means in all

comparisons but had a relatively shorter maxillary tooth-

row (MxT%) than ssp. transcaucasica. For comparison

with 7: /. dogramacii ssp. nov. see under that subspecies.

Distribution. The Black Sea coast and mountains from

vicinity of Zonguldak to Trabzon. Endemic to Turkey.

Talpa levantis transcaucasica Dahl, 1945

(Fig. 5c)

Talpa europaea transcaucasica Dahl, 1945: 48. The year

of publication on the cover page 1s 1944; with 1945

we follow Pavlinov & Rossolimo 1998: 8). Type lo-

cality (p. 49): “OkpecHoctu cea BockpeceHoBcKu

(KuposakaHcknii p-H Apm. CCP) ... Baicora 1845 m

Bonn zoological Bulletin 69 (2): 275-291

Haluk Kefelioglu et al.

Hajl ypoBHem Mops [Surroundings of the village of

Voskresenovka (Kirovakan district of the Armenian

Soviet Socialist Republic) ... Altitude 1845 m above

sea level]”. Since names of places changed since

1945, the type locality is now: Lermontovo (formerly

Voskresenovka), Lori Province (formerly Kirovokan

district), Armenia.

Talpa minima Deparma, 1959:31. Type locality is “Ces.-

3am. KaBka3, BepxoBba peku beso, O1u3 nWocesiKa

XaMbIlKH, 500 Mm yp. M.” — [“north-western Caucasus,

the upper stream of River Beloy, near the settlement

Khamyshki, 500 m a. s. 1|.”] (from Borissenko et al.

2001: 164), Adygea (Adyghe) Republic, Russia. In

Deparma 1960: 97, the type locality is cited as: “Cha-

mischki am Oberlauf des Flusses Belaja; NW-Kauka-

sus; 500 m t.M. [Meter tber Meereshohe = metres

above sea level]”

T[falpa] — ofrientalis]

1959:388.

T[alpa] h[ercegoviensis] minima: Kuzyakin, 1965:50.

T[alpa] c[aeca] minima: Gromoy, Gureev, Novikov,

Sokolov, Strelkov & Chapskty, 1963:79.

T[alpa] Ifevantis] minima: Sokolov & Tembotov,

1989:249.

T[alpa] |[evantis] transcaucasica: Sokolov & Tembotov,

1989:249. First use of current name combination.

T[alpa] transcaucasica: Demurtas, Silstpir, Searle, Bil-

ton & Gundtiz, 2020 (unpaginated early online release).

transcaucasica: Vereschagin,

Diagnosis. Identical to the eastern sublineage of Demur-

tas et al. (2020) and to the Eastern lineage of Talpa le-

vantis as retrieved in this study through the phylogenetic

analysis of the mitochondrial Cyt b gene. In our dataset,

the subspecies transcaucasica has unique mutations in

comparison with sequences of both the nominotypical

subspecies and 7: I. dogramacii new subspecies at the

following positions of our Cyt 5 alignment (see Appen-

dix 2): 42:T, 54:G, 162:G, 213:C, 219:T, 223:C, 225:A,

231:G, 246:T, 279:C, 396:A, 480:C, 603:T, 640:T, 651:C,

667:C, 675:G, 678:C, 858:G, 867:T, 913:T, 1008:T.

Description and comparison. Similar to the remain-

ing subspecies and the differences are on average. For

comparisons see under 7! /. dogramacii ssp. nov. and the

nominate subspecies.

Distribution. The north-eastern and eastern Black Sea

coast, the Lesser Caucasus in north-eastern Turkey, Geor-

gia, and Armenia, and the Greater Caucasus in Georgia

and Russia.

Miscellaneous. Deparma published the taxonomic de-

scription and naming of 7a/pa minima in two papers,

in Russian (Deparma 1959) and in German (Deparma

1960). This caused the inconsistency in reporting the

year of publishing the name. While Russian authors con-

©ZFMK

Taxonomic revision of the Levant moles of Turkey 287

sistently quoted 1959 (Gureev 1979, Gromov et al. 1963,

Kuzyakin 1965, Pavlinov & Rossolimo 1987, Sokolov &

Tembotov 1989, Zaytsev et al. 2014), Western authors

were aware only of the German version and cited 1960

(Hutterer 2005).

Sokolov & Tembotov (1989) recognized minima as

subspecifically distinct from transcaucasica. The for-

mer is smaller (mean CbL is 28.66 mm in males and

28.25 mm in females) and occupies the western Cauca-

sus; the latter is larger (mean CbL 1s 30.12 mm in males

and 30.02 mm in females) and lives in the north-central

Piedmont of the Greater Caucasus and the eastern Lesser

Caucasus (Sokolov & Tembotov 1989).

Talpa_ levantis dogramacii ssp. nov.

KryStufek, Selcuk, Hutterer & Astrin

(Figs. 6a, 7)

urn: |sid:zoobank. org: act: E3600CE0-7682-422B-8 30B-D0A6556FCD7B

Kefelioglu,

Holotype and type locality. Skin, skull, pelvis and tissue

sample in ethanol of an adult male (OMU 1352; Fig. 7);

tissue also deposited in ZFMK (ZFMK-TIS-35886),

collected by Ahmet Yesari Selcuk in March 2019 near

Barakh village, Mt. Uludag, Bursa, Turkey (39.96056 N,

Fig. 7. Skull and mandible of the type specimen of 7alpa levan-

tis dogramacii ssp. nov. OMU 1352. Scale bar = 5 mm.

Bonn zoological Bulletin 69 (2): 275-291

29.2633 E, 1100 m above sea level). DNA of this speci-

men has been deposited (ZFMK-DNA- FD02298704) at

ZFMK, Bonn, and the cytochrome b sequence is avail-

able from GenBank (Accession number MT738557) and

Appendix II.

Measurements of holotype. Body mass 58 g, head

and body 120 mm, tail 28 mm, hind foot 18 mm, con-

dylobasal length of skull 29.8 mm, maxillary tooth-row

11.6 mm, breadth of braincase 14.7 mm, breadth of ros-

trum over canines 4.0 mm, breadth of rostrum over mo-

lars 8.7 mm, greatest length of pelvis 22.1 mm, breadth

of pelvis 11.9 mm.

Diagnosis. Identical to the Western lineage of Zalpa le-

vantis as retrieved in the phylogenetic analysis of the mi-

tochondrial Cyt 6 gene. In our dataset, the new subspe-

cies has unique mutations in comparison with sequences

of both the nominotypical subspecies (corresponding to

Central lineage) and 7. transcaucasica (Eastern lineage)

at five positions of our Cyt b alignment (see Appendix IT):

522: T, positions 654, 731, 786, 1005: G. The new sub-

species has a proportionally longer maxillary tooth-row,

a proportionally broader rostrum over molars and the

least bowed posterior margin of the braincase compared

to the other two subspecies of 7) /evantis.

Paratypes. Three individuals collected on Mt. Uludag

and preserved as museum vouchers, tissue samples and

with cytochrome b sequences deposited in the GenBank

(see Table 1). OMU 1350, an unsexed individual; pre-

served as a skull; tissue ZFMK-TIS-35885; DNA sample:

ZFMK-DNA- FD02298617; GenBank No. MT738556.

OMU 1353: an unsexed individual; preserved as a skull:

tissue ZMMU-TIS-35887; DNA sample: ZFMK-DNA-

FD02298696; GenBank No. MT738558. All paratypes in

OMU were collected in August 2018 by Ahmet Yesari

Selcuk. PMS 10,650: a female collected on 30 June 1994

by B. KryStufek, preserved as a skull, skin and postcrani-

al skeleton; GenBank No. FN640571.

Measurements of paratypes. External measurements of

a female PMS 10,650: body mass 55 g, head and body

118 mm, tail 28 mm, hind foot 17 mm. Skull measure-

ments of OMU 1350, OMU 1353, and PMS 10.650: con-

dylobasal length of skull 31.2, 29.8, 30.2 mm, maxillary

tooth-row 12.1, 11.4, 11.8 mm, breadth of braincase 14.9,

damaged, 14.4 mm, breadth of rostrum over canines 4.1,

4.1, 3.9 mm, breadth of rostrum over molars 8.9, 8.8,

8.9 mm.

Description and comparisons. Ta/pa_ levantis do-

gramacii ssp. nov. is of about the same external appear-

ance and body proportions as the remaining subspecies of

T: levantis. It differs significantly from the nominotypical

subspecies by a shorter head and body (males), shorter

©ZFMK

288 Haluk Kefelioglu et al.

condylobasal length (females) and broader rostrum over

molars (females). 7alpa |. dogramacii ssp. nov. differs

significantly from ssp. transcaucasica in having a longer

maxillary tooth-row, both absolutely (in males) and rela-

tive to length of skull (in both sexes), a narrower breadth

across molars, both absolutely and relative to length of

skull (both in males; Table 2), and a less bowed posterior

outline of the braincase (Fig. 3).

Distribution. The western-most part of the range of

T. levantis, 1.e., along the Anatolian coast of the Sea of

Marmara and westward until Zonguldak.

Etymology. 7alpa levantis dogramacii ssp. nov. is an ep-

onym to Dr. Salih Dogramaci (1 July 1941, Elena, Bul-

garia — 30 September 1993, Samsun; Fig. 8), a Professor

of zoology at the Ondokuz Mayis University, Samsun,

and an outstanding Turkish mammalogist. Among others,

Professor Dogramaci published works of crucial impor-

tance for the taxonomy of 7a/pa in Turkey (Dogramaci

1988, 1989a, b) and a revised list of Turkish mammals

(Dogramaci 1989c). He published in Turkish and in

journals with limited circulation outside of Turkey and

is therefore not well known beyond his native country.

Salih Dogramaci built an important research collection

of Turkish small mammals with well prepared and me-

ticulously labelled museum vouchers. The collection is

deposited at the Ondokuz Mayis University and also pro-

vided an invaluable source of information for the pres-

ent study. Microtus dogramacii Kefelioglu & KrySstufek,

1999, a species of social vole endemic to south-western

Asia, is another eponym to the late Professor DoSramaci.

Miscellaneous. Zalpa levantis dogramacii ssp. nov.

was first recognized as distinct from 7’ /evantis in a cra-

niometric study (Krystufek 2001) and was separated

from 7: /evantis under the tentative name Jalpa caeca

(KryStufek & Vohralik 2001).

Species of the genus 7a/pa in Turkey

Demirtas et al. (2020) stressed that Turkey is “home

to six distinct species [of moles], more than any other

comparable geographical region” which “[emphasises|

the importance of this region as a global centre of mole

diversification.” Measuring, quantifying and comparing

biodiversity can be tricky when dealing with a complex

geopolitical entity like Turkey. First, the country spreads

across two continents, which since the last glacial max-

imum were separated by the sea, but in the past were

intermittently connected by a land bridge. As discussed

above, the land bridge at the Turkish straits both facili-

tated and filtered the transcontinental faunal migrations.

As poor dispersers (KryStufek & Motokawa 2018) moles

were obviously filtered by this land corridor. As we have

seen, our study falsified the hypothesis of Demurtas et al.

Bonn zoological Bulletin 69 (2): 275-291

Fig. 8. Dr. Salih DoSramaci and his wife (Foto Yener, Ankara).

(2020) regarding the transcontinental range of 7alpa le-

vantis. The two sides of the Turkish straits have no mole

Species in common and their species evolved in differ-

ent centres of diversification, the south-eastern European

centre and in south-west Asia with further two similar

centres.

Moles with restricted distributions are usually endemic

to the Quaternary refugia and each of the main south-

ern-European peninsulas has at least two small-range

endemics of the genus 7alpa (cf. KryStufek & Motoka-

wa 2018). The number of mole endemics is remarkably

similar between centres of endemism being either two or

three endemics per centre (Table 3). Turkey does not con-

tain all endemics from any of the three centres it encom-

passes, but on the other hand, comprises three out of total

five such centres, as we know them in the western Pa-

laearctic (Table 3). The number of centres encompassed

by Turkey is the reason for the sum of partial regional

species numbers, which is high enough to rank the coun-

try higher than any other in the species richness of the ge-

nus Jalpa. This conclusion does not downgrade the high

biodiversity richness of Turkey, but makes it explicable.

Subsequently, we briefly review mole species, other

than 7: /evantis, occupying Turkey. The genus has been

reviewed by DoSramaci (1989a), Kefelioglu & Gen¢osg-

lu (1996), and KryStufek & Vohralik (2001). For karyo-

types see Sevindik (2013; for 7: europaea), Kefelioglu &

Gencoglu (1996; 7 ognevi), and S6zen et al. (2012:

T: davidiana).

©ZFMK

Taxonomic revision of the Levant moles of Turkey 289

Table 3. Presence of moles in five centers of endemism. Pres-

ences in Turkey are shown by dots. 7alpa europaea is a wide-

spread species while the remaining moles are endemic to two

centres (7: caeca) or a single centre (the rest). Centres of ende-

mism: Ip — Iberian Peninsula; It — Italian Peninsula; Ba — Bal-

kan Peninsula; PC — Pontic Mts. and the Caucasus; AH — Ana-

tolian-Iranian High Plateau and the Hyrcanian coast. Based on

KryStufek & Motokawa (2018).

Centre of endemism

Species Ib It Ba PC AH

T. europaea O e

T. occidentalis fo)

T. aquitania fo)

T. romana fe)

T. caeca O fe)

T. stankovici fe)

T. martinorum e

T. levantis e

T. ognevi e

T. caucasica fe)

T. davidiana ry

T. talyschensis fo)

Species total 23 4 3

Talpa europaea Linnaeus, 1758

Talpa europaea Linnaeus, 1758:52. Type locality (origi-

nally Europe) subsequently restricted to Sweden, Kris-

tianstad, Engelholm.

Reported for Turkey by Osborn (1964). Occupies Euro-

pean Turkey; range mapped by Dogramac1 (1989a).

Talpa martinorum KryStufek, Nedyalkov, Astrin &

Hutterer, 2018

Talpa martinorum KryStufek, Nedyalkov, Astrin & Hut-

terer, 2018 (KryStufek et al. 2018a:45). Type locality:

near Zvezdets, Mt. Strandzha, Bulgaria.

Reported for Turkey as Talpa caeca Savi, 1822 (Osborn

1964, Dogramaci 1988, 1989b), and afterwards as T°: /e-

vantis (Vohralik 1991, KryStufek & Vohralik 2001). Pres-

ence in eastern Turkish Thrace postulated by KryStufek

et al. (201 8a) and for the first time confirmed in this study.

Bonn zoological Bulletin 69 (2): 275-291

Talpa ognevi Stroganov, 1944

Talpa romana ognevi Stroganov, 1944:131. Type locali-

ty: “baxypuanu, I py3ua [Bakuriani, Georgia]”.

Reported for Turkey as 7alpa caucasica Satunin, 1908

(Dogramaci 1989b). The name ognevi was elevated to

species in KryStufek & Motokawa (2018), following the

evidence provided by Bannikova et al. (2015). Range is

in Georgia and NE Turkey (Hopa region).

Talpa davidiana (A. Milne Edwards, 1884)

Scaptochirus davidianus A. Milne Edwards, 1884:1143.

Type locality: “environs d’Akbes, sur les confins de la

Syrie et de l’Asie Mineure” (p. 1142), now Meydanek-

bez, southwest of Gaziantep, Turkey (KryS8tufek et al.

2001:140)

Earlier reported for Turkey as 7alpa streeti Lay, 1965; the

name is a junior synonym of Scaptochirus davidianus,

which is a member of the genus 7a/pa (KryStufek et al.

2001). Occupies south-eastern Turkey and Lake Van area

(Krystufek et al. 2001, S6zen et al. 2012).

Acknowledgements. We thank Anna Bannikova for providing

geo-referenced information for haplotypes from Zonguldak and

published in Bannikova et al. (2015). Marina Baskevich and

Leonid Voyta helped with references published in the Soviet

Union and Franc Janzekovié assisted with statistics. An anon-

ymous referee and the associate editor provided constructive

criticism and helped with an earlier version of the manuscript.

B. K. acknowledges the financial support from the Slovenian

Research Agency (research core funding no. P1-0255).

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APPENDICES

electronic supplements, available at http://www.zoologicalbulletin.de

APPENDIX I.

The list of museum vouchers used in this study.

APPENDIX IL.

Sequencing of the new Turkish samples.

APPENDIX III.

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©ZFMK

BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (2): 293-307

2020 - Kanturski M. & Lee Y.

https://do1.org/10.20363/BZB-2020.69.2.293

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:A23A 8204-E5CB-45BA-B01A-7DC949743D1F

Hitherto unknown and poorly known sexual morphs of three Asiatic species

of the aphid genus Uroleucon

(Hemiptera: Aphididae)

Mariusz Kanturski'* & Yerim Lee?

' Zoology Research Team, Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences,

University of Silesia in Katowice, Bankowa 9, PL-40-007 Katowice, Poland

? Insect Biosystematics Laboratory, Department of Agricultural Biotechnology, Seoul National University,

Seoul 151-921, Republic of Korea

“Corresponding author: Email: mariusz.kanturski@us.edu.pl

‘urn:lsid:zoobank.org:author:78C290A3-D07B-4A F9-9358-ED8C05A702BF

2 urn:Isid:zoobank.org:author:CC7525 15-8295-474E-B997-8EDF96C5D20B

Abstract. In this paper, we describe hitherto unknown and redescribe poorly known sexual morphs (oviparous females

and males) of three Asiatic species of the Macrosiphini genus Uroleucon Mordvilko, 1914. The oviparous female of Uro-

leucon (Uromelan) amamianum (Takahashi, 1930) is described in detail as well as the oviparous female and alate male

of U. (Uroleucon) fuchuense (Shinji, 1942). The hitherto unknown oviparous female of U. (U.) formosanum (Takahashi,

1921) is described and the poorly known alate male is redescribed. Notes about distribution and host plants of these spe-

cies are also given.

Key words. Aphids, description, U. amamianum, U. formosanum, U. fuchuense.

INTRODUCTION

Uroleucon Mordvilko, 1914 (Hemiptera: Aphididae:

Macrosiphin1), which comprises about 241 species with-

in six subgenera, is regarded as one of the most speciose

genus within the macrosiphines (Favret 2020). Members

of Uroleucon are characterised by particularly often di-

vergent antennal tubercles, apterous viviparous females

with secondary rhinaria on the antennal segment ITI, quite

a long terminal process and long and cylindrical siphun-

culi with a developed area of subapical reticulation. The

cauda is often long and finger shaped, and the first seg-

ments of the tarsi usually have five, and in several species

three or four setae. The abdomen of most Uroleucon spe-

cies bears rounded or oval scleroites and quite long setae

(Heie 1995; Blackman 2010; Blackman & Eastop 2020).

More than 170 species live on herbaceous plants that be-

long to Asteraceae and Campanulaceae (Blackman 2010;

Blackman & Eastop 2020). Uroleucon representatives

have so far been described and recorded from almost all

continents and zoogeographical regions including the

East Palaearctic.

Apterous and alate viviparous females are the most

well-known morphs of almost every species that has

been described including Uroleucon in the East Palaearc-

tic (e.g., Takahashi 1921; 1923; 1924; Miyazaki 1971;

Pashchenko & Lobkova 1990; Pashchenko 2001). On

Received: 07.09.2020

Accepted: 09.10.2020

the other hand, in many cases, the sexual morphs (ovip-

arous females and males) of many aphids are still poorly

known or unknown, and have very rarely been collected

and described. Despite this rarity, the importance of the

sexual generation has been proven in the expansion of

our knowledge of the general biology of poorly known

species, but also by solving taxonomical problems or

improving our understanding of the evolution of aphids

(Iharco 1965; Wieczorek et al. 2013; Depa et al. 2015;

Pérez Hidalgo et al. 2016; Kanturski et al. 2017; Nowins-

ka et al. 2017; Stekolshchikov & Buga 2017; Kanturski

et al. 2018; Mier Durante et al. 2020).

In the Republic of Korea, a total of 20 species of Uro-

leucon have been recorded to date (Lee et al. 2002a; Lee

et al. 2002b; Choi et al. 2012; Choi 2019). However, there

has been little research on their sexual morphs. During an

examination of the aphid collection in the Biology Cen-

tre of the Czech Academy of Sciences, Institute of Ento-

mology, Ceské Budéjovice (Czech Republic), specimens

of unknown and poorly known sexual morphs of three

native East Palaearctic species of Uroleucon collected

by the late J. Holman were discovered. We describe the

oviparous female of U. (Uromelan) amamianum (Taka-

hashi, 1930), the oviparous female and alate male of

U. (Uroleucon) fuchuense (Shinji, 1941) and U. (Uroleu-

con) formosanum (Takahashi, 1921) and redescribe the

poorly known alate male of the latter.

Corresponding editor: R. Peters

Published: 27.10.2020

294 Mariusz Kanturski & Yerim Lee

MATERIAL AND METHODS

The specimens were examined using a Leica DM 3000

LED light microscope and photographed using a Leica

MC 190 HD camera using a differential interference con-

trast. The measurements were done according to Ilharco

and van Harten (1987). The current host plant names are

given according to The Plant List (2013).

The following abbreviations are used: ABD: abdomi-

nal tergite; ANT: antennae or their lengths; ANT I-VI:

antennal segments I, II, I, IV, V, VI or their lengths (ra-

tios between antennal segments are simply given as e.g.

‘VI: III’); BASE: basal part of last antennal segment or

its length; BD III: basal articular diameter of ANT III;

BL: body length (from the anterior border of the head

to the end of cauda); II] FEMORA: hind femora or their

length; HW: greatest head width across the compound

eyes; HT I: first segment of the hind tarsus; HT II: sec-

ond segment of the hind tarsus or its length; LS ANT III:

length of the longest setae of ANT III; PT: processus ter-

minalis of the last antennal segment or its length; SIPH:

siphunculus or its length; III TIBIAE: hind tibiae or their

1.00 mm

Fig. 1. Oviparous female of Uroleucon amamianum.

Bonn zoological Bulletin 69 (2): 293-307

length; URS: ultimate segments of the rostrum (IV + V)

or their lengths. In the case of a series of single slides

with a single specimen with the same collection data

for the examined material sections, all of them present

the same data as the full previous slide in order to avoid

repetition. The terminology of the male genitalia follows

Wieczorek et al. (2011). The photos of apterous vivip-

arous females of U. formosanum in Figure 6a and 6b

are used with permission of JADAM Organic Farming,

http://en.jadam.kr/news/article View. html? idxno=10121

(Daejeon, Republic of Korea)

The material examined 1s deposited in IECA — the Bi-

ology Centre of the Czech Academy of Sciences, Institute

of Entomology, Ceské Budéjovice (Czech Republic);

RESULTS

Uroleucon (Uromelan) amamianum (Takahashi, 1930)

Figs 1-2

Macrosiphum amamianum Takahashi, 1930: 318

©ZFMK

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 295

Dactynotus amamianus Takahashi, 1962: 76

Uroleucon (Uromelan) amamianum Eastop & Hille Ris

Lambers, 1976: 255

0.05 mm

The apterous viviparous females of this species are bright

shiny red to reddish brown with black antennae, siphun-

culi, cauda and distal halves of the femora (Takahashi

1930; Blackman & Eastop 2020). According to Miyazaki

(1971), Uroleucon amamianum is similar to U. lactucico-

0.10 mm ‘ 0.05 oa

Fig. 2. Oviparous female of Uroleucon amamianum, morphological details. a. ANT II secondary rhinaria. b. Third and ultimate

rostral segments. ce. Hind tibia with scent plaques distribution. d. Scent plaques, detailed view. e. Abdomen. f. Siphunculus. g. Cau-

da.

Bonn zoological Bulletin 69 (2): 293-307

©ZFMK

296 Mariusz Kanturski & Yerim Lee

Ja (Strand, 1928) due to the rather small and flat primary

rhinarium on ANT V but differs in the ratio of the SIPH/

cauda, which is less than 1.33 in the apterous viviparous

females. This is quite a poorly known species, which

as yet is only known from Japan and Korea. Miyazaki

(1971) collected many apterous and alate viviparous fe-

males mostly from Solidago virga-aurea and Aster sp. in

Japan. In The Republic of Korea, the species was record-

ed for the first time by Lee at al. (2002a), and was later

reviewed with other species of the genus Uromelan by

Choi et al. (2012), which found it on Aster pinnatifidus,

A. maackii, Patrinia scabionsaefolia, Picris hieracioides,

Solidago virga-aurea vat. asiatica and S. virga-aurea vat.

gigantus. Choi (2019) redescribed the apterous and alate

viviparous female but no sexual morphs were included.

Oviparous female — description (n = 10)

Figs 1-2

Colour in life. Unknown. Pigmentation on slide: head

brown; ANT I-II dark brown; ANT II brown with paler

bases and sometimes with paler distal end; ANT IV-VI

brown; pronotum and mesonotum usually with scleroti-

sation, brown; femora yellow with brown to dark brown

distal halves; fore and middle tibiae with yellow middle

section and dark brown bases and apices; hind tibiae

brown to dark brown, sometimes with slightly paler sec-

tions near the proximal and distal ends but the very ends

are always dark brown; tarsi dark brown; abdomen yel-

low with brown sclerites and scleroites; SIPH uniformly

dark brown, cauda dark brown (Fig. 1).

BL 3.10-3.42 mm. HW 0.57-0.59 mm, 0.15-

0.16xANT. Head with long, rigid setae with mostly

pointed apices, 0.075—0.110 mm long. ANT tubercles

each with 2-3 setae on internal angles. ANT 3.44—

3.66 mm, 1.03—1.17 x BL. ANT HI 0.81—0.87 mm with

27-38 protuberant, rounded or oval, different-sized sec-

ondary rhinaria with sclerotised rims, 0.01—0.02 mm

in diameter (Fig. 2a), ANT IV 0.63—0.67 mm, ANT V

0.56-0.60 mm. ANT VI 1.14—-1.27 mm, BASE 0.19-

0.21 mm, PT 0.95—1.08 mm, 4.57—5.68 x BASE. Other

antennal ratios: VI:III 1.37—1.49, V:HI 0.67—0.69, IV:III

0.75-0.77, PT: 1.12-1.27, PT:IV 1.50-1.63, PT:V

1.65—1.89. ANT chaetotaxy: ANT have thick, rigid setae

with slightly blunt or narrow capitate apices. ANT III se-

tae 0.03-0.05 mm long, LS ANT III 1.12—1.25 x BD III.

ANT I with 10-11, ANT II with 4, ANT HI with 20-26,

ANT IV with 12-14, ANT V with 8-12 setae. ANT VI

with 2—3 basal, 3-4 apical and 4-6 setae along the PT.

Rostrum reaching hind coxae. URS 0.16—0.17 mm, 0.18—

0.20xANT II, 0.12-0.14xANT VI, 0.14-0.17 PT,

0.80—0.89 x BASE and 1.30-1.36 x HT II with 8-9 fine,

pointed accessory setae (Fig. 2b). Mesosternal furca

fused, wide, without stem. HI FEMORA 1.22—1.25 mm

with medium-length to long, stiff, rigid setae with point-

ed or slightly blunt apices, 0.020—0.05 mm long. III TIB-

Bonn zoological Bulletin 69 (2): 293-307

IAE 2.17—2.25 mm, swollen with large number (c. 300—

330) of rounded to oval or some 8-shaped scent plaques

(pseudosensoria) on entire area and length (besides the

very ends) (Fig. 2c—d). Setae on II] TIBIAE rigid with

mostly pointed or slightly blunt apices, 0.020—0.085 mm

long. HT I with 3:3:3 setae, HT II 0.12—0.13 mm, 0.14—

O.15xANT II, 0.09-0.11xANT VI, 0.11-0.13 x PT

and 0.61—0.65 x BASE. Abdomen membranous, with

well-visible, rounded and irregular scleroites in spinal,

dorsal and marginal areas (Fig. 2e), without marginal

tubercles with medium-length to long, thick, rigid setae

with pointed or slightly blunt apices, 0.055—0.110 mm

long on ABD TERG I-V and 0.070-0.120 mm long on

ABD TERG VI-VHI. ABD VII with 8—9 setae. SIPH

0.67—0.70 mm, tubular, tapering, straight with distinct

zone of subapical reticulation, well-developed postsi-

phuncular sclerites and small flange (Fig. 2f). Reticu-

lated zone 0.31—0.37 x SIPH. SIPH 1.22-1.40 x cauda,

0.20-0.21 x BL and 0.79-0.82 x ANT III. Genital plate

with 2-3 anterior, 6-12 median and 28—29 posterior se-

tae. Cauda 0.49-0.57 mm long and 0.19—0.22 mm wide,

tapering, slightly constricted near base, 2.27—3.00 x its

width at base and 0.15—0.16 x BL with 22—26 fine, point-

ed setae of two lengths (Fig. 2g).

Material examined. REPUBLIC OF KOREA, Gyeo-

nggi-do, Pocheon-si, Gwangneung Royal Tomb Arbo-

retum, Dendrological Park, 19 October 2000, Solidago

virgaurea, J. Holman leg., 1 oviparous female, 1 apter-

Ous viviparous female, 0OH075 (ovipara 9-10) (IECA), 2

oviparous females, 0OHO75 (ovipara 19-20), 2 oviparous

females, 0OH075 (ovipara 21-22), 1 oviparous female, 1

apterous viviparous female 00H075 (ovipara 23-24), 2

oviparous females, 0OHO75 (ovipara 25-26), 2 oviparous

females, 00OH075 (ovipara 27-28).

Uroleucon (Uroleucon) formosanum (Takahashi, 1921)

Figs 3-6

Macrosiphum formosanum Takahashi, 1921: 6

Dactynotus (Dactynotus) formosanus Takahashi, 1962:

Uroleucon formosana Ghosh et al. 170: 390

This species 1s one of the most commonly recorded Uro-

leucon in Eastern Asia, feeds mostly on species of Lactu-

ca, Ixeris, Picris, Sonchus and others (Higuchi & Miyaza-

ki 1969; Holman 2009) and can be easily recognised by

its very long ANT III (in comparison to ANT IV and V)

and large and extremely protuberant secondary rhinaria.

Apterous viviparous females are shining red-brown with

a broad black patch on the proximal part of the abdomen,

black siphunculi and a pale yellow cauda (Fig. 3a—b).

Alate viviparous females are similar in colour, with dark

dorsal side of thorax and darker ventral side of abdomen

(Fig. 3c). The species was described from Taiwan based

©ZFMK

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 297

Fig. 3. Uroleucon formosanum viviparous generation on Lactuca and U. fuchuense in Korea. a. Colony of apterous viviparous

females and larvae of U. formosanum. b. Apterous viviparous female of U. formosanum colour. c. Alate viviparous female of

U. formosanum colour d. Apterous viviparous female of U. fuchuense colour.

on the viviparous generation (Takahashi 1921). In the

same paper, Takahashi gave information that in Novem-

ber sexual morphs were observed near Tokyo in Japan,

but not in Taiwan. Later, Takahashi provided information

that the alate males and oviparous females occur in Japan

from the last part of October until the end of November,

whereas near Taihoku, the viviparous generations were

observed throughout the year (Takahashi 1923). Shinji

(1941) redescribed the viviparous generation and gave

only a brief description of the alate male but as his mono-

graph is in Japanese, the information was not available

for a broad group of researchers. As for the occurrence,

besides Taiwan (Takahashi 1921, 1923, 1924), the Ko-

rean Peninsula (Okamoto & Takahashi 1927; Lee et al.

2002b; Choi 2019; Choi et al. 2019) and Japan (Taka-

hashi 1921; Shinji 1941; Miyazaki 1971; Sorin 1992:

Sorin & Arakawa 2005; Adachi & Yoshitomi 2012, 2013;

Yoshitom1 2014a, b, 2015), U. formosanum 1s known

from China (Lou 1935; Tao 1963, 1968), India (Ghosh

et al. 1970), Russian Far East (Pashchenko 1988, 2000)

and Vietnam (Szelegiewicz 1968) in Asia. The species

has been also recorded from Mariana Islands (Microne-

Bonn zoological Bulletin 69 (2): 293-307

sia) which belong to the USA (Miller et al. 2003). Pike

et al. (2005) provided a detailed redescription of the ap-

terous and alate viviparous female during the comparison

with U. sonchellum but the sexual generation was still

not included.

Oviparous female — description (n = 9)

Figs 4—5

Colour in life. very similar to the apterous viviparous

female (Shinji 1941). Pigmentation on slide: head and

thorax dark brown; ANT uniformly brown to dark brown

with sometimes slightly paler distal parts of ANT I'V and

ANT V; femora yellow with dark brown distal halves;

fore and middle tibiae yellow middle sections and dark

brown proximal and distal ends; hind tibiae brown with

slightly paler distal half and dark brown proximal and

distal ends; tarsi dark brown; abdomen yellow with

brown sclerites and scleroites; SIPH uniformly dark

brown, cauda yellow or pale (Fig. 4a).

BL 2.77-3.57 mm. HW _ 0.50-0.55 mm, 0.14—

0.17xANT. Head with medium-length, fine, rigid setae

©ZFMK

Mariusz Kanturski & Yerim Lee

298

1.00 mm

Fig. 4. Sexual morphs of Uroleucon formosanum. a. Oviparous female. b. Alate male.

Bonn zoological Bulletin 69 (2): 293-307 ©ZFMK

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 299

0.05 mm

Fig. 5. Oviparous female of Uroleucon formosanum, morphological details. a. ANT II secondary rhinaria. b. Third and ultimate

rostral segments. ec. Hind tibia with scent plaques distribution. d—e. Scent plaques, detailed view. f. Abdomen. g. Siphunculus.

h. Cauda.

with mostly pointed apices, 0.035—0.070 mm long. ANT

tubercles each with 2—3 setae on internal angles. ANT

2.93—3.73 mm, 1.04—1.09 x BL. ANT III very long, 1.15—

1.57 mm, with 78-110 mostly rounded and oval, differ-

ent-sized and extremely protuberant secondary rhinaria,

without sclerotised rims (Fig. 5a), ANT IV 0.31—0.41 mm,

ANT V 0.30-0.41 mm. ANT VI 0.89-1.07 mm, BASE

0.12-0.16 mm, PT 0.77—0.92 mm, 5.56—6.41 x BASE.

Other antennal ratios: VI:III 0.66—0.77, V:HI 0.24—0.27,

Bonn zoological Bulletin 69 (2): 293-307

IV:III 0.25—0.26, PT:HI 0.56-0.66, PT:ITV 2.22—2.56,

PT:V 2.24-2.56. ANT chaetotaxy: ANT bearing thick,

rigid setae with mostly pointed or slightly blunt apices.

ANT III setae 0.020-0.035 mm long, LS ANT III 0.62—

0.87 BD III. ANT I with 6-7, ANT II with 4, ANT III

with 18-26, ANT IV with 5-6, ANT V with 5-7 setae.

ANT VI with 3-4 basal, 4 apical and 4—5 setae along the

PT. Rostrum reaching hind coxae. URS 0.17 mm, 0.10—

0.14xANT ID, 0.15-0.19xANT VI, 0.18-0.22 x PT,

©ZFMK

300 Mariusz Kanturski & Yerim Lee

1.06—1.41 x BASE and 0.94—1.03 x HT II, with 8—9 short,

fine, pointed accessory setae (Fig. 5b). Mesosternal fur-

ca fused, wide and robust, without or with poorly-devel-

oped and very stem. IIT FEMORA 1.05—1.30 mm, bear-

ing medium-length to long, thick, rigid setae with mostly

pointed or slightly blunt apices, 0.020-0.045 mm long.

Ill TIBIAE 1.87—2.30 mm, swollen in the proximal part

with large number (c. 313-343) of mostly rounded or

slightly irregular scent plaques (pseudosensoria) on the

entire area and length (besides the very ends) (Fig. 5c—e).

III TIBIAE bearing rigid setae with mostly slightly point-

ed apices, 0.020-0.055 mm long. HT I with 5:5:5 ventral

setae, HT II 0.16—0.18 mm, 0.11-0.14xANT HI, 0.16—

0.18xANT VI, 0.19-0.21 xPT and 1.12—1.37 x BASE.

Abdomen membranous, with small but well-visible,

rounded or irregular scleroites in spinal, dorsal and

marginal area, without marginal tubercles, with medi-

um-length to long, rigid setae with pointed apices, 0.035—

0.075 mm long on ABD TERG I-V and 0.040—0.085 mm

long on ABD TERG VI-VIII. SIPH with well-developed

antesiphuncular and postsiphuncular sclerites (Fig. Sf).

SIPH 0.67—0.90 mm, tubular, tapering, rather straight,

with distinct zone of subapical reticulation and flange

(Fig. 5g). The reticulated zone 0.24—0.29 x SIPH. SIPH

1.26—1.69 x cauda, 0.24—0.26 x BL, and 0.54—0.60 x ANT

II. Genital plate with two anterior setae that are longer

than the others, 8—14 median and 18—21 posterior setae.

Cauda finger-shaped, 0.53-0.55 mm, long and 0.17—

0.22 mm wide, 2.40—3.11 <its width at base and 0.15—

0.19 x BL, with 26-28 fine setae of two lengths (Fig. Sh).

Alate male — redescription (n =4)

Figs 4, 6

Colour in life. Unknown. Pigmentation on slide: head

and thorax brown; ANT brown except basal part of ANT

If] and ANT VI PT which are paler; coxae brown; femora

brown with yellow proximal parts or halves; tibiae with

yellow middle section and brown apices; tarsi brown;

SIPH brown; cauda pale (Fig. 4b).

BL 2.07-2.55 mm. HW 0.44-0.48 mm, 0.16—

0.17xANT. Head with fine, rigid setae with pointed

apices, 0.025—0.040 mm long. ANT tubercles each

with 3-4 setae on internal angles. ANT 2.58—3.00 mm,

1.17-1.30x BL. ANT III long, 0.91-1.05 mm, with 56—

80 mostly rounded, different-sized, secondary rhinaria

with sclerotised rims located on the whole length and

surface (Fig. 6a—b), ANT IV 0.28—0.37 mm, with only

3-5 secondary rhinaria (Fig. 6c). ANT V, 0.29-0.39 mm,

with 5—13 secondary rhinaria (Fig. 6d). Primary rhinaria

rims on ANT V and VI with delicate projections (Fig. 6e,

f). ANT VI 0.88-1.01 mm, BASE 0.12-0.15 mm, PT

0.76-0.86 mm, 5.64—-6.33 x BASE. Other antennal ra-

tios: VIII 0.88-1.01, V:HI 0.31-0.37, IV:IH 0.30—0.37,

PT:HI 0.75—-0.86, PT:IV 2.19-2.71, PT:V 2.25-2.62.

ANT has short, thick, rigid setae with slightly pointed

Bonn zoological Bulletin 69 (2): 293-307

or blunt apices. ANT III setae 0.015—0.030 mm long,

LS ANT II 0.71-0.83 x BD III. ANT I with 46-7, ANT

II with 4, ANT IT with 22-26, ANT IV with 7, ANT V

with 6-8 setae. ANT VI with 3-4 basal, 4 apical and

4—S setae along the PT. Rostrum reaching metaster-

num. URS 0.14—0.16 mm, 0.14—0.16xANT III, 0.15—

0.16xANT VI, 0.18-0.19*PT, 1.06—-1.20 x BASE and

0.93—1.06 x HT II, with 7—8 fine, pointed accessory setae

(Fig. 6g). IIT FEMORA 0.83-0.92 mm, with short to me-

dium-length, thick, rigid setae with pointed or blunt api-

ces, 0.012—0.035 mm long. III TIBIAE 1.45—1.82 mm,

have thick, rigid setae with mostly pointed or blunt api-

ces, 0.004—0.045 mm long. HT I with 5:5:5 ventral setae,

HT II 0.14-0.16 mm, 0.15xANT ID, 0.14-0.17 x ANT

VI, 0.10-0.20xPT and 1.00—-1.16xBASE. Abdomen

membranous, with rounded or oval scleroites, without

marginal tubercles with medium-length, fine setae with

pointed apices, 0.020-0.055 mm long on ABD TERG

I-V and 0.025—0.060 mm long on ABD TERG VI-VIII.

ABD VII with 4 setae. SIPH with ante- and postsiphun-

cular sclerites (Fig. 6h). SIPH 0.30—0.41 mm, tubular,

slightly tapering, straight with distinct zone of subapical

reticulation and flange (Fig. 61). Reticulated zone 0.24—

0.26 xSIPH. SIPH 1.30—2.00xcauda, 0.14—0.17 x BL,

and 0.32-0.41 x ANT III. Cauda long-triangular, 0.20-—

0.25 mm long and 0.10—0.14 mm wide, without constric-

tion, 1.42—2.30 xits width at base and 0.08-0.11 x BL

with 11-12 fine setae of two lengths. Parameres triangu-

lar in ventral, flattened in ventrolateral side with round-

ed tips covered with numerous short, fine, pointed setae.

Basal part of phallus as long as or slightly longer than

parameres with numerous sensilla (Fig. 6)).

Material examined. REPUBLIC OF KOREA, Gyeong-

gi-do, Suwon-si, Seoul National University campus, 15

October 2000, Picris hieracloides glabrescens, J. Hol-

man leg., 1 alate male, OOH033 (IECA); /xeris dentata,

2 alate males, O0OH025 (IECA); RDA (Yogi-San), 05

October 2000, /. dentata, J. Holman leg., 1 alate male,

OOHo01 (IECA); Gyeonggi-do, Suwon-si, NIAST, (Mt.

Yeogi-San), 05 October 2000, 1. dentata, J. Holman leg.,

2 oviparous females, OOH0O1 (ovipara 1-2) (IECAO), 2

Oviparous females OOH0O1 (ovipara 3-4) (IECA), 1 ap-

terous viviparous female, 2 oviparous females 00H001

(ovipara 5-7) (IECA); Gyeonggi-do, Suwon-si, Seoul

National University campus, 15 October 2000, P. hiera-

cioidea glabrescens, J. Holman leg., 2 oviparous females,

00H033 (ovipara 4-5) (IECA), 1 apterous viviparous fe-

male, 1 oviparous female, O0H033 (apt. 3+ovipara 1)

(IECA).

©ZFMK

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 301

0.10 mm

0.20 mm

0.10 mm 0.10 mm

= 0.05 mm 0.10 mm

Fig. 6. Alate male of Uroleucon formosanum, morphological details. a. ANT III secondary rhinaria distribution. b. Secondary

rhinaria structure. c. ANT IV secondary rhinaria distribution. d. ANT V secondary rhinaria distribution. e. Structure of primary

rhinaria on ANT V. f. Primary rhinaria on ANT VI. g. Third and ultimate rostral segments. h. Abdomen. i. Siphunculus. j. Genitalia.

Uroleucon (Uroleucon) fuchuense (Shinji, 1942) Uroleucon fuchuense Eastop & Hille Ris Lambers, 1976:

higses 58

Macrosiphum fuchuensis Shinji, 1942: 4 Apterous viviparous females of U. fuchuense are charac-

Dactynotus (Dactynotus) fuchuense Takahashi, 1962:75 _ terised by a shiny salmon red to reddish brown colour in

life with dark antennae, distal halves of femora, dark tib-

Bonn zoological Bulletin 69 (2): 293-307 ©ZFMK

302 Mariusz Kanturski & Yerim Lee

1.00 mm

sf!

Fig. 7. Sexual morphs of Uroleucon fuchuense. a. Oviparous female. b. Alate male.

©ZFMK

Bonn zoological Bulletin 69 (2): 293-307

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 303

iae and pale cauda (Fig. 3d). Although this poorly known

species is similar to U. monticola (Takahashi, 1935) due

to the presence of a row of short, peg-like setae on the

hind tibiae, it can be distinguished from it by ANT III

with more than 20 secondary rhinaria, the SIPH only

slightly longer than the cauda which has more than 35 se-

tae. The species is known from Korea (Lee et al. 2002b;

Choi 2019), Japan (Shinji 1941; Miyazaki 1971) and the

Russian Far East (Pashchenko 1988, 2000, 2001). Mi-

yazaki (1971) collected many apterous and alate vivipa-

rous females from Aster scaber. It has also been included

in the review of the Uroleucon of Korea by Lee et al.

(2002b) and A. scaber and Lactuca raddeana are the

host plants. In the Russian Federation, U. fuchuense is

known from Kamchatka and the Primorsky Krai (Pash-

chenko 2001; Pashchenko & Lobkova 1990). Although

Pashchenko (2001) provided a detailed redescription of

an apterous and alate viviparous female, the sexual gen-

eration was still unknown.

Oviparous female — description (n = 8)

Figs 7-8

Colour in life. Unknown. Pigmentation on slide: head

brown; ANT uniformly brown with only slightly paler

PT and sometimes slightly paler base of ANT III; pro-

notum and mesonotum usually sclerotised, brown; fem-

ora of legs yellow with dark brown distal halves; fore

and middle tibiae yellow to light brown in proximal

half, knee areas and distal halves dark brown; hind tibi-

Fig. 8. Oviparous female of Uroleucon fuchuense, morphological details. a. ANT III secondary rhinaria. b. Third and ultimate

rostral segments. c. Hind tibia with scent plaques and a peg-like setae distribution (arrows). d. Scent plaques, detailed view, and

peg-like setae location (arrow) e. Peg-like setae, detailed view. f. Abdomen. g. Siphunculus. h. Cauda.

Bonn zoological Bulletin 69 (2): 293-307

©ZFMK

304 Mariusz Kanturski & Yerim Lee

0.05 mm

0.20 mm

Fig. 9. Alate male of Uroleucon fuchuense, morphological details. a. ANT III secondary rhinaria distribution. b. Secondary rhinar-

ia structure. ec. ANT IV secondary rhinaria distribution. d. ANT V secondary rhinaria distribution. e. Primary rhinaria on ANT V.

f. Primary rhinaria on ANT VI. g. Third and ultimate rostral segments. h. Abdomen. i. Siphunculus. j. Genitalia.

ae brown with paler proximal part and dark brown knee

area and distal halves; tarsi dark brown; abdomen yellow

with brown sclerites and scleroites; SIPH uniformly dark

brown, cauda yellow (Fig. 7a).

BL 3.60-4.20 mm. HW 0.63-0.66 mm, 0.14—

0.15xANT. Head with long, rigid setae with apices,

0.070-0.090 mm long. ANT tubercles each with 3 setae

Bonn zoological Bulletin 69 (2): 293-307

on internal angles. ANT 4.20-4.41 mm, 1.05—1.16 x BL.

ANT HUI 1.01-1.12 mm, with 20-26 mostly round, dif-

ferent-sized secondary rhinaria with very well-devel-

oped sclerotised rims (Fig. 8a), ANT IV 0.73-0.76 mm,

ANT V 0.71-0.73 mm. ANT VI 1.36—-1.46 mm, BASE

0.20-0.24 mm, PT 1.14—1.22 mm, 5.08—5.85 x BASE.

Other antennal ratios: VI:HI 1.26—1.34, V:HI 0.64—0.72,

©ZFMK

Hitherto unknown and poorly known sexual morphs of three Asiatic species of the aphid genus Uroleucon 305

IV: 0.67-0.72, PT:IIT 1.08-1.12, PT:IV 1.56—1.60,

PT:V 1.56—-1.69. ANT chaetotaxy: ANT has thick, rig-

id setae with mostly pointed or slightly blunt apices.

ANT HI setae 0.025—0.060 mm long, LS ANT HI 1.00—

1.33 x BD IN. ANT I with 7-9, ANT II with 3-5, ANT

IH with 28-33, ANT IV with 16-17, ANT V with 11-12

setae. ANT VI with 3 basal, 3 apical and 8 setae along

PT. Rostrum reaching hind coxae. URS 0.17—0.19 mm,

0.16xANT IE, 0.12-0.13xANT VI, 0.14—0.15 x PT,

0.77-0.87 x BASE and 1.06—1.11xHT II with 9-10

short, fine, pointed accessory setae (Fig. 8b). Mesoster-

nal furca fused, wide without stem. IIT FEMORA 1.37—

1.47 mm, with medium-length, thick, rigid setae with

mostly pointed or slightly blunt setae, 0.025—0.065 mm

long. III TIBIAE 2.62—2.80 mm, swollen in the proximal

part with large number (c. 340-363) of mostly rounded

or slightly irregular scent plaques (pseudosensoria) on

entire area and length (except very ends) (Fig. 8c—d).

III TIBIAE have rigid setae with mostly slightly pointed

apices, 0.025—0.080 mm long and a row or very minute

peg-like sensilla on ventral side (Fig. 8e). HT I with 5:5:5

ventral setae, HT H 0.16—0.17 mm, 0.14—0.15 x ANT III,

0.11xANT VI, 0.13-0.14<PT and 0.70—0.80 x BASE.

Abdomen membranous, with by well-visible mostly

irregular scleroites in spinal, dorsal and marginal areas

(Fig. 8f),without marginal tubercles with long, rigid

setae with mostly pointed apices, 0.007—0.10 mm long

on ABD TERG I-V and 0.075—0.12 mm long on ABD

TERG VI-VII. SIPH 0.72-0.81 mm, tubular, slightly

tapering, slightly curved with distinct zone of subapical

reticulation and flange (Fig. 8g). Reticulated zone 0.23—

0.26 xSIPH. SIPH 1.20-1.22xcauda, 0.19-0.20 x BL,

and 0.71-0.72 x ANT III. SIPH surrounded by well-de-

veloped postsiphuncular sclerites. Genital plate with two

anterior setae that are longer than the others, 10-14 me-

dian and 15-20 posterior setae. Cauda 0.59-0.66 mm

long and 0.20-0.25 wide, tongue-shaped, slightly con-

stricted near base, 2.64—2.95 x its width at base and 0.15—

0.17 x BL with 40-44 fine setae of two lengths (Fig. 8h).

Alate male — description (n = 6).

Figs 7, 9

Colour in life. Unknown. Pigmentation on slide: head

and thorax light brown to brown; ANT uniformly brown

to dark brown except basal part of ANT III and ANT VI,

which are usually paler; coxae brown; femora with yel-

low bases and brown to dark brown distal 2/3 of their

length; tibiae brown with light brown to yellow section

near proximal part; tarsi brown; SIPH brown; cauda pale

to yellow (Fig. 7b).

2.65—3.02 mm. HW 0.56—0.59 mm, 0.14—0.16 x ANT.

Head with medium-length, fine setae with pointed apices,

0.025—0.055 mm long. ANT tubercles each with 3 setae

on internal angles. ANT 3.47-4.06 mm, 1.27—1.44 x BL.

ANT II 0.75—0.80, with 44-65 rounded or slightly oval,

Bonn zoological Bulletin 69 (2): 293-307

different-sized, secondary rhinaria with well-developed

sclerotised rims located on entire length but not on entire

surface of segment (Fig. 9a—b), ANT IV 0.60-0.80 with

12-19 secondary rhinaria mostly in one row (Fig. 9c).

ANT V 0.60—0.68 mm, with 12-17 rhinaria mostly in

one row (Fig. 9d). Primary rhinaria surrounded by scle-

rotic rim with minute projections (Fig. 9e—-f). ANT VI

1.26—-1.45 mm, BASE 0.18—0.22 mm, PT 1.08—1.25 mm,

5.13-6.25 x BASE. Other antennal ratios: VI:II 1.53-

1.68, V:II 0.75—0.80, IV: 0.77-0.91, PT:III 1.28-1.44,

PT:IV 1.56—1.58, PT:V 1.75—1.83. ANT have short or

medium-length thick, rigid setae with pointed or slightly

blunt apices. ANT III setae 0.015—0.045 mm long, LS

ANT III 0.87-1.12 x BD III. ANT I with 8-9, ANT II

with 4-5, ANT II with 25-32, ANT IV with 12-15, ANT

V with 9-10 setae. ANT VI with 3-4 basal, 3-4 apical

and 5—7 setae along the PT. Rostrum reaching meso or

metasternum. URS 0.17—0.18 mm, 0.19—0.22 x ANT III,

0.12-0.13x ANT VI, 0.14—0.15 x PT, 0.77-0.94 x BASE

and 1.17—1.21 x HT I with 9-11 fine, pointed accesso-

ry setae (Fig. 9g). IIT FEMORA 1.05—1.17 mm, bearing

short to medium-length, rigid setae with pointed api-

ces, 0.010-0.055 mm long. II] TIBIAE 2.05—2.30 mm,

bearing thick, rigid setae with pointed apices, 0.030-—

0.065 mm long. HT I with 5:5:5 ventral setae, HT II

0.14-0.15 mm, 0.15-0.18xANT II, 0.10-0.11 x ANT

VI, 0.12 x PT and 0.63—0.77 x BASE. Abdomen membra-

nous, with very few scleroites (Fig. 9h), small margin-

al tubercles on marginal sclerites on ABD II-IV (which

can be poorly visible in some specimens) and with long

and fine setae with pointed apices, 0.035—0.060 mm

long on ABD TERG I-V and 0.050—0.080 mm long

on ABD TERG VI-VHI. ABD VIII with 4 setae. SIPH

0.44-0.46 mm, tubular, straight with distinct zone of

subapical reticulation and small but well-visible flange

(Fig. 91). The reticulated zone 0.21—0.26 x SIPH. SIPH

1.48-1.55 x cauda, 0.16—0.16 x BL, and 0.51-0.60 x ANT

II. SIPH surrounded by ante- and postsiphuncular scler-

ites. Cauda 0.29-0.31 mm long and 0.12—0.16 mm wide,

tapering, without constriction, 1.93—2.41 <its width at

base and 0.09-0.10 x BL, with 18—24 fine, pointed setae

of two lengths. Parameres robust, subtriangular in ven-

tral, slightly flattened in ventrolateral side, with rounded

tips, covered by with numerous short, fine, pointed setae.

Basal part of the phallus not longer than the parameres

with numerous sensilla (Fig. 9)).

Material examined. REPUBLIC OF KOREA, Gyeo-

nggi-do, Pocheon-si, Gwangneung Royal Tomb Arbore-

tum, 19 October 2000, Aster scaber, J. Holman leg., 1

alate male, O0OH079-80 (IECA), 1 alate male, O0OH079-80

(IECA), 1 alate male, 00H079-80 (IECA), 1 alate male,

00H079-80 (IECA), 1 alate male, 00H079-80 (IECA),

1 alate male, 00H079-80 (IECA), 1 oviparous female, 1

apterous viviparous female, 00OHO79-80 (IECA), 1 ovip-

arous female, 1 apterous viviparous female, OOHO79-80

©ZFMK

306 Mariusz Kanturski & Yerim Lee

(IECA), 2 oviparous females, 00OHO79-80 (IECA), 2

Oviparous females, O0OHO79-80 (IECA), 2 oviparous fe-

males, 00HO79-80 (IECA).

Acknowledgements. We are sincerely grateful to Ale’ Bezdék

(Biology Centre of the Czech Academy of Sciences, Ceské

Budéjovice, Czech Republic) for his kind assistance and support

during the visits to the collection as well as for the loan of the

many slides. Special thanks also go to Prof. Colin Favret (Mon-

tréal University, Canada), Prof. Shin-Ichi Akimoto (Hokkaido

University, Sapporo, Japan), Dr. Masakazu Sano (Hokkaido Ag-

ricultural Research Center, Japan) and Dr. Andrey Stekolshchi-

kov (Russian Academy of Sciences, Russia) for access to many

papers and translations of papers on East Palaearctic Uroleu-

con species. We would like to thank JADAM Organic Farming

(Daejeon, Republic of Korea) for access and permission to use

the photos of live U. formosanum apterous viviparous females

and Prof. Hyojoong Kim (Kunsan National University, Repub-

lic of Korea) for photos of alate viviparous females of U. for-

mosanum and apterous viviparous female of U. fuchuense.

Mariusz Kanturski gratefully acknowledges the Scholarship for

Outstanding Young Scientists from the Ministry of Science and

Higher Education of Poland (1165/E—340/ST YP/12/17).

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©ZFMK

BHL

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AM Z5ENiG Bonn zoological Bulletin 69 (2); 309-366 ISSN 2190-7307

2020 - Steenis J. van et al. http://www.zoologicalbulletin.de

https://do1.org/10.20363/BZB-2020.69.2.309

Research article

urn:|sid:zoobank.org:pub:34A9FC4A-EBEC-4617-A91B-C3D767E24A11

Faunistical overview of the European species of the genera

Brachyopa Meigen, 1822 and Hammerschmidtia Schummel, 1834

(Diptera: Syrphidae)

Jeroen van Steenis'*, Menno P. van Zuijen’, Sander Bot’, Leendert-Jan van der Ent*, Anatolij Barkalov’, André van Eck®,

Julien Fleury’, Rita Féldesi®, Helge Heimburg’, Jiti Hadrava"’, Barbel Koch", Erikas Lutovinovas”, Libor Mazanek’’,

Frank Van de Meutter™, Lukasz Mielezarek"*, Christoper J. Palmer’, Grigory V. Popov’’, SnezZana Radenkovi¢"’,

Menno Reemer”, Axel M. Ssymank”’, Wouter van Steenis”!, Sandor Toth”, Ante Vuji¢? & Bastiaan Wakkie”

' Research Associate NBC—Naturalis, Leiden. % Hof der Toekomst 48, NL-3823 HX Amersfoort, the Netherlands

? Kolkakkerweg 21-2, NL-6706 GK Wageningen, The Netherlands

3 Kerklaan 30E, NL-9751 NN, Haren, The Netherlands

* Sara Mansveldweg 19, NL-6874 CB, Wolfheze, The Netherlands

° Laboratory of Systematics of Invertebrate Animals, Institute of Systematics and Ecology of Animals, Russian Academy of Sciences, Siberian

Branch, RU-I1 Frunze Street, Novosibirsk 630091, Russia

° BioMongol Foundation, Korte Hoefstraat 30, NL-5046 DB Tilburg, The Netherlands

7 271 rue de la Commune de Paris, F-45770 Saran, France

° Agroecology and Organic Farming Group, Institute of Crop Science and Resource Conservation, University of Bonn, Auf dem Higel 6,

D-53121 Bonn, Germany

° Pfanghofweg 29, A-8045 Graz, Austria

'° Department of Zoology, Faculty of Science, Charles University, Vinicnd 7, 128 43 Praha 2 & Biology Centre of the Czech Academy of Sciences,

Institute of Entomology, Branisovskd 31, CZ-370 05 Ceské Budéjovice, Czech Republic

" Via Chiusa 5, CH-6863 Besazio, Switzerland

? Laboratory of Entomology, Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania

3 Jivovd 231, CZ-783 16 Jivova, Czech Republic

4 Research Institute for Nature and Forest (INBO), Herman Teirlinckgebouw, Havenlaan 88 bus 73, BE-1000 Brussel, Belgium

'S Krakow Municipal Greenspace Authority, Reymonta 20, PL-30-059 Krakow, Poland

'© 6 Gofton Avenue, Portsmouth, PO6 2NG, United Kingdom

"7 I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Bogdan Chmielnitski Str. 15, UA-01601 Kiev, Ukraine

'823 University of Novi Sad, Faculty of Science, Department of Biology and Ecology,

Trg Dositeja Obradoviéa 2, RS-21000 Novi Sad, Serbia

” Naturalis Biodiversity Center, European Invertebrate Survey, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands

?” Falkenweg 6, D-53343 Wachtberg, Germany

?! Research Associate Naturalis Biodiversity Center, Leiden. % Vrouwenmantel 18, NL-3621 TR Breukelen, the Netherlands

22 H-8420 Zirc, Széchenyi u. 2, Hungary

4 Juliette Wytsmanstraat 69, BE-1050, Brussel, Belgium

“Corresponding author: Email: jvansteenis@syrphidaeintrees.com

‘urn:lsid:zoobank.org:author:C7FODO01C-B182-4B93-AF73-E4154367B535

7 urn:Isid:zoobank.org:author:C82093D8-EE58-47DD-B13A-4F47BDF73911

3urn:lsid:zoobank.org:author:E40B61D9-87D8-43F9-AE84-078F 10973F97

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>urn:lsid:zoobank.org:author:08 1 B4176-2B32-43B7-BBB5-E0597FA70CD9

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'Surn:lsid:zoobank.org:author:B695CD 15-B840-4090-B872-F29F83745BBA

'6urn:Isid:zoobank.org:author:4A41921E-164B-48C3-8A AF-2FCBDE7BAD5B

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'8urn:Isid:zoobank.org:author:26DF35D9-55FA-4485-8E8C-C 1 FSOEFE1 036

' urn:|sid:zoobank.org:author:9086F7C0-622F-4E5F-BDEB-14E71A027BEE

°urn:lsid:zoobank.org:author:58B9D453-586C-4B08-BA D6-BCC606E3D654

7! urn:Isid:zoobank.org:author:59753746-8DB9-4954-A 22B-6D5D582132A2

2 urn:lsid:zoobank.org:author: 189149A9-D882-46F2-A5E6-FE858E7E7159

3 urn:lsid:zoobank.org:author:A20D5863-CF | 8-4BF7-BB68-ODA75D34B7A8

4 urn:lsid:zoobank.org:author:EDD44861-E7C5-4572-B487-394B2CD7C022

Received: 03.08.2020 Corresponding editor: X. Mengual

Accepted: 15.10.2020 Published: 27.10.2020

310

Jeroen van Steenis et al.

Abstract. The European fauna of the genera Brachyopa Meigen, 1822 and Hammerschmidtia Schummel, 1834 is revie-

wed. The distribution and phenology based on extensive literature and database research are provided. The biology of

adults as well as larval habitats are treated. An illustrated key is presented for easy identification of the adults, including

three species known from adjacent Mediterranean countries. A key to the larvae, based on the available literature, is also

provided. The data originate from a study of available literature, from several databases and from the private collections

of the authors. The data are compiled into one large dataset in which all the available information is gathered together

with the source of the data. Based on the biology and trend analysis for each species it is indicated whether they show

stable, fluctuating or extremely fluctuating populations. The habitat preferences of the adults and larvae are used to dis-

cuss possible threats to each of the species for future survival. Finally, the main habitat of all species is discussed from a

conservation point of view.

Key words. Distribution, biology, habitat threats, trend analysis, identification key, larvae.

INTRODUCTION

The genera Brachyopa Meigen, 1822 and Hammer-

schmidtia Schummel, 1834 are found in the Holarctic and

Oriental realms with 44 species of Brachyopa and five

species of Hammerschmidtia currently described (Stack-

elberg 1952: Chu 1994; Van Steenis 2015; Skevington

et al. 2019). In Europe, 20 species of Brachyopa and two

species of Hammerschmidtia are known to occur (Spel-

ght 2020). Except for one species known from the Orien-

tal realm, the occurrence of both genera 1s concentrated in

the Nearctic subrealm and in the Mediterranean and Cir-

cumboreal region, and in the Caucasian and Manchurian

provinces within the Palearctic subrealm. All these bio-

geographical areas are characterized by the occurrence of

coniferous and deciduous, broadleaved forest (Udvardy

1975; Reemer et al. 2009; Van Steenis 2015; Skevington

et al. 2019). Central Europe, as part of the Circumboreal

and Mediterranean regions, harbours a high number of

species and several of them are endemic to this region

(Kaplan & Thompson 1981; Kassebeer 2000a, 2000c,

2001, 2002; Doczkal & Dziock 2004; Van Steenis & Van

Steenis 2014; Pérez-Bafion et al. 2016).

Adults of Brachyopa and Hammerschmidtia superfi-

cially resemble dung-flies (Scatophagidae) and some An-

thomyiidae and Muscidae (Torp 1994; Rotheray 1996).

They can be separated from other Syrphidae by the fol-

lowing combination of characters: small to medium sized

(4-12 mm), rather broad, mainly brown, brown-red or

black coloured flies with relatively small heads and a

yellow face; postpronotum pilose; eyes bare; basoflagel-

lomere round to oval, third antennal segment often with

clearly visible sensory pit; arista subbasal, bare to long

plumose; vein R,,. straight; crossvein rm before middle

of discal cell; vein M, oblique to vein R,,. (Meigen 1822;

Schummel 1834; Thompson & Rotheray 1998).

Larvae occur in a diverse array of microhabitats asso-

ciated with tree sap runs in or within dead or living trees.

Some of the species are generalists and can be found

in broadleaved as well as coniferous trees, while other

species seem to have a more restricted tree preference

(Lundbeck 1916; Hartley 1961; McLean & Stubbs 1990;

Rotheray 1991, 1996; Sivova et al. 1999; Krivosheina

Bonn zoological Bulletin 69 (2): 309-366

2005; Dussaix 2013; Ricarte et al. 2013). Adults, and es-

pecially the males, are regularly found patrolling dam-

aged live or dead trees with sap runs or accumulations

of sap, but also on trees, tree trunks or tree logs with no

visible sap runs or any other visible damage. Flower vis-

iting is observed regularly in most Brachyopa species

at plants with abundant, “open” and generally white co-

loured flowers, such as species within the families Apia-

ceae and Rosaceae. The flight period is from March until

July (Torp 1994; Bartsch et al. 2009; Reemer et al. 2009;

Bot & Van de Meutter 2019). It is not unusual to find

several species of Brachyopa simultaneously on the same

flower or around trees with supposed sap runs (e.g., Wak-

kie et al. 2011; Van Steenis & Van Steenis 2014; Mutin

et al. 2016).

Larvae can be separated from other Syrphidae by the

following characters: dorso-ventrally flattened; gradual-

ly elongating projections along lateral margin; posterior

respiratory process dark, longer than broad and marked

with pits and striations, four groups of sensilla anterior

to anal opening (Krivosheina & Mamaev 1967; Rotheray

1996; Rotheray & Gilbert 1999; Krivosheina 2005, 2019;

Pérez-Bafion et al. 2016).

Brachyopa larvae are slow-moving, possibly to avoid

being detected by predators such as birds, carabid beetles

and the larvae of other Diptera such as Phaonia subventa

(Harris, 1780) (Muscidae) and Systenus pallipes (Von

Roser, 1840) (Dolichopodidae) (Rotheray 1996). The lar-

vae are disguised by being coated with dried sap, espe-

cially on the posterior part of the body. This sap hides the

larvae from detection in the existing sap run by crypsis

and possibly also by the virtual absence of gustatory and

movement cues (Rotheray 1996). In general appearance

they are similar to larvae of Fannia spp. (Fanniidae) and

Nosodendron fasciculare (Olivier, 1790) (Coleoptera:

Nosodendridae) with which they often share microhabi-

tat. Some species can be very abundant in sap runs, with

100 larvae present in one sap-run, and some can tolerate

desiccation better than others with survival after desic-

cation of 65% in Brachyopa pilosa Collin, 1939 against

95% for Brachyopa insensilis Collin, 1939 (Rotheray

1996).

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

Fig. 1. Adult habitus, A-E dorsal view, F lateral view. A. Brachyopa obscura, male, Olloy-s-Viroin, Belgium. B. B. testacea, male,

Engsbergen, Belgium. C. B. vittata, male, Eupen, Belgium. D. B. zhelochovtsevi, male, Tumnin, Russian Far East. E. Hammer-

schmidtia ferruginea, male, Fiby urskog, Sweden. F. H. ingrica, male, Bychika, Russian Far East.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

312

Some authors have posed the question as to whether

Hammerschmidtia is merely a subgenus of Brachyopa

(Vockeroth & Thompson 1987; Speight 2020). Based on

recent molecular studies (Skevington et al. 2019) these

genera are clearly separated and this opinion is followed

here. One species, Brachyopa (Trichobrachyopa) tristis

Kassebeer, 2001, has been placed in a different subgenus

(Kassebeer 2001) but no phylogenetic studies are avail-

able to support this classification.

The European species of the genus Brachyopa can be

separated into two subgroups based on larval morpholo-

gy and ecology. One subgroup (which includes Brachy-

opa dorsata Zetterstedt, 1837, B. panzeri Goffe, 1945

and B. vittata Zetterstedt, 1843) comprises larvae with

a strongly developed anal segment living in the tunnels

made by other animals, mainly Coleoptera (Lymexyli-

dae). The other subgroup has larvae with a poorly devel-

oped anal segment which live in sap-runs or accumula-

tions of sap under bark (Krivosheina 2005).

Adults can be separated morphologically into three

subgroups based on the colour of the scutum, the length of

the aristal pile and the presence of an antennal pit (Zetter-

stedt 1837; Kassebeer 2000a; Doczkal & Dziock 2004).

The first subgroup comprises all species with red-brown

scutum, plumose arista and large antennal pit: Brachyo-

pa obscura Thompson & Torp, 1982, B. testacea (Fallén,

1817), B. vittata and B. zhelochovtsevi Mutin, 1998, with

possibly B. dorsata and B. panzeri also belonging to this

subgroup, or maybe forming their own group. Members

of the second subgroup have a grey pollinose scutum,

short pilose arista and a clearly visible and sometimes

very large antennal pit: Brachyopa pilosa, B. plena Col-

lin, 1939 and B. scutellaris Robineau-Desvoidy, 1844.

The species of the third and most species-rich subgroup

have a grey pollinose scutum, bare arista and, at most,

a small and weakly visible antennal pit: Brachyopa at-

lantea Kassebeer, 2001, B. bicolor (Fallén, 1817), B. bi-

maculosa Doczkal & Dziock, 2004, B. cinerea Wahlberg,

1844, B. grunewaldensis Kassebeer, 2000, B. insensilis,

B. maculipennis Thompson, 1980, B. minima Vujic &

Pérez-Bafion in Pérez-Bafion et al., 2016, B. quadri-

maculosa Thompson in Kaplan & Thompson, 1981,

B. silviae Doczkal & Dziock, 2004 and B. vernalis Van

Steenis & Van Steenis, 2014. This last subgroup has pre-

viously been referred to as the B. bicolor group or, alter-

natively, the B. guadrimaculosa group (Kassebeer 2002;

Doczkal & Dziock 2004; Pérez-Bafion et al. 2016). Fur-

ther research is needed to establish monophyly of these

morphological groups.

The starting point of this paper was the initiation of the

IUCN European Syrphidae Red List and the first work-

shop held in Novi Sad, Serbia in April 2019. For this

workshop preliminary distributional data, habitat pref-

erences and possible threats were presented as basis for

further evaluation of the species. This paper gives litera-

ture as well as original, new information on distribution,

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

phenology and habitat preferences for the species of the

genera Brachyopa and Hammerschmidtia. A short intro-

duction is presented about population dynamics of some

of the species. A literature review on habitat changes and

threats is presented too. A key is presented for the known

larvae and adults of the species. The key is based on liter-

ature and own observations on the adults. Each species is

presented based on a fixed format with information from

literature and own observations and discussion. This

could be used for a final Red List assessment as required

by the IUCN.

MATERIAL AND METHODS

The data presented here result from a merging of infor-

mation from literature sources, online and offline data-

bases, visits to museum collections as well as the acqui-

sition of new data from private collections.

The terminology used and the way the specimens are

measured is based on the comprehensive morphology list

in Skevington et al. (2019).

For countries having a centralised database including

faunistic data (e.g., Reemer et al. 2009), the data are in-

corporated in the central database of this study. Other

resources are accessible online of which the following

ones have been used for this study: Artportalen Sweden

(https://www.artportalen.se/), Artsobservasjoner Nor-

way (https://www.artsobservasjoner.no/), Diptera.info

(https://diptera.info/forum/index.php), the Finnish Bio-

diversity Information Facility (https://laji-fi/en), Global

Biodiversity Information Facility (https://www.gbif.org/,

https://doi.org/10.15468/dl.711aax), Observation.org

(https://observation.org/) including Waarneming (https://

waarneming.nl/, https://waarneming.be/), National Bio-

diversity Network UK (https://species.nbnatlas.org/) and

the National Biodiversity Data Centre Ireland (https://

maps. biodiversityireland.ie/Dataset/159). The authors of

this article have provided additional data from other re-

sources that are not published or online, such as private

collections, e.g., indicated as PJSA (private collection

Jeroen van Steenis Amersfoort) and preliminary nation-

al checklists (e.g., Austria and Switzerland). Much ad-

ditional data from literature sources is incorporated for

which details are provided in the datafile rather than in

the manuscript. All the literature consulted is listed in the

reference section.

The following collections were visited and their re-

cords are incorporated in the database with reference to

the relevant depository: FSUNS, University of Novi Sad,

Faculty of Science, Department of Biology and Ecology,

Novi Sad, Serbia; MEB, Museum of East Bohemia, Hra-

dec Kralové, Czech Republic; MMB, Moravian Museum,

Brno, Czech Republic; MWBP, Museum of West Bohe-

mia, Plzem, Czech Republic; MZH, Zoological Museum

Helsinki, Helsinki, Finland; NBC, Naturalis Biodiversity

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

Fig. 2. Adult habitus, dorsal view. A. Brachyopa dorsata, male, Hessen, Germany. B. B. panzeri, male, Hestreux, Belgium.

C. B. maculipennis, male, Fruska Gora, Serbia. D. B. pilosa, male, Drentsche Aa, the Netherlands. E. B. plena, male, Ioannina,

Greece. F. B. scutellaris, male, Savelsbos, the Netherlands.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

314 Jeroen van Steenis et al.

Center, Leiden, The Netherlands; NHM, Natural History

Museum, London, UK; NRC, Nature Research Center,

Vilnius, Lithuania; NMP, National Museum, Prague,

Czech Republic; UMO, Oxford University Museum of

Natural History, Oxford, UK; ZISP, Zoological Institute

of the Russian Academy of sciences, Saint Petersburg,

Russia; ZMSU, Zoological Museum of the Moscow

State University, Moscow, Russia; ZMUC, Zoological

Museum University, Copenhagen, Denmark.

The validity of several of the old literature records and

some of the records from websites has not been verified

by the authors. Due to name changes (Thompson 1980)

and recently split species (Kassebeer 2000a; Doczkal &

Dziock 2004; Van Steenis & Van Steenis 2014) several

old records applied the wrong names such as Brachyopa

insensilis and B. bicolor for B. grunewaldensis (Ricarte

et al. 2013) or B. insensilis identified as B. bicolor (e.g.,

Claussen 1984; Kassebeer 1993). The name B. conica

(Panzer, 1798) has been used for many species (Thomp-

son 1980) and made the separation of B. obscura from

B. testacea a puzzle (Torp 1979) until Thompson & Torp

(1982) clarified this when describing B. obscura. The

distinction of some species, especially between B. dor-

sata and B. panzeri, has been problematic (e.g., Reem-

er et al. 2007) particularly when based on photographs

alone. These difficult identifications will possibly have

affected some of the species distribution patterns. How-

ever, the most likely effect will be that it overestimates

the common species while underestimating the rare spe-

cies. This should be taken into account while reading the

discussion under each species. In addition, several na-

tional Red Lists have been published and these have been

discussed under each species, where relevant.

The information for each species is presented is a fixed

format. The Distribution section lists the known world-

wide distribution in general and the more specific Eu-

ropean distribution. The European distribution is based

on literature and own observations and we indicate if the

species is here recorded as new country record. In the

Biology section the information about the adult and lar-

val biology is given. The information about biology from

the literature is listed first, with all used references given,

and new information is listed after. The flight period and

altitudinal range are both taken from the species data-

base and consists of information from literature and new

observations. The section Population fluctuations are in-

terpretations based on the literature, own observations

and the known or suspected habitat preferences and, as

such, it is a novelty of this work. The Remarks are used

to highlight specific information about identification,

taxonomy, explanation for its distribution or other note-

worthy comments; most of this information has not been

published before. The Red List section gives an overview

of the published Red List status of the species in several

European countries followed by a novel discussion on

the possible threats for this species in Europe as a whole.

Bonn zoological Bulletin 69 (2): 309-366

The habitat and habits of the species are taken from

literature and extended by personal observations and by

notes in the consulted online and offline databases. For

each species the published information is given first with

references, followed by the unpublished information

without reference, which is referred to the main database

(see below).

The names of the food plants are taken from the litera-

ture and the current name and authorship for each taxon

is in line with the Plant List (WFO 2019).

Illustrations

The illustrations of pinned specimens were made using

a digital SLR camera. The camera setup consisted of a

Canon 6D, Canon MPE-65 macro lens, a transmitter di-

recting two flashes and a macro rail. Helicon Focus 7.6.1

stacking software was used and photos were edited in

Adobe Photoshop® 20.0.4. For the composition of the

illustrations of the basoflagellomere, a similar setup was

used with the addition of a Canon Extender EF 2x III and

a Yongnuo YN14EX macro ring lite as light source. With

the aid of a Cognisys StackShot rail, multiple pictures

were taken which were stacked with Zerene Stacker 1.03.

The illustrations of immature stages are taken from the

literature, as acknowledged under each figure. All illus-

trations were further edited and assembled into the fig-

ures with GNU Image Manipulation Program 2.8.22.0.

Databasing and distribution maps

The diverse datasets available from online databases,

collections, literature citations, institutional and private

databases and data sheets were converted to a standard-

ized database format designed to provide distribution

maps and flight activity diagrams for this paper (refered

as database hereafter).

The different coordinate systems were converted to

geodetic WGS84 coordinates. If no coordinates were

available in the dataset, on specimen labels or literature

citations, the locality information on the label / dataset /

citation was used to search Google Earth® (www.goo-

gle.nl/intl/nl/earth) and GeoNames (www. geonames.org)

for coordinates. In uncertain cases this was verified by

searching for the coordinates through the Google search

engine (www.google.com).

Some records are based on province lists. In this case,

the coordinates of the centre of the province are used.

Outliers on the maps were checked carefully, whether the

given coordinates correlate with the label/record infor-

mation.

Using records from different sources has a risk of du-

plicates with (slightly) different coordinates, for instance

coordinates of the precise location and coordinates of the

centre of the province. For the distribution maps it does

not matter that much as long as duplicate records have

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

approximately the same coordinates, especially for areas

with a high number of records. For species with fewer

than 100 records, the records were checked manually:

same date, observer and location description was used

as an indication of a duplicate. If all information in other

fields of these records supports this evidence, the deriva-

tive record was marked as a duplicate of the first record.

This was also done in areas with only a few records: the

Mediterranean, Ireland, Fenno-Scandia North of the Po-

lar circle and Russia.

For the flight activity diagrams the database was que-

ried for records of adults with a single observation da-

tum (start date = end date). This was summed per week

starting January 1“ and plotted as moving average of two

weeks. Outliers were checked manually and corrected or

rejected when information in other fields of the record

provided evidence to do so.

Altitude information from labels, literature records,

databases and datasheets were used to give an altitudi-

nal range per species. Elevations in feet were transferred

to metres and all subsequent elevations are expressed in

metres above sea level.

All data are included in the distribution maps, except

for those marked as duplicates. The distribution maps

are made in QGIS 3.10.6 with Natural EarthII (@natu-

ralearthdata.com) as background. The country borders in

the maps are from ©EuroGeographics for the adminis-

trative boundaries. Records are placed in the distribution

maps in order of year of observation, with the most re-

cent observation on top of older ones. Records with no

given date are represented with a cross; records before

1950 are represented with an open symbol (white), re-

cords between 1950 and 1999 are represented with an

open symbol with a central dot, and records from 2000

onwards are represented as filled symbols. Records with

doubtful locality data are represented with an open sym-

bol with a question mark.

RESULTS

Population dynamics

Only few published papers deal with the temporal dy-

namics of populations of the genera Brachyopa or Ham-

merschmidtia (Nilsson et al. 2007, 2012; Rotheray et al.

2008, 2014). Based on these papers and the known or

suspected larval habitat, deductions can be made on the

fluctuation in the number of populations and their den-

Sity.

In the Scottish Highlands several populations of Ham-

merschmidtia ferruginea (Fallén, 1817) have been in-

vestigated and the number of populations and popula-

tion sizes varied greatly over the years (Rotheray et al.

2008). In that work, authors discussed the decline and

rise in number of populations from as many as 13 down

Bonn zoological Bulletin 69 (2): 309-366

315

to 5, and back up to 8 over a period of 16 years. These

fluctuations were caused by randomly occurring storms

and coincided with the number of fallen trees, with an

increase in populations after a delay of 2—5 years, each of

which then lasts for 1-3 years (Rotheray & MacGowan

2000; Rotheray et al. 2014). These population fluctua-

tions are likely to be more extreme in areas with scattered

forest patches of small size, because only one locality

in Scotland was found to hold stable populations when

monitored from 1990 onwards (Rotheray & MacGowan

2000; Rotheray et al. 2008). The size of the forest patches

with stable populations from 1990 to 2008 was between

5 and 25 ha, and the overall mean dispersal distance was

measured to be 1 km, with a maximum of 5 km (Rother-

ay et al. 2014). A single forest with a size of more than

15 ha seems to be the lower limit for continuous survival.

The number of logs is crucial for survival, and although

one single fallen log can produce as many as one thou-

sand hatched adults, the number of usable trees each year

should be 34 at a minimum (Rotheray et al. 2008).

Similar population fluctuations have been observed for

both Brachyopa and Hammerschmidtia at Stenbrohult,

Djaknabygd, Sweden as well (Nilsson et al. 2007, 2012).

At this 17-ha site with 7 ha of forest, Hammerschmidtia

ferruginea and seven species of Brachyopa were found

in large numbers between 2007 and 2010 after a storm in

2005 created suitable larval habitat. This was especially

so for the species supposedly dependent upon wet decay

in fallen logs or in standing dead trees, such as Brachy-

opa obscura and Hammerschmidtia ferruginea, both of

which showed remarkably high numbers of individuals

present compared to other sites in Sweden.

Species depending on sap runs on living trees (e.g.,

Brachyopa bicolor, B. insensilis and B. minima) are most

likely to exhibit extreme fluctuations dependent upon

the availability of suitable old trees (Sjuts 2004; Pérez-

Bajfion et al. 2016). In Great Britain Brachyopa insensilis

suffered from loss of suitable larval habitat (slime fluxes

on Ulmus spp.) due to the Dutch Elm disease causing

most trees to die (Stubbs & Falk 1996). On the island of

Lesvos, B. minima was only found on one single sap run

on a Populus nigra L. between the years 2005 and 2011:

by 2013 the tree was almost completely healed (Pérez-

Bafion et al. 2016) with only a few larvae found by that

time.

Another group of Brachyopa species (e.g., B. dorsata,

B. testacea and B. vittata), which develop in trees with

tunnels of various saproxylic insects and in tree stumps

with wet decay, have a more long lived larval habitat

and seem less dependent on infrequent natural storms

(Lohr 1992; Krivosheina 2005). However, they are likely

to benefit from the regular felling of trees during forest

management, as is the case for Blera fallax (Linnaeus,

1758) (Rotheray & MacGowan 2015).

Some species, e.g., Brachyopa bicolor, have benefited

strongly from massive planting of fast-growing poplars

©ZFMK

316 Jeroen van Steenis et al.

along roads. Such trees are often pruned and inhabited by

goat moth caterpillars (Cossus cossus Linnaeus, 1758),

resulting in the frequent presence of sap runs and suitable

conditions for dispersion.

Besides storms and forest management, diseases caus-

ing damage to trees can be a major factor influencing

population fluctuations, as in the case of the oak dieback

causing acute oak decline, Dutch Elm disease and, more

recently, the bleeding canker of Horse-Chestnuts (Clous-

ton & Stansfield 1979; Fuhrer 1998; Thomas 2008; de

Keizer et al. 2012; Denman et al. 2014; Denman et al.

2018).

Habitat changes and threats

The species of the genera Brachyopa and Hammer-

schmidtia are highly dependent on a very specific larval

habitat, namely senescent trees with sap runs or recently

fallen tree trunks and stumps with a buildup of decaying

sap. The adults are often found near the larval habitat and

feed on various flowering herbs, shrubs and trees. The

population size will probably be restricted by the avail-

ability of suitable larval habitat, but perhaps the avail-

ability of a nearby adult food source may also play a role

in maintaining healthy populations (Fayt et al. 2006).

Several species are known to visit flowers frequently and

are likely be able to fly long distances.

Both the quality and quantity of resources, e.g., the

number of senescent trees and the surface of the forested

area, are probably the most important factor influencing

the population size of the species. The changes in Euro-

pean forest dynamics and de- or re-forestation have been

thoroughly investigated (Kaplan et al. 2009; Taff et al.

2009; Hughes et al. 2012). Forest cover has changed con-

siderably over time, leading to a net decrease of ancient

forest throughout Europe. Broadleaved floodplain forests,

swamp forests of different kinds and some Macaronesian

and Mediterranean forests are most severely threatened.

The central European alluvial and swamp forests have

been lost due to the regulation of rivers and changes in

hydrology, with possibly only 5% preserved in small

remnants (Hughes et al. 2012; Potapov et al. 2012; Birks

et al. 2016; European Commission 2016; Zanon et al.

2018). In some West-European countries, however, the

forested area is recovering and forest management has

changed in ways that favour Syrphidae (Reemer 2005;

Fuller et al. 2013).

In Europe, small areas with primaeval forest remain

in Fennoscandia, Poland, Portugal and the alpine coun-

tries, while in South-Eastern Europe larger areas still

have untouched forest (Sabatini et al. 2018; Jaroszewicz

et al. 2019). Many of these forest remnants are not pro-

tected, and even those that are protected are threatened

by logging activities and large infrastructure develop-

ment (Jaroszewicz et al. 2019; McGrath 2019). Mean-

while, in Eastern Europe there are reports of reforestation

Bonn zoological Bulletin 69 (2): 309-366

due to changing land use. People are moving from the

countryside to cities and the abandoned fields eventu-

ally become overgrown with trees. However, the inten-

sive management of the forest has also ceased in many

places, influencing the forest composition and possibly

in some cases causing a deterioration of adult (loss of

flowering plants due to abandoning fields) and even the

larval habitat (Alix-Garcia et al. 2016; Gutman & Rade-

lof 2017; Prokopova 2018). Commercial forests tend to

have a monoculture of tree species with few flowering

herbs and shrubs as potential adult food sources. In more

open agricultural landscapes, these flowering plants are

still available but solitary old trees are being removed in

an increasingly way. These two effects result in a spatial

mismatch between larval and adult habitat, likely to lead

to a decrease in population size and eventually also in the

number of populations (de Foresta et al. 2013; Scherber

et al. 2014; Felton et al. 2016; Liu et al. 2018).

Traditionally oak (Quercus sp.) has been widely man-

aged and used for a variety of purposes, such as bark for

tanning, wood for construction and mining, glass pro-

duction and forest pasture for livestock. In the absence

of traditional forestry practices, such as coppicing with

standards, most oak and oak-hornbeam forest undergoes

a natural succession to beech-dominated forest in which

ancient oak trees with sap runs disappear. This loss can

be exacerbated by modern forestry practices in which all

trees are harvested at the same time (Bobiec et al. 2018;

Molder et al. 2019). However, it has also been suggest-

ed that the natural succession to beech could possibly

be suppressed by diseases causing a (recent) decline in

beech populations (Jung 2009).

Other threats to the forest come from deposition of ni-

trogen, carbon dioxide and pesticides (Bleeker & Eris-

man 1998: Wamelink et al. 2009; van Dobben & de Vries

2017; Zou & Knops 2018) disturbing the natural balance

within the forest and causing multifaceted effects. The

effects have not been studied in detail for Syrphidae,

but it seems that nitrogen and carbon dioxide influence

floral growth rate in such a way that trees tend to age

faster (Erisman et al. 2014; Vogels et al. 2017; Wallis de

Vries & Bobbink 2017; EEA 2018). This could, tempo-

rarily, increase the larval habitat. A recent study, howev-

er, showed a negative impact on pollinators as a response

to increased deposition of nitrogen (Carvalheiro et al.

2020). Insecticides and fungicides on the other hand have

a strong negative influence on larval development and

adult fecundity in aphidophagous Syrphidae (Colignon

et al. 2003). It is highly likely these pesticides will also

have a negative influence on saproxylic species like in

the genera Brachyopa and Hammerschmidtia.

Finally, global climate change has a great impact on the

natural world and forest composition, which in turn will

have a great effect on its fauna (Ramsfield et al. 2016;

Morin et al. 2018; Pureswaran et al. 2018; Jactel et al.

2019; Jandel et al. 2019). These effects are even more

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

complex than those from nitrogen or pesticide deposi-

tion and are increasingly being investigated for Syrphi-

dae. These studies (Radenkovic¢ et al. 2017; Milici¢ et al.

2018; Milic et al. 2019) show that different species have

different responses, ranging from extensions in range,

to declines and even extinction. The dispersal capability

of each species and especially the dispersion of the hab-

itat of that species are factors not easily accounted for

and thus range extension is not only related to climate

change per se, but mostly to habitat change (Warren et al.

2001; Schweiger et al. 2012; Fourcade et al. 2017; Milic¢

et al. 2019). The most remarkable conclusion was that

this could lead to a decrease in lowland species richness

(Roth et al. 2014; Milici¢ et al. 2018; Mili¢ et al. 2019),

which in turn could lead to an increased decline of al-

ready rare species due to possible increased competition

from commoner species (Warren et al. 2001).

It is clear that the forests and woodlands of Europe are

threatened in many ways and that protective measures

are needed to ensure their future survival and the flora

and fauna dependent upon them. The EU (2016) list of

threatened habitats is a good example of what is need-

ed for this protection. Under each Syrphidae species the

threat category of the habitat, given in the codes of the

EUNIS (EUropean Nature Information System) habitat

classifications of Woodlands, is discussed based on the

information from this Red List.

Key to the adults of the European and circum Medi-

terranean species of Brachyopa and Hammerschmid-

tia

1 Vein M, perpendicular to vein R,,, and abdomen

straight, almost parallel-sided (Fig. 1E); all femora

enlarged, clearly thicker than 2.2 times the width

of tibiae; metatibia with short stout black setae

posteromedially (Fig. 16G); male with tuberculate

face (Figs 8E, 8F) ...Hammerschmidtia Schummel

— Vein M, ending oblique to vein R,,. and abdomen

conical, widest at posterior part of tergum II,

gradually and clearly narrowing towards posterior

tip of abdomen (see Figs 1A—C); femora only

slightly enlarged and not much wider than 1.5 times

the width of tibiae; metatibia with only normal short

pile; male and female without facial tubercle (see

FAS BADD eo ea scnlteas Ovetoed Brachyopa Meigen

Hammerschmidtia key

1 Arista plumose (Fig. 19E); katepisternum with

dorsal and ventral pile patch, in female dorsal patch

consisting of very few pili; postero-ventral part of

katepisternum with long, strong, black setae; apex of

profemur anteriorly with 1 strong, long yellow or

black setae (Fig. 16F); apex of mesofemur posteriorly

with 3 long and very strong, black setae, more than

Bonn zoological Bulletin 69 (2): 309-366

317

3 times longer than other black setae; large species

1G Fa 958 100 10 re eA RA Poe SCAR ht ae

saccae Hammerschmidtia ferruginea (Fallén, 1817)

— Arista short pilose and pile no longer than 3 times the

diameter of arista at base (Fig. 19F); katepisternum

with ventral pile patch and sometimes some white

pile on postero-dorsal corner; postero-ventral part

of katepisternum only with normal white pile; apex

of profemur anteriorly without strong, long yellow

or black setae; apex of mesofemur posteriorly with

3 rather long and strong, black setae, at most 2

times longer than other black setae; smaller species

lp STINT che, en) Ran Acer Hammerschmidtia ingrica

Stackelberg, 1952

Brachyopa key

Not all species were available and the key is adjust-

ed based on the studied material and the following lit-

erature: Kassebeer (2000a, b, 2001, 2002), Doczkal &

Dziock (2004), and Pérez-Bafion et al. (2016). All the

species from the circum Mediterranean region including

North Africa and Turkey are incorporated here as well

since they could occur in Europe too. The genitalia of

several species of Brachyopa have been illustrated by

Pellmann (1998), for each of these species this is indi-

cated by “*S?” indicating the * sign as remark and © as

genitalia Pellmann (1998). Most of the missing species

in Pellmann (1998) have been illustrated in the papers in

which the species were published for the first time (e.g.,

Thompson & Torp 1982; Mutin 1998; Kassebeer 2001;

Van Steenis & Van Steenis 2014).

1 Frons bulging, clearly visible above the eyes in

lateral view; face very wide; subscutellar pile fringe

well developed; proepimeron pilose; length 12.7 mm

....Brachyopa (Trichobrachyopa) tristis Kassebeer,

2001 (Only known from its type locality in Algeria)

— Frons flat, hardly visible above the eyes; face narrow;

subscutellar fringe at most poorly developed;

proepimeron at most with a few pili; smaller species

eR a 02 sr Re at 2 (Brachyopa sensu stricto)

2 Arista pilose to bare, length of pile at most 1,5 times

longer than width of basal part of arista (Figs 20

—21); scutum and pleura blueish-grey with black

ground colour (see Figs 2C—F) or brown-reddish

(ENS S ARE Ne gat aoe tn ee el 6

— Arista plumose, length of pile at least 2 times longer

than width of basal part of arista (Figs 19A—D);

scutum and pleura almost entirely brown-reddish

(S66: FV SS VA SDS oo arndi dls scan pa nbelvonmntnie enna Agsirnecomuarnch 3

3. Arista long plumose, pile more than 3 times longer

than width of basal part of arista (Fig. 19C);

katepisternum with dorsal and ventral pile patch;

©ZFMK

Jeroen van Steenis et al.

Fig. 3. Adult habitus, A-C, E, F dorsal view; D lateral view. A. Brachyopa atlantea, female, Granada, Spain. B. B. bicolor, male,

Engsbergen, Belgium. C. B. bimaculosa, male, Bolgenachtal, Germany. D. B. cinerea, male, Komsomolsk-na-Amur, Russian Far

East. E. B. grunewaldensis, male, Arkadia, Greece. F. B. insensilis, male, Diest, Belgium.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

face strongly produced antero-ventrally; posterior

anepisternum with 4—10 long strong black setae;

post-alar callus with long and strong black setae-like

pile mixed with light-yellow pile, black pile almost

twice as long as pile on scutum; length 8—11 mm ....

Fe ea aan Brachyopa vittata Zetterstedt, 1843 *°

Arista short plumose, pile at most 3 times longer

than width of basal part of arista (Figs 19A, 19B,

19D); katepisternum with ventral pile patch only;

face weakly to slightly produced antero-ventrally;

posterior anepisternum with at most 3—5 rather long,

black setae; post-alar callus with yellow or mixed

yellow and black pile, black pile only slightly longer

and stronger than pile on scutum

Face rather strongly produced antero-ventrally

(Fig. 8D); katepisternum and meron brown-reddish,

same colour as rest of pleura; sensory pit narrow,

longer than wide, tapering towards ventral margin;

arista rather long pilose, pile 2—3 times larger than

diameter of arista at base (Fig. 19D); length 6.0-

fEoe ilo Ramee Brachyopa zhelochovtsevi Mutin, 1998

Face only slightly produced antero-ventrally

(Figs 8A, 8B); in males at least ventral half of

katepisternum and meron dark-brown to black,

contrasting with brown-reddish rest of pleura;

sensory pit small and circular; arista long or short

DIlOSS: CRISS POAC OB) he i Ree eh ee 5

Abdomen with medial black vitta on terga I-IV

(Fig. 1B); face produced antero-ventrally (Fig. 8B);

arista longer pilose, pile almost 3 times longer

than width of arista basally (Fig. 19B); length 6.5—

8.0 mm......... Brachyopa testacea (Fallén, 1817) *°?

Abdomen without medial black vitta on terga III'V

(Fig. 1A); face weakly produced antero-ventrally

(Fig. 8A); arista rather short pilose, pile about 2

times longer than basal width of arista (Fig. 19A);

LET SCG =F WIT Shes sr ec oewreee oc aeanga nee sanwe 2 me

5 ee Brachyopa obscura Thompson & Torp, 1982

Arista virtually bare and = sensory pit on

basoflagellomere at most weakly developed small

dickround (Ess: 2UC 2 1)s tee 8m ae nestles en ewe. 1]

Arista pilose, pile at least as long as width of

arista and sensory pit on basoflagellomere clearly

developed, round or oval to large kidney shaped

(Figs 20A—B, 20D-F) ..0.....00cc ccc cccccctceeeenseeees 7

Scutum and pleura greyish, blue-grey pollinose with

weaker pollinose pattern (Figs 2C—D)

Scutum and pleura reddish-brown, brownish

pollinose with extensive shiny pattern (Figs 2A, 2B)

Posterior margin of scutellum with long black

bristles, 2-4 times longer than pile in the middle

Bonn zoological Bulletin 69 (2): 309-366

Aw,

319

of scutellum; scutellar disc extensively pollinose

medially and anteriorly; sensory pit as small as

diameter of arista at base (Fig. 20A); postero-dorsal

corner of anepisternum with some black setae; length

6-9 mm .... Brachyopa dorsata Zetterstedt, 1837 *°?

Posterior margin of scutellum without long black

bristles; scutellum only anterior margin narrowly

pollinose; sensory pit large, more than 2,5 diameter

of arista at base (Fig. 20B); anepisternum with only

Vee pile Meme 269-3 oaecop ES A icra vo pate etd

eh. ni cee Me Brachyopa panzeri Goffe, 1945 *°?

Postpronotum and post-alar callus blackish, same

colour as scutum and tergum II with at most a few

black pili on posterolateral margin (Fig. 2D); frons

in male more narrowly pollinose (Fig. 13C); length

6-8 mm .............. Brachyopa pilosa Collin, 1939 *°

Postpronotum and post-alar callus orange-brownish,

lighter than scutum and tergum IT extensively black

pilose postero-lateral margin (Figs 2E, 2F); frons in

male broadly pollinose (Figs 13D, 13E) .............. 10

Sensory pit on basoflagellomere small, rounded

(Fig. 20E); scutellar disc rather long pilose, pile

length about half as long as posterior scutellar setae;

length 7-8 mm ......... Brachyopa plena Collin, 1939

Sensory pit on basoflagellomere large, kidney-

shaped (Fig. 20F); scutellar disc rather short pilose,

pile length at most 1/3 as long as posterior scutellar

setae; length 6-8 mm

Brachyopa scutellaris Robineau-Desvoidy, 1844 *°?

Abdomen shiny black, antennae, face, scutellum

and male genitalia orange-yellow (Fig. 3D); length

6—8 mm. ............ Brachyopa cinerea Wahlberg, 1844

Abdomen reddish, often with dark-brown to black

markings, scutellum and genitalia greyish (Figs 3A—

I I Bay ate Me Palace wiley biel Ono 8 Re auld en 12

Wing with two small black maculae and postpronotum

dark-orange, lighter than rest of scutum (Fig. 2C);

PST CT FOO Se ain teeny AUNT oe Blaee ta vanat tte eA

Hine Brachyopa maculipennis Thompson, 1980 *°?

Wing hyaline and postpronotum dark brown, greyish

pollinose, same colour as rest of scutum (Figs 3A,

2) 8 yrge) bodod Cec! ie RRL Ome, ME a | Pe A 13

Notopleural sulcus at most weakly developed:

scutellum with a distinct transverse depression and

with distinct patch of microtrichia at base; protarsus

entirely black; metafemur enlarged; basoflagellomere

with distinct sensory pit (Fig. 21B); length 6-9 mm

Be a ieesttaste Brachyopa bicolor (Fallén, 1817) *°°

Notopleural sulcus well developed; scutellum

without transverse depression; protarsus mixed

black and yellow coloured; mesofemur less clearly

©ZFMK

Jeroen van Steenis et al.

Fig. 4. Adult habitus, dorsal view. A. Brachyopa cruriscutum, male paratype, Hakkari, Turkey. B. B. si/viae, male, Bringhausen,

Germany. C. B. minima, male, Lesvos, Greece. D. B. vernalis, male paratype, Crete, Greece. E. B. gquadrimaculosa, male, Samos,

Greece. F. B. guadrimaculosa, female, Samos, Greece.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

enlarged; basoflagellomere with at most a weak

Sensory. pil(Fies 2A Ww 21 C* ARs DAB yew 5. cn tists 14

Scutum (Fig. 4A) and vertical triangle (Fig. 15A)

extensively shiny, black with weak coverage of blue-

greyish microtrichia; length 6-7 mm

Brachyopa cruriscutum Van Steenis & Van Steenis,

2014

Scutum and vertical triangle almost entirely to

entirely covered with blue-greyish microtrichia

(Figs 4B-F, 14, 1SB-D) o.oo ceceteee 15

Scutum microtrichose except for 2 or more clear

black shiny maculae, bare of microtrichia (Figs 3A,

3C, 4B, 4D-F); postalar callus entirely microtrichose

or with medial part bare and shiny .............0....0... 17

Scutum entirely covered with microtrichia (Figs 3E,

3F); postalar callus microtrichose, with medial part

Barcrdiid:-Shity;: vss da/Bcentetes Mimar sekealysseo ax tie 16

Protarsus almost entirely dark-brown to black

coloured (Fig. 3F); ocellar triangle entirely greyish

pollinose (Fig. 14E); mouth-edge rather strongly

protruding (Fig. 10F); length 6.0-8.5 mm

Pge dia eaaiee. re Brachyopa insensilis Collin, 1939 *°?

Protarsus with tarsomeres bicoloured, basal part

yellow apical part dark-brownish (Fig. 3E); ocellar

triangle weakly pollinose, with shiny black pattern

(Fig. 14D); mouth-edge only weakly protruding

(Fie, TOE) length: 705825 Mice. .fc 5. seen thee

Sere Brachyopa grunewaldensis Kassebeer, 2000

aliereentirel y=Viel OW tee Mh ne B eke eek armas 19

Halter yellow except for capitulum which is partly

dark-greyish (see Fig. 4D) .......0 ccc ecceeeeeees 18

Face yellow with black triangular fascia between eyes

and antennae (vaguely visible in Fig. 11D); proleg

with tarsomere 1 yellow, tarsomeres 2—3 dark-brown

with broad yellow apical margin, and tarsomeres

4—S entirely dark-brown; posteroventral corner of

anterior anepisternum nearly entirely microtrichose,

at most a tiny bare macula; length 5.5—7.5 mm

Rete Brachyopa vernalis Van Steenis & Van Steenis,

2014

Face yellow, mouth edge narrowly black (Figs 11E,

11F); proleg with tarsomeres 1—5 entirely dark-brown;

posteroventral corner of anterior anepisternum with

shiny macula, bare of microtrichia; length 6-8 ........

densi Brachyopa quadrimaculosa Thompson, 1981

Postalar callus with medial part bare and shiny ... 21

Postalar callus entirely microtrichose .................. 20

Scutum with one pair of round bare shiny maculae

at the transverse suture (Fig. 3C); hypostomal bridge

Bonn zoological Bulletin 69 (2): 309-366

Ips

321

yellow (Fig. 10C); ocellar triangle densely covered

with microtrichia, not shiny (Fig. 14B); ventral

scutellar fringe absent; sterna entirely pollinose;

LTT CAG SATE Te ee ne Oe |

.... Brachyopa bimaculosa Doczkal & Dziock, 2004

Scutum with one pair of triangular bare shiny maculae

at the transverse suture (Fig. 4B); hypostomal bridge

blackish (Fig. 11B); at least centre of ocellar triangle

bare of microtrichia, shiny black; ventral scutellar

fringe present; more than half of the surface of sterna

3 and 4 non-pollinose; length 7-8 mm .....................

aioe te Se Brachyopa silviae Doczkal & Dziok, 2004

Wing with dark-brown macula on vein r-m; medial

end of transverse suture with brownish pollinose

macula; scutellum entirely orange-brown; length

6.5 mm ..... Brachyopa tabarkensis Kassebeer, 2002

Wing hyaline (Figs 3A, 4C); medial end of transverse

suture with non-pollinose, shiny black macula

(Fig. 3A) or grey pollinose like the other pollinosity

of the scutum; scutellum orange-brown with dark-

brOWIrAnte ROM Mareim Mises ccs, oak eee este ee. 22.

Medial end of transverse suture with non-pollinose,

shiny black macula (Fig. 3A); length 6-8 mm .........

sector Boe oe ae Brachyopa atlantea Kassebeer, 2000

Medial end of transverse suture pollinose; length

oe POMIMIT ens arte Moen trek Mactetcene Pian akt Ue a rere Se

Key to the known third-instar larvae of the European

species of Brachyopa and Hammerschmidtia

(Based on Krivosheina & Mamaev 1967; Rotheray 1996;

Rotheray & Gilbert 1999: Kassebeer 2000a; Krivosheina

2003; Krivosheina 2005, 2019; Pérez-Bafion et al. 2016)

Posterior respiratory process (prp) relatively short,

protruding only slightly beyond last pair of anal

lappets (Fig. 5C); anal lappets of nearly equal length;

dorsal part of abdomen evenly coated in setae, not

forming “transverse rows”; abdominal segments 2-6

with oblique furrow, separating the medial from the

COL al SCIs dl hae 50.5 eee Saket Nc Berets No aT

PRP relatively long, protruding strongly beyond last

pair of anal lappets (Fig. 5A); anal lappets of unequal

length, becoming increasingly shorter posteriorly;

dorsal part of abdomen with either transverse rows

of setae or coated in blotches; abdominal terga

2-6 without oblique furrow, the medial and dorsal

sensilla not separated from each other

Beek hada dh cheep: Poe be reed sansbbac Brachyopa Meigen

©ZFMK

322 Jeroen van Steenis et al.

omens ne

aE. og!

Fig. 5. Third instar larva and pupa. A. Brachyopa bicolor, larva, after Pérez-Bafion et al. 2016. B. Brachyopa insensilis, pupa, Brus-

sels, Belgium, photo B. Wakkie. C. Hammerschmidtia ingrica, larva, after Krivosheina 2003. Abbreviations: 7as = 7" abdominal

segment; ans = anal segment; Ip = lappets; prp = posterior respiratory process.

eens ote ey 8

‘te at"

bd rats

aL :

“ee = Fd

Fig. 6. Posterior respiratory process, after Krivosheina 2003. A. Hammerschmidtia ferruginea. B. Hammerschmidtia ingrica.

Key to the larvae of the European species of Hammer- pair ending close to the lateral margin of the prp

schmidtia (Fig. 6A) .... Hammerschmidtia ferruginea (Fallén)

— PRP with openings shorter, about 1/3 of the width

1 Posterior respiratory process (prp) with three pairs of the prp, lateral respiratory opening more straight,

of spiracular openings, length about half the width the medial pair further away from the lateral margin

of the prp, the lateral pairs strongly bent, the medial (Fig. 6B) ....Hammerschmidtia ingrica Stackelberg

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 323

Fig. 7. Posterior respiratory process, A after Kassebeer 2000c, B—D, F after Krivosheina 2005, E after Rotheray 1996. A. Brachy-

opa atlantea. B. Brachyopa bicolor. C. Brachyopa dorsata. D. Brachyopa pilosa. KE. Brachyopa scutellaris. ¥. Brachyopa vittata.

Key to the known larvae of the European species of

Brachyopa

Note: larvae of Brachyopa obscura, B._ testacea,

B. zhelochovtsevi, B. plena, B. bimaculosa, B. cinerea,

B. grunewaldensis, B. maculipennis, B. quadrimaculosa,

B. silviae, B. vernalis and B. tristis are not known.

Body with dense spinae; posterior end of abdomen

oval, usually darker than rest of the body .............. p)

Body at most with scattered spinae; posterior end

of abdomen conical, same colour as rest of the

ACOTINCTIA 9S. 0 De Bh tty tace deel ncdtbtainaeliy encecé oe. Beep ta atgethcac 4

Lateral papillae on posterior segments small,

tuberculate; posterior segments with several

Bonn zoological Bulletin 69 (2): 309-366

tubercles, without rows of spinae ...........0....000ece

dt acnrastanetha dem ata nt cornea tee Brachyopa vittata Zetterstedt

At least 3 or 4 lateral papillae on posterior segments

well developed, large; posterior segments with

several tubercles, with clear rows of spinae ........... 3

Lateral papillae on posterior segment unequally

sized, 5th and 6th as long as wide, 7th about 1.5

times longer than wide; 3rd and 4th pair of papillae

short, with short lateral appendages and 2 longer

apical appendages ............ Brachyopa panzeri Goffe

Lateral papillae 5—7 on posterior segments equally

sized, about 1.5 times longer than wide; all papillae

with long curved appendages, some longer than

18/30) 00 Es Wiens eae rae Mea Brachyopa dorsata Zetterstedt

©ZFMK

324

4 Abdomen without transverse rows of setae, some

isolated stump like setae may be present; body

coated in dark coloured blotches of various sizes ..5

— Abdomen with rows of setae; body with blotches

inconspicuous and pale, or entirely absent.............. 6

5 A large tubercle present between the first pair of

sensilla on tergum VII; setae of last three pairs of

anal lappets directed apically 0.0.0.0...

he sent Re B. minima Vuji¢ & Pérez-Bafion

— Area between the first pair of sensilla flat; setae of

last three pairs of anal lappets directed laterally and

AIC AVS. gr wie Aen eB eee B. insensilis Collin

6 Rows of setae on abdomen strictly aligned;

abdominal segments 1—6 with sensilla pairs 1 and 2

wath Z-laree and '2 Small "Setdee seek. cowed elected aes 7,

— Rows of setae on abdomen not aligned; sensilla pairs

1 and 2 usually with more than 2 large setae ......... 8

7 Spiracular opening on prp long and obliquely placed

(GcOTAg A by eee Rea tec eee ee B. bicolor (Fallén)

— S§Spiracular openings on prp short and medial pairs

almost horizontally placed (Fig. 3A) «0.00.00...

Dre eee does oo Ye A ean see a B. atlantea Kassebeer

8 PRP>1 mm long, as long as or longer than width of

body; ventral surface of prp apically smooth, without

[SIUC RAPER eenAL eae i, hd Ol aan eee B. pilosa Collin

— PRP<1mmlong, shorter than width of body; ventral

surface of prp apically with pits 0.00000.

ss berrtedl sea NB Rs oh B. scutellaris Robineau-Desvoidy

The European species of the genus Brachyopa Mei-

gen, 1822

Brachyopa atlantea Kassebeer, 2000

Brachyopa atlantea Kassebeer, 2000c: 142; 3 and

types in private collection of C.F. Kassebeer (present

condition or whereabouts unknown), not studied.

Figs 3A, 7A, LOA, 18A, 21A, 22

Distribution. Described from Morocco, based on five

adult specimens and several puparia and larvae collected

in Morocco. Only one European record from Spain (Van

Steenis & Van Steenis 2014) is known. It is classified as

an Ibero-Maghreb endemic species.

Biology. Adults, puparia and larvae have been found on

external sap runs on Populus spp. in the Atlas Mountains.

The species was collected at the same locality two years

in a row (Kassebeer 2000c). The record from Europe was

most likely from the South-Western part of the Sierra

Nevada in an area with Mediterranean evergreen Oak

(Quercus ilex Lour. and Q. pyrenaica Willd.) forest.

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

The flight period is not well known as only one adult

was collected, on the 24" of March, in the field. All oth-

er records are from larvae and puparia, many of which

were empty, between March 6" and April 16" (Kassebeer

2000c). The European specimen was collected on the 13"

of April (Van Steenis & Van Steenis 2014).

The species has been collected at altitudes of 550 and

1000 m a.s.l.

Population fluctuations. In Morocco the species was

collected at the same locality two years in a row. It 1s not

known if the species disappeared after that or that the lo-

cality has not been visited after these years. Based on the

larval habitat, external sap-runs, which tend to dry out in

the course of several years (Pérez-Bafion et al. 2016) it is

likely the population shows large fluctuations.

Remarks. The identification of the European specimen

is based on the characters given in Kassebeer (2000b).

The female specimen is listed in the database and, in the

distribution map, the African distribution of this species

is not shown.

Red List. Not present on any Red List. Due to its pre-

sumed relict occurrence in Europe and the small area of

occupancy in Morocco this species has little flexibility of

coping with threats. If major habitat threats are present,

its future survival will be under severe pressure, how-

ever, the presumed forest type G2.1 is listed as “Least

Concern” in the European Red List of habitats (European

Commission 2016).

Brachyopa bicolor (Fallén, 1817)

Rhingia bicolor Fallén, 1817: 33; @ lectotype and

9 paralectotype, in NHRS, not studied.

Figs 3B, 5A, 7B, 10B, 14A, 18B, 21B, 23, 38A

Distribution. A widespread European species occurring

from Southern Norway and Sweden to Spain and Greece

and from Wales into the European part of Russia and Ja-

pan.

Biology. Its main habitat consists of different deciduous

woodland and parkland forest types such as alluvial A/-

nus-Quercus-Fraxinus, thermophilous and xerophilous

Quercus-Ulmus-Fraxinus forests (Reemer et al. 2009;

Speight & Castella 2011; Ball & Morris 2014).

Larvae are known from a wide variety of trees, decid-

uous: Aesculus hippocastanum L., Fagus sylvatica L.,

Platanus spp., Populus alba L., Pyrus spp., Quercus spp.

and Ulmus spp. as well as coniferous Abies spp., in ac-

cumulations of sap under bark of live trees or tree trunks

and sap runs. Larvae are associated with sap runs caused

by larvae of the caterpillar of Cossus cossus (Lepidop-

tera) and larvae of the beetles Hylecoetus flabellicor-

nis (Schneider, 1791), Trypodendron lineatum (Olivier,

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 325

Fig. 8. Head male, lateral view. A. Brachyopa obscura, Olloy-s-Viroin Belgium. B. B. testacea, Elzetterbos, the Netherlands.

C. B. vittata, Eupen, Belgium. D. B. zhelochovtsevi, Aktru, Altay, Russia. E. Hammerschmidtia ferruginea, Borjomi NP, Georgia.

F. H. ingrica, Bychika, Russian Far East.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

326

1795) and T. signatum (Fabricius, 1792) on Abies spp.,

Populus tremula L., Quercus robur L. and Salix spp.

(Torp 1986; Rotheray 1991; Nielsen 2005; van Eck et al.

2016; Wolton & Luff 2016; Krivosheina 2019).

It is assumed that sap runs on Quercus spp. is the pre-

ferred larval habitat of this species (Ball & Morris 2014;

Krivosheina 2019). One population on a single Quercus

robur tree was monitored over a period of seven years

after which the tree was storm felled. This tree had an

age of 118 years and possibly over the last 20 years it

suffered from drought stress and loss of hardwood cre-

ating suitable larval habitat (Wolton & Luff 2016). The

larvae found in sap-runs on Aesculus hippocastanum and

Quercus robur are prone to be parasitized by Tetrastichus

brachyopae Graham, 1991 (Hymenoptera: Eulophidae),

with up to 18 wasps hatching from one single puparium

(Rotheray 1996; van Eck et al. 2016).

Adults were found visiting flowers of e.g. Acer spp.,

Crataegus laevigata (Poir.) DC., Prunus padus L.,

P. serotina Ehrh., P. spinosa L., Valeriana spp.(Stuke

1996; Bartsch et al. 2009; Nilsson et al. 2012), and Pla-

tanus spp. (database). They are more often found flying

around trees such as Acer pseudoplatanus L., Betula

pendula Roth, Castanea sativa Mill., Populus spp., Sa-

lix alba L. and the above mentioned trees with supposed

sap-runs where they can fly high into the trees (R6der

1990; Torp 1994; Nilson et al. 2007; Reemer et al. 2009;

Ricarte et al. 2014; van Steenis et al. 2019; Mielczarek

et al. 2019) as well as Carpinus betulus L., Fagus spp.

and Tilia spp. (database). The larvae overwinter, with pu-

parial formation occurring from February to May; the du-

ration of the puparial phase is 3.5 weeks (Dussaix 2013).

The overall flight period is from the beginning of April

until the end of July with extreme dates of the 6" of

March and the 15" of August (Fig. 38A). There is a range

shift and shortening in flight period from south to north,

so that the flight period in the boreal countries is from the

end of April until the end of June. Collected at altitudes

of 0O-1620 m a.s.1. (Maibach et al. 1992; database). This

species has many records from the 19th century in sever-

al countries, e.g., Austria, Germany and Sweden, but has

only rather recently been found in the Netherlands and

Norway, with the first records from 1966 and 1980 re-

spectively. The number of observations in different time

periods of 50 years differs greatly between and also with-

in countries. Over the periods before 1900, from 1900 to

1950, from 1950 to 2000 and after 2000, in Austria there

were respectively 6, 2, O and 6 records; in Serbia 0, 0, 6

and 7 records are known, while in Sweden 2, 2, 5 and 31

records are known.

Population fluctuations. This species is associated with

external sap runs on Quercus spp. and several other trees,

and as this type of microhabitat is known to fluctuate

over time this species would be expected to be adapted

to sucj fluctuations. In light of this, it is most likely this

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

species shows large fluctuations, especially within mar-

ginal habitats and possibly even within large areas with

suitable habitat. This conclusion can also be drawn from

the fluctuating number of records as given above.

Remarks. Several of the old records of this species could

actually belong to different species.

Red List. This species occurs on several regional Red

Lists and is categorized from “Least Concern” to “En-

dangered” (Bygebjerg 2004; Farkaé et al. 2005; Ssymank

et al. 2011; Ball & Morris 2014; Henriksen & Hilmo

2015; Artdatabanken 2019). Even within Germany large

differences between the “Bundeslander” exist where it

is classified from “Data Deficient” and “Vulnerable” to

“Endangered” (Pellmann et al. 1996; Stuke et al. 1998:

Doczkal et al. 2001; Dziock et al. 2001; von der Dunk

et al. 2003; Dziock et al. 2004). These differences depend

on several factors, such as being at the edge of its distri-

butional range and thus being at a higher threat level, the

availability of new records lowering the threat category

and possibly also the use of different criteria.

Brachyopa bimaculosa Doczkal & Dziock, 2004

Brachyopa bimaculosa Doczkal & Dziock, 2004: 45;

9 holotype in SMNM, not studied

Figs 3C, 10C, 14B, 18C, 21C, 24

Distribution. Single records are known from three local-

ities around the Alps (Germany and Slovenia) and one in

central Greece. A large population has been found on the

Peloponnesos, Greece (van Steenis & van Steenis 2014).

This species is regarded as a European endemic.

Biology. The species is recorded in sub-alpine forests

dominated by Abies alba Mill. and Fagus sylvatica along

small rivers in the shade of trees such as Acer spp., Al-

nus spp. and Salix spp. (Doczkal & Dziock 2004; van

Steenis et al. 2013) and on open flower-rich limestone

meadows within forests dominated by Abies cephalonica

Loudon and Pinus nigra J.F. Arnold. No larval records

are known and adults have only been found while vis-

iting flowers of several different plant species such as

Acer spp., Aegopodium podagraria L., Bupleurum cf. ro-

tundifolium, Prunus spp. and Salix aurita L. (Doczkal &

Dziock 2004; van Steenis et al. 2013; van Steenis & van

Steenis 2014).

In the Alpine population the specimens were collected

on the 3 and 19" of June at altitudes of 970 and 1050 m

a.s.l. respectively (Van Steenis & Van Steenis, 2014). In

the Northern part of the Schwarzwald one specimen was

collected on the 31st of March between 260 and 310 m

a.s.l. (Doczkal & Dziock, 2004). In Greece the species

was collected between 22" of April and the 28" of May

and had an altitudinal range of 980-1700 m a.s.l. (Van

Steenis & Van Steenis, 2014, database). The first record

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 327

Fig. 9. Head male, lateral view. A. Brachyopa dorsata, Rocherath, Belgium. B. B. panzeri, Oudergem, Belgium. C. B. maculipen-

nis, Fru8ka Gora, Serbia. D. B. pilosa, Drentsche Aa, the Netherlands. E. B. plena, Ioannina, Greece. F. B. scutellaris, Oudergem,

Belgium.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

328 Jeroen van Steenis et al.

dates back to 1990 and it has been seen regularly in the

21st century.

Population fluctuations. Only post 1990 records are

available from very widely separated localities. It is pos-

sible this species has been recorded before 1990 but was

not separated from similar species such as B. insensilis.

No evidence was found that this species has an extreme

fluctuation in populations or in population size.

Remarks. This species has a restricted range of occur-

rence and is only found in larger numbers on the Pelo-

ponnesos. The localities around the Alps are possibly

relict populations and may not be viable for maintaining

a steady population. The species distribution is severely

fragmented and the seemingly large population on the

Peloponnesos 1s not likely to colonize the Alpine locali-

ties. The larval habitats of the species of Brachyopa are

all connected with sap-runs or accumulations of sap un-

der bark and thus depending on natural forests with over-

mature trees. This habitat is under pressure in Greece and

especially on the Peloponnesos and on many Mediterra-

nean islands due to overgrazing and forest fires (WWF

2007; Caballero 2009; Kizos et al. 2013; Kalabokidis

et al. 2013).

The male specimens from the Alps differ in several

morphological characters from those collected on the

Peloponnesos in such a way that two species could be

involved. The male genitalia as well as molecular data do

not show large variation between these two putative spe-

cies and further study is needed to sort out the taxonomy

of the species.

Red List. This species only occurs on one regional Red

List. In Germany it is regarded as “Data Deficient” as only

one record was known (Ssymank et al. 2011). The habitat

where the species was found in the Alpine region could

be classified as G4 and possibly G4.1 both of which are

categorized as “Least Concern” (European Commission

2016); the Peloponnesian Black pine forests (G3.5) are

“Least Concern” too (European Commission 2016). On

Mt Taygetos, where part of the population was found, the

negative effect of forest fires clearly pose a great threat to

this type of forest (Sarris et al. 2014) despite its classifi-

cation, and thus to this Brachyopa species.

In the light of the possible split of this species, it is

advised to treat the Alpine populations separately from

the Greek populations.

Brachyopa cinerea Wahlberg, 1844

Brachyopa cinerea Wahlberg, 1844: 65; types in NHRS,

not studied.

Figs 3D, 10D, 14C, 18D, 21D, 24

Bonn zoological Bulletin 69 (2): 309-366

Distribution. Found in the boreal parts of Norway, Swe-

den and Finland, and eastwards into the boreal zone of

Siberia and Japan.

Biology. A relatively early flying subarctic species found

in Betula-Salix-Alnus and mountain Betula forests vis-

iting flowers of Ribes rubrum L. and Salix glauca L.

(Nielsen 1992, 1998; Mutin 1998; Bartsch et al. 2009)

and Anthriscus sylvestris L. (database). In the Russian

Far East it is more widespread and ‘with more specimens

found together visiting Prunus padus and Salix bebbiana

Sarg. (Mutin et al. 2016). No larval records are known.

The flight period of this species is from the beginning

of May until the middle of July (database). Collected at

altitudes between 25 and 1475 m a.s.]. (database). The

number of records from the 21 century equals that of

the period 1950-2000. The relatively many records from

the period from 1900-1950 indicate a possible decline in

populations.

Population fluctuations. This species has not been col-

lected at the same locality in different years and as only

single records are known from Europe it cannot be con-

cluded that this species shows extreme fluctuations.

Remarks. A rare and very local species, which almost al-

ways occurs as single specimens at collecting sites. Very

little is known about its biology. Due to the low numbers

found in Europe, it could be argued that the species is at

its western limit of occurrence, and hence vulnerable to

habitat changes.

Red List. This species occurs on the Red List of Fin-

land, Norway and Sweden, and it is classified from “Near

Threatened” to “Vulnerable” (Henriksen & Hilmo 2015;

Artdatabanken 2019; Hyvarinen et al. 2019). These cat-

egories seem to be based on weak assessments since,

given its distribution, there is likely to be considerable

undersampling of this species. More research is required

in order to make a well founded decision on its status

in Europe. The main habitat for this species, forest type

G1.5, is classified as “Vulnerable” (European Commis-

sion 2016).

Brachyopa dorsata Zetterstedt, 1837

Brachyopa dorsata Zetterstedt, 1837: 35; types in ZIL,

not studied

Brachyopa sibirica Violovitsh, 1982: 58, type in ZISP,

(syn by Mutin & Barkalov 1991), not studied.

Figs 2A, 7C, 9A, 13A, 17A, 20A, 25, 38B

Distribution. A widespread temperate and boreal (Fin-

land, Norway and Sweden) species with its western dis-

tributional boundary from the western part of the French

Pyrenees along the Alps and the Vosges into the eastern

parts of Belgium and the Netherlands, eastwards through

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 329

Fig. 10. Head, lateral view. A. Brachyopa atlantea, female, Granada, Spain. B. B. bicolor, male, Engsbergen, Belgium. C. B. bi-

maculosa, male, Arkadia, Greece. D. B. cinerea, male, Komsomolsk-na-Amur, Russian Far East. E. B. grunewaldensis, male,

Zagreb, Croatia. F. B. insensilis, male, Engsbergen, Belgium.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

330

Serbia and European Russia into the Russian Far East

and Japan. No records are known from the Mediterranean

area.

Biology. The adult habitat consists of lowland to subal-

pine mixed forest and of palsa- (see Zuidhoff & Kolstrup

2005; van Steenis & Zuidhoff 2013) and Pinus-Betu-

la-bogs in Northern Scandinavia (Hippa et al. 1981;

Nielsen 1992; Reemer et al. 2007; Bartsch et al. 2009).

Larvae are found in accumulations of sap under bark

of trunks and stumps of Betula spp., Populus tremula and

Ulmus spp. often together with other Diptera larvae: Lib-

notes ladogensis (Lackschewitz, 1940) and Gnophomyia

acheron Alexander, 1950 (both Limoniidae), Hammer-

schmidtia ingrica Stackelberg, 1952 (Syrphidae), Solva

semota Krivosheina, 1972 (Xylomyidae) and larvae of

the beetle Hylecoetus dermestoides (Linnaeus, 1760)

(Lymexylidae) (Mutin 1998; Krivosheina 2005, 2019).

Found on flowers of Acer platanoides L., Caltha palus-

tris L., Crataegus spp., Euphorbia cyparissias L., Malus

sylvestris (L.) Mill., Prunus domestica ssp. insititia, (L.)

Bonnier & Layens, P. padus, Rubus chamaemorus L., Sa-

lix spp. (Hippa et al. 1981; Nilsson et al. 2007; Reemer

et al. 2007; Bartsch et al. 2009; van Steenis 2011; Nilsson

et al. 2012; Speight 2020), and also Anthriscus sylvestris

(L.) Hoffm., Geranium sylvatica L., Prunus avium (L.)

L., Salix udensis Trautv. & C.A. Mey. and Spirea spp.

(database). Adults are more often found near trunks and

stumps of Betula spp. and damaged coniferous trees or at

sap runs on Fagus spp. and Quercus spp. (Roder 1990;

Mutin et al. 2016; Mielczarek et al. 2019). In the Rus-

sian Far East, it is found near damaged coniferous trees

together with several other Brachyopa species such as

B. panzeri, B. testacea and B. zhelochovtshevi (Mutin

et al. 2016). Larvae are found in tunnels created by Ly-

mexylidae larvae from Betula and Ulmus (Krivosheina,

2005) and under bark of Fagus, Picea, Populus and

Quercus trees (Mutin 1998; Dussaix, 2020).

This species has a main flight period (Fig. 38B) from

the beginning of April until the end of July, with ex-

treme dates of the 17" of March and the 5" of August.

The altitude at which this species 1s collected range from

0-—1503 m a.s.l. (database). It has been found in fluctuat-

ing numbers during different periods in Austria and Ger-

many, with relatively many records from before 1900. In

several other countries it has been recorded increasingly

many times since 1980 (Sweden), 2007 (Netherlands)

and 2009 (Belgium) indicating a possible extension of its

distributional range.

Population fluctuations. No clear trends are published,

but based on the larval habitat it seems likely this species

will not exhibit strong population fluctuations. The larval

habitat consists of trunks and stumps of a wide variety

of tree species which form a natural and rather constant

factor in European forests.

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

Remarks. This is a species that has been misidentified

in many instances. References before 1980 should be

treated with special care (cf. Reemer et al. 2007). The

discriminating characters were first fully understood by

Thompson (1980), but even since then, this species and

Brachyopa panzeri have been mixed up (e.g. Stuke et al.

2000; Mielczarek et al. 2019). It seems that B. dorsata is

the more northern and Alpine species, and has recently

spread to the Netherlands and Belgium (Bot & Van de

Meutter 2019).

Red List. This species is mentioned in four regional

Red Lists and was either not evaluated or assumed to

be of “Least Concern” (Bygebjerg 2004; Ssymank et al.

2011; Henriksen & Hilmo 2015; Artdatabanken 2019;

Hyvarinen et al. 2019).

Brachyopa grunewaldensis Kassebeer 2000

Brachyopa grunewaldensis Kassebeer 2000a: 8; < ho-

lotype in private collection of C.F. Kassebeer (present

condition or whereabouts unknown), not studied.

Figs 3E, 10E, 14D, 21E, 26

Distribution. A temperate and southern European spe-

cies with a very scattered distribution from Spain in the

west, to Belgium and the eastern part of Germany in the

north, and to Slovakia in the east. Also known from sev-

eral countries on the Balkan Peninsula. This species is

regarded as a European endemic.

Biology. Adults are found in Mediterranean acidophilus

Quercus-Fraxinus forests, mixed thermophilus Quer-

cus-Carpinus and Fagus-Picea forests, alluvial Quer-

cus-Populus and Carpinus forest and riparian Platanus

forest (Kassebeer 2000a; Doczkal & Dziock 2004; van

Steenis et al. 2019; Speight 2020).

The larva is unknown but adults were collected in

emergence traps on Fraxinus angustifolia Vahl, Quercus

Jfaginea Lam. and Q. pyrenaica, indicating the larvae live

in rot-holes in at least these tree species (Ricarte et al.

2013).

It visits flowers of Acer spp., Crataegus monogyna

Jacq., Pyrus spinosa Forssk., Sorbus torminalis (L.)

Crantz and Zamarix spp. (Marcos-Garcia 1987; van Stee-

nis & van Steenis 2014; Mielczarek et al. 2019; Speight

2020) and flies close to trees with sap runs including Aes-

culus hippocastanum, Carpinus betulus, Castanea sati-

va, and Quercus spp. (Doczkal & Dziock 2004; Mielcza-

rek et al. 2019; van Steenis et al. 2019; Speight 2020),

and Acer spp. (database).

This widely distributed but very scattered species has

been collected between the 8" of April and the 16" of

June, with extreme dates of the 28" of February and

the 16" of July. There are no indications of differences

between southern and northern populations (Kassebeer

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 3311

Fig. 11. Head, lateral view. A. Brachyopa cruriscutum, male paratype, Hakkari, Turkey. B. B. si/viae, male, Bringhausen, Germany.

C. B. minima, male, Lesvos, Greece. D. B. vernalis, male paratype, Crete, Greece. E. B. quadrimaculosa, male, Samos, Greece.

F. B. quadrimaculosa, female, Samos, Greece.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

332

2000; Doczkal & Dziock 2004, database). Collected at

altitudes of 50-1700 m a.s.l. (database). The first record

dates from 1969, and most of its records are from the

21st century. This is most likely due to the fact that more

entomologists know this species and thus tend to collect

it more often.

Population fluctuations. This species is only recently

described and it seems to be a very rare but widespread

species. The habitat preferences are not fully known and,

as such, it is impossible to know whether this species

might undergo population fluctuations.

Remarks. This is a recently described species confused

with B. bicolor in the past and possibly more widespread

than presently known. The habitat preferences are not

well known and it might be a very specialized species

with high demands on its habitat. This will make the spe-

cies more vulnerable to habitat changes and thus its fu-

ture survival more threatened.

Red List. It is only listed on the German Red List un-

der category “Endangered” (Ssymank et al. 2011). The

habitat of this species consists of a wide range of differ-

ent forest types and each of these types is classified in a

different threat category. The Mediterranean acidophilus

forest (G1.8) is “Vulnerable” while the thermophilous

forests (G1.7 and G4.6) are classified as “Least Concern’.

The alluvial forests (G1.1-—G1.3) are categorized from

“Near Threatened” to “Endangered” (European Commis-

sion 2016). The precise habitat preferences are not well

known and due to its very scattered distribution and low

population density nothing can be concluded about its

main habitat. The combination of low population density,

the very scattered occurrence and the supposed threat to

several of its habitats indicates that this species is at risk.

The database does not provide any evidence to estimate

any overall population trend or possibility of fluctuating

populations and so the exact threat category 1s unknown

as this can only be estimated by applying the IUCN Red

List criteria.

Brachyopa insensilis Collin, 1939

Brachyopa insensilis Collin, 1939: 105; ¢& lectotype,

4 33,3 2° paralectotypes in UMO, studied.

Figs 3F, 5B, 10F, 14E, 18E, 21F, 27, 38C

Distribution. A widespread European species from

southern Sweden south to Spain, Italy and Greece and

from Ireland through central Europe into the European

part of Russia. It is regarded as European endemic spe-

cies.

Biology. Found in a wide variety of wooded habitats

from tree-lined streets in cities to broadleaved and mixed

forests and often found flying around sap runs on trees

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

in these situations (e.g., Torp 1994; Bartsch et al. 2009;

Reemer et al. 2009).

Larvae are found in a wide variety of external sap runs

on broadleaved trees: Acer pseudoplatanus, Aesculus hip-

pocastanum, Alnus glutinosa (L.) Gaertn., Betula spp.,

Cornus mas L., Fagus spp., Populus spp., Quercus spp.

and Ulmus glabra Huds. and also on coniferous trees:

Abies alba and Pinus nigra (e.g. Trop 1979; Claussen

1985, Rotheray 1991, 1996; Schmid & Grossmann 1996;

Stubbs & Falk 1996; Bygebjerg 2001; van Steenis et al.

2001; Dussaix 2013; Ricarte et al. 2014; van Steenis &

van Steenis 2014; Krivosheina 2019).

The larvae are found together with larvae of the wood

gnat Mycetobia pallipes Meigen, 1818 (Diptera: Aniso-

podidae) (Krivosheina 2019). Large and small larvae are

present in the sap runs at the same time as the flight pe-

riod of the adults indicating a life cycle of more than one

year for the larvae (Rotheray 1996). Larvae, found on

Quercus robur, were infested by Tetrastichus brachyo-

pae (Hymenoptera: Eulophidae) (van Eck et al. 2016).

Infestation with parasitoid wasps, possibly 7? brachyo-

pae, was also observed in reared larvae collected from

Pinus nigra on the Peloponnesos, Greece (J. van Steenis,

pers. obs.).

Several species of flowers are visited by adults such

as Aegopodium podagraria, Anthriscus sylvestris, Malus

sylvestris, Photinia spp., Prunus padus and Sorbus spp.

(Torp 1973; Claussen 1985; de Buck 1990; Bygebjerg

2001; Bartsch et al. 2009; Speight 2020) and Cornus

mas, Prunus serotina, P. spinosa and Pyrus spp. (data-

base). In many instances adults were found flying around

sap runs on these larval trees and also on the following

trees: Platanus spp., Salix alba (Mielczarek et al. 2019;

van Steenis et al. 2019), and Acer campestre L., Betu-

la spp., Carpinus spp., Fraxinus excelsior L. and Popu-

lus spp. (database).

The main flight period (Fig. 38C) is from the beginning

of April until the end of July with extreme dates of the

27" of March and the 30" of August. These early and late

extremes were found in SE Europe only, but no clear dif-

ferences in main flight period between other southern or

northern populations has been found (database). Found

from sea level up to 1760 m a.s.1. (database). The records

of this species are not evenly distributed over different

time periods in different countries. In several countries

such as Denmark and Germany the species has many re-

cords from before 1920 and only few recent records. In

other countries, such as Great Britain, Hungary, the Neth-

erlands and Sweden, the first records date from around

1950 with most records from the 21* century, although

in Sweden there are large gaps of three to eight years in

which no records are available. The records from Austria,

Belgium and France are mostly from the 21“ century (da-

tabase).

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 333

Fig. 12. Head male, dorsal view. A. Brachyopa obscura, Fiby urskog, Sweden. B. B. testacea, Elzetterbos, the Netherlands.

C. B. vittata, Mangkarbo, Sweden. D. B. zhelochovtsevi, Aktru, Altay, Russia. E. Hammerschmidtia ferruginea, Riikanmaa, Fin-

land. F. H. ingrica, Bychika, Russian Far East.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

334

Population fluctuations. This species is very likely to

have a strongly fluctuating population size and density

since it is highly dependent upon external sap runs. These

sap runs tend to dry out over a short period of time causing

fluctuations in suitable larval habitat (e.g., Pérez-Bafion

et al. 2016). The occurrence tends to follow several tree

specific diseases (see more under remarks) causing large

fluctuations in the availability of larval habitat. Popula-

tion fluctuations could also be argued from the fluctuat-

ing records noted above.

Remarks. Previously in Great Britain this species was

believed to be dependent on sap runs on Ulmus spp.

(Robinson 1953; Stubbs & Falk 1996). This was proba-

bly influenced by Dutch Elm disease, a vasular wilt dis-

ease affecting leaves and causing death of the tree within

several years, creating many damaged trees. This first

“wave” of Dutch Elm disease entered England in 1927

and died out around 1940, and was a mild one causing

delayed growth and only slightly damaging trees. A more

aggressive form was first noticed around 1960 and by

1990 hardly any Elm trees were left (Clouston & Stans-

field 1979; Holmes & Heybrook. 1990; Harris 2017).

This century the available larval habitat has increased

(Sjuts 2004) again since 2001—2002 throughout Western

Europe due to the bleeding canker affecting Aesculus

hippocastanum trees (e.g. de Keijzer et al. 2012; Laue

2014; Pirc et al. 2018). This increase in larval habitat

will eventually decrease again due to recent discoveries

of methods to stop this disease (de Keijzer et al. 2012),

and there are also indications that trees naturally become

more and more resistant to this bacteria (Pankova et al.

2015) thus decreasing the number of affected trees and

hence suitable larval habitat.

Molecular data show two separate groups (J.H. Skev-

ington, pers. comm.), one from the Peloponnesos and the

other from the rest of Europe indicating some kind of

gene flow barrier and possible speciation.

Red List. This species occurs on several regional Red

Lists and is mostly classified as “Least Concern” (By-

gebjerg 2004; Ssymank et al. 2011; Ball & Morris 2014;

Artdatabanken 2019) but also “Vulnerable” (Farkaé et al.

2005).

Brachyopa maculipennis Thompson, 1980

Brachyopa maculipennis Thompson, 1980: 211; new

name for Musca arcuata Panzer, 1798: 15, prima-

ry homonym preoccupied by Linnaeus (1758); type

in private collection of Panzer (presumably lost), not

studied.

Brachyopa arcuata var. lateralis Oldenberg, 1916: 105;

type in DEI, (syn by Peck 1988), not studied.

Figs 2C, 9C, 14F, 20C, 28, 38D

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

Distribution. This is a temperate European species with

scattered records from Germany in the north to Italy in

the south, eastwards to Ukraine. This species is endemic

to Central Europe.

Biology. The main habitat consists of alluvial Salix-Til-

ia-Populus forest and to a lesser extent also humid broad-

leaved Fagus spp. forest with Populus alba, Quercus

petraea (Matt.) Liebl. and some scattered Pinus spp. (Ra-

denkovic et al. 2004; Mielczarek et al. 2019; van Steenis

et al. 2019).

Adults have been found near external sap-runs on Pop-

ulus alba and Salix alba (van Steenis et al. 2019) and

on Aesculus spp. (database), and it is assumed that these

sap-runs form the larval habitat of the species. In Poland

Oviposition was observed on senescent Populus alba.

The oviposition took place about 15 cm away from the

sap run (P. Trzcinski, pers. comm.). Adults visit flowers

of Crataegus spp., Malus spp., Prunus padus and Fran-

gula alnus Mill. (as Rhamnus frangula L.) (Mielczarek

et al. 2019; Speight 2020).

The species is collected between the 7" of April and

24" of June (Fig. 38D) at altitudes of 70-800 m a.s.1. The

Species seems to be collected relatively often in the 19"

and 21* century, but with a strong decline in the first half

of the 20" century. Many of the old records are from Cro-

atia, Germany, Italy and Slovakia (database).

Population fluctuations. As with other species de-

pendent on external sap-runs, such as B. insensilis and

B. minima, it is very likely that this species also shows

fluctuations in population size and densities over sever-

al decades. In Germany and Italy there are only old re-

cords and the species seems to be Critically Endangered

in these countries although Germany does seem to have

some post-2000 records (https://diptera.info/forum/view-

thread.php?thread_1d=6239) but the precise information

was not available for this paper. In Serbia and especially

the Czech Republic and Poland there are several recent

records (Mielczarek et al. 2019; van Steenis et al. 2019)

indicating there are still flourishing populations.

Remarks. The species is easy to identify and does not

seem to be misidentified (e.g. Sommaggio 2007). Its oc-

currence is unlikely to have been overlooked in Austria,

Germany or Italy in recent years, indicating that the evi-

dence of decline 1s a true decline.

Red List. This species is listed as “decreasing” in the

Balkan Peninsula (Vuji¢ et al. 2001), “Endangered” in

the Czech Republic (Farkaé et al. 2005) and “Critically

Endangered” in Germany (Ssymank et al. 2011). It is a

very rare species with few and scattered records through-

out its distributional range. Especially in the northern

and western edge of its distribution there are mostly old

records indicating a strong decline. The habitat from

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 335

Fig. 13. Head male, dorsal view. A. Brachyopa dorsata, Den Treek, the Netherlands. B. B. panzeri, Beek (Gld), the Netherlands.

C. B. pilosa, Hagadalen, Sweden. D. B. plena, male, Ioannina, Greece. E. B. scutellaris, Eure et Loire, France.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

336 Jeroen van Steenis et al.

Fig. 14. Head male, dorsal view. A. B. bicolor, Novi Sad, Serbia. B. B. bimaculosa, Bolchenachtall, Germany. C. B. cinerea, Kom-

somolsk-na-Amur, Russian Far East. D. B. grunewaldensis, Arkadia, Greece. E. B. insensilis, Novi Sad, Sebia. F. B. maculipennis,

Fruska Gora, Serbia.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

which this species is known can be categorized as ripar-

ian forests under EUNIS classification G1.1 to G1.3 and

G1.A. These forest classes are considered “Vulnerable”

to “Endangered” on the Red List of European habitats

(European Commission 2016). The area and quality of

the alluvial forests in Europe are rapidly declining (Se-

cerov & Nevenic 2004; Hughes et al. 2012) and, as such,

this habitat and Brachyopa maculipennis could be clas-

sified as “Endangered” or even “Critically Endangered”.

Brachyopa minima Vujié & Pérez-Bafién in Pérez-

Banion et al. 2016

Brachyopa minima Vujic & Pérez-Bafion in Pérez-Bafion

et al. 2016: 220; ¢ holotype, 6 ¢, 3 9° paratypes in

FSUNS and 9 paratype in MZH, studied.

Figs 4C, 11C, 15B, 22

Distribution. Only known from two localities in Greece,

on Lesvos Island from one single Populus nigra tree, and

northern Greece (Vujic et al. 2020). It is assumed to be a

European endemic.

Biology. Larvae were found from the 26" of April until

the 3 of May and on the 13™ and the 28" of September.

The adults and larvae were all found on a single Populus

nigra tree with a large wound creating a slime-flux with

different larval stages of several species present: Brach-

yopa aff pilosa and B. quadrimaculosa. The B. minima

larvae survived desiccation for two years, as found in the

similar B. insensilis. The tree was part of a small Popu-

Jus stand along a small stream, otherwise surrounded by

olive groves. The Populus nigra tree was the only one

in a large area with a visible sap run (Pérez-Bafion et al.

2016).

Collected between the 12" of April and the 3™ of May

at altitudes between 25 and 225 m a.s.I. (database).

Population fluctuations. It seems very likely this spe-

cies shows extreme fluctuations in population size as it

is highly dependent on naturally occurring external sap-

runs on old Populus trees. These sap-runs are known to

be scarce on the island of Lesbos and tend to heal over

after relatively short periods of time (Pérez-Bafion et al.

2016), mostly no longer than 10 years.

This species seems to be at risk due to overgrazing,

mainly by sheep (Kizos et al. 2013), and forest fires (Ka-

labokidis et al. 2013) which are major threats to the natu-

ral forests on Lesvos (Pérez-Bafion et al. 2016).

Remarks. This species belongs to a widespread species

complex with possibly more undescribed Mediterranean

species.

Red List. This species is not mentioned in any Red List

as it has only very recently been described. Based on its

Bonn zoological Bulletin 69 (2): 309-366

337

restricted occurrence and the possible threat to the habi-

tat, as outlined above, this species is severely threatened.

Brachyopa obscura Thompson & Torp, 1982

Brachyopa obscura Thompson & Torp, 1982: 441; ¢

holotype and 8 44 paratypes in ZISP, studied here.

Figs 1A, 8A, 12A, 16A, 19A, 29, 39A

Distribution. A widespread northern species with a dis-

junct distribution in other parts of central and south-east-

ern Europe. Its occurrence east of European Russia is

unknown but likely.

Biology. It is associated with mixed boreal forests with

Overmature trees such as Betula spp., Populus tremula

and P. nigra and other rich deciduous forests of the “A/-

nion glutinosae”’ and “Alno-Ulmion” classes (Nielsen

1992: Stuke 2001b; Bartsch et al. 2009; Wakkie et al.

2011; Pétremand et al. 2020). Unlike the very similar

adults of B. testacea, it is very rare in coniferous dom-

inated forests.

The larva is unknown but there is one record of an

adult which hatched from the bark of a Pyrus spp. (Niel-

sen 2005), indicating the larvae live in accumulations of

sap under bark or in internal sap-runs.

This species has been collected on flowering herbs and

bushes such as Acer platanoides, Aegopodium podagrar-

ia, Anthriscus sylvestris, Crataegus spp., Prunus padus,

P. serotina, P. spinosa, Ribes alpinum L. and Salix spp.

(van Steenis 1998; Stuke 2001b; Haarto & Kerpolla

2007; Nilsson et al. 2007; Bartsch et al. 2009; van Stee-

nis 2011; Nilsson et al. 2012; Mielczarek et al. 2019) and

Filipendula ulmaria (L.) Maxim (database).

The overall flight period is from May to July (Fig. 39A)

and the Northern populations have a flight period from

the 2™ of May to the 2™ of July, with an extreme datum of

15" of July. The other scattered records throughout east

and central Europe are from the 20" of April to the 21*

of June. The altitudinal range is from 40-1560 m a.s.l.

(database).

Population fluctuations. Population size increased

strongly a few years after a large storm during which

several Populus tremula trees were felled (Nilsson et al.

2007, 2012). Based on these observations in Sweden this

species shows an extreme fluctuating population size.

Remarks. The records in central and south-eastern Eu-

rope could be interpreted as isolated populations. The

extreme fluctuations in population size, in combination

with the lack of suitable habitat, could account for the

fact that B. obscura records are so scattered over this part

of Europe.

Red List. This species is reported in the Fennoscandian

Red Lists as of “Least Concern” to “Endangered” (Hen-

©ZFMK

338 Jeroen van Steenis et al.

Fig. 15. Head male, dorsal view. A. Brachyopa cruriscutum, male paratype, Hakkari, Turkey. B. B. minima, male, Lesvos, Greece.

C. B. vernalis, male paratype, Crete, Greece. D. B. guadrimaculosa, male, Samos, Greece.

riksen & Hilmo 2015; Artdatabanken 2019; Hyvarinen

et al. 2019). In Germany it is very rare and not put into

any Red List category (Ssymank et al. 2011). On the Bal-

kan Peninsula it occurs in a very small and restricted area

and is categorized as “Threatened” (Vujic et al., 2001).

It has a wide occurrence in Fennoscandia and a very

disjunct distribution in other parts of Europe and regional

differences in threat category are to be expected.

Brachyopa panzeri Goffe, 1945

Brachyopa panzeri Goffe, 1945: 278; new name for con-

ica Panzer, 1798: 20, junior primary homonym, ac-

cording to Thompson (1980) preoccupied by Gmelin

(1790); type in private collection of Panzer or NWM

(presumably lost), not studied.

Figs 2B, 9B, 13B, 17B, 20B, 30, 39B

Bonn zoological Bulletin 69 (2): 309-366

Distribution. Widespread in northern and temperate Eu-

rope from southern Sweden to Spain and from central

France eastwards through European Russia and into Si-

beria.

Biology. Mostly found in humid Fagus forests but also in

alluvial Populus forest, mixed Carpinus-Quercus-Pinus

forests and even in coniferous forests (Torp 1994; Laut-

erbach 2001, 2002; Reemer et al. 2009).

The larva has been found in a sap run on Fagus syl-

vatica (Stuke & Schulz 2001) and maybe also in a Pi-

cea spp. stump in the larval tunnels of Hy/ecoetus flabel-

licornis (Coleoptera: Lymexylidae) (Krivosheina 2005).

The larvae are found together with larvae of Gnophomy-

ia lugubris (Zetterstedt, 1838) (Diptera: Limoniidae),

Mycetobia pallipes (Diptera: Anisopodidae) and with

Brachyopa vittata (Krivosheina 2019). The records from

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 339

Fig. 16. Brachyopa and Hammerschmidtia species, A-E head female, dorsal view, F male profemur, dorsal view, G male metatibia,

dorsal view. A. Brachyopa obscura, Fiby urskog, Sweden. B. B. testacea, Hautes-Fagnes, Belgium. C. B. vittata, Bolgenachtall,

Germany. D. B. zhelochovtsevi, Aktru, Altay, Russian. E. Hammerschmidtia ferruginea, Fiby urskog, Sweden. F. H. ferruginea,

Rukanmaa, Finland. G. H. ferruginea, Fiby urskog, Sweden.

Bonn zoological Bulletin 69 (2): 309-366 ©ZFMK

340

Krivosheina (2005, 2019) are based on larvae only and it

is not clear if these larvae really belong to B. panzeri as

no adults were reared from these larvae (Speight 2020).

Adults have been seen visiting flowers of Acer pseudo-

platanus, Anthriscus sylvestris, Crataegus spp., Prunus

padus, P. spinosa, Salix spp., Sambucus racemosa L.,

(Barkemeyer, 1986; Roder 1990; Nilsson et al. 2007;

Reemer et al. 2009) as well as on Prunus cerasus L. (da-

tabase). Adults are more often found hovering around

stumps or at sap runs on Acer spp., Aesculus hippocast-

anum, Castanea sativa, Fagus spp., Pinus spp. and U/-

mus spp. (Torp 1994; Lauterbach 2002; Bartsch et al.

2009; Merz 2009; Ricarte et al. 2014; Mutin et al. 2016).

The flight period (Fig. 39B) is from the beginning of

April until the beginning of July, with the latest date of

the 20" of July. It was collected at altitudes of 0-1375 m

a.s.l. (Barkemeyer 1986; Maibach et al. 1992; Ricarte

et al. 2014; database). In several countries pre 1900 re-

cords are available, but several other countries only have

records after 1950 to 1970. In most countries there are no

records over several consecutive years and the number of

records seems to have increased during the 21“ century.

Population fluctuations. This species seems to fluctuate

over the years in the Netherlands and has not been found

in consecutive years at the same locality. The larval habi-

tat consists of trunks and stumps of a wide variety of tree

species which form a natural and rather constant factor in

European forests. Thus, based on the larval habitat, it is

predicted that this species will not show strong popula-

tion fluctuations.

Remarks. In Western Europe this species is supposedly

connected with Fagus forests which have provided con-

sistent forest cover for centuries and perhaps explains

why this species does not seem to fluctuate much in the

number of populations (database).

Red List. In most countries treated as “Near Threatened”

or “Vulnerable”, except in Germany where it is of “Least

Concern”. However, in several Bundes-Lander it is clas-

sified as “Vulnerable” (Pellmann et al. 1996; Doczkal

et al. 2001; Bygebjerg 2004; Dziock et al. 2004; Farkaé

et al. 2005; Ssymank et al. 2011; Artdatabanken 2019).

The habitat of this species is listed as “Least Concern”

in the European Red List of habitats (European Commis-

sion 2016).

Brachyopa pilosa Collin, 1939

Brachyopa pilosa Collin, 1939: 107; 3 43 syntypes

NHM and 2 3 syntype in UMO, studied here.

Figs 2D, 7D, 9D, 13C, 17C, 20D, 31, 39C

Distribution. A widespread European species, from

northern Norway south to the Pyrenees and Italy, and

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

from Ireland to European Russia in the east; also known

from Georgia.

Biology. Found either in rich deciduous forests (prefer-

ably Fagus), alluvial forests with Populus nigra, humid

Picea spp. forest or even city parks (R6der 1990; Reemer

et al. 2009; Ball & Morris 2014).

Larvae are found under bark of Betula spp., Fagus

sylvatica, Populus tremula, Quercus spp., and Picea

abies trunks (McLean & Stubbs 1990; Rotheray 1991;

Kassebeer 1993; Torp 1994; Lauterbach 2001; Kri-

vosheina 2005; Mielczarek et al. 2019). The species is

often accompanied by larvae of the following species:

Gnophomyia viridipennis (Gimmerthal, 1847) (Diptera:

Limoniidae), Mycetobia pallipes, Sylvicola cinctus (Fa-

bricius,1787) (Diptera: Anisopodidae) and species of

the family Sesiidae (Lepidoptera) and Ceratopogonidae

(Diptera). In contrast to the known larvae of other Brach-

yopa species, there are no xylophagous larvae associated

with Brachyopa pilosa (Krivosheina 2019). Larvae are

known to be parasitized by Tetrastichus spp. (Hymenop-

tera: Eulophidae) (Kassebeer 1993). Several larvae found

in a sap run on Quercus robur were infested by Tetrasti-

chus brachyopae (van Eck et al. 2016).

Flowers visited include Acer campestre, A. pla-

tanoides, A. pseudoplatanus, Aegopodium podagrica,

Allium ursinum L. Anemone nemorosa L., Anthriscus

sylvestris, Cardamine pratensis L., Crataegus spp., Her-

acleum pubescens (Hoffm.) M. Bieb., Malus sylvestris,

Photinia spp., Prunus cerasifera Ehrh., P. padus, P. spi-

nosa, Pyrus communis L., Salix spp. and Viburnum opu-

lus L. (Torp 1973, 1994; Claussen 1985; de Buck 1990,

Kormann 1993; Bygebjerg 2001; Nilsson et al. 2007; van

Steenis 2016; Speight 2020) as well as Astilbe spp., Cor-

nus spp., Prunus avium, P. serotina, Rhamnus cathartica

L., Spirea spp. and Tilia spp. (database). Adults are found

on the tree trunks of Betula spp. Populus tremula, Quer-

cus rubra or the logs of coniferous trees such as Lar-

ix spp. and Picea spp. They are seldomly seen around

trees with sap runs (Reemer et al. 2009).

The main flight period (Fig. 39C) is from the end of

March until the end of July, with extreme dates of the 21“

of February and the 24" of July, from an altitudinal range

from sea level up to 1582 m a.s.]. (Maibach et al. 1992;

database). In many countries this species seems to have

stable populations because the number of records does

not show great fluctuations over the years. In Denmark

the species seems to have declined although the map is

somewhat misleading as many records are from 1990 to

1999 and thus rather recent.

Population fluctuations. This species can be found

during many consecutive years at the same locality and

it seems unlikely that this species shows strong popula-

tion fluctuations. The larval habitat consists of trunks and

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 341

Fig. 17. Head female, dorsal view. A. Brachyopa dorsata, Fiby urskog, Sweden. B. B. panzeri, Tumnin, Russian Far East. C. B. pi-

losa, Fiby urskog, Sweden. D. B. plena, Zagreb, Croatia. E. B. scutellaris, Gronsveld, the Netherlands.

342 Jeroen van Steenis et al.

stumps of a wide variety of tree species which form a

natural and rather constant factor in European forests.

Remarks. A widespread species possibly with good

dispersal capacities because it has spread throughout

the Netherlands within 50 years (Reemer et al. 2009),

and colonized a small city park in an otherwise agricul-

ture-dominated environment within some years of the

felling of Populus spp. (J. and W. van Steenis, pers. obs.).

Red List. Mentioned in several European Red Lists and

mainly categorized as “Least Concern” except in the

Czech Republic (“Vulnerable”) and Norway (“Endan-

gered”) (Bygebjerg 2004; Farkaé et al. 2005; Ssymank

et al. 2011; Ball & Morris 2014; Henriksen & Hilmo

2015; Artdatabanken 2019; Hyvarinen et al. 2019). In

Norway the species reaches its northern distributional

limit which makes it vulnerable. The habitat is listed as

“Least Concern”.

The wide distribution in many parts of Europe is the

reason why this species is classified as “Least Concern”

on other Red Lists.

Brachyopa plena Collin, 1939

Brachyopa plena Collin, 1939: 108; 2 ¢& syntypes in

UMO, studied.

Figs 2E, 9E, 13D, 17D, 20E, 32

Distribution. A South-East European species with re-

cords from Germany (Kassebeer, 2000; Lauterbach

2002, see below) and further known from Austria, Cze-

chia, Hungary, Slovakia and the Balkan Peninsula. This

is a European endemic.

Biology. Found in Mediterranean oak forests and decidu-

ous alluvial gallery forest within Pinus brutia Ten. forest

(Speight 2020).

Flowers visited include Acer campestre, Cratae-

gus spp., Pyrus spinosa, Salix spp. and Sorbus torminalis

(Speight 2020). Adults are also seen flying around the

base of Quercus spp. (database).

This species has been collected between the 4" of April

and the 28" of May with an latest date of the 19" of July.

The altitudinal range of this species is 113-1000 m a.s.l.

(database). The number of records in the 21" century

equals those of the 20" century and based on the strong

increase in observers in the 21‘ century possibly indicat-

ing a slow decline.

Population fluctuations. There are no data supporting a

strong fluctuation in population size or density. The larval

habitat of this species is not well known. This makes it

impossible to estimate if this species experiences strong

population fluctuations.

Bonn zoological Bulletin 69 (2): 309-366

Remarks. Almost identical with B. scutellaris that re-

places this species in the western parts of Europe. The

study of the type material of B. plena (J. van Steenis,

pers. obs.) confirms the identity of the south-east Euro-

pean specimens as belonging to this species. The differ-

ences between these specimens and those of the west-

ern counterpart B. scutellaris are very small and further

study is needed to see whether these species should be

synonymized or kept as two separate species. Molecu-

lar data show a small difference between B. plena and

B. scutellaris indicating there is some genetic variation

between these species (J.H. Skevington, pers. comm. ).

Red List. It is listed in Germany (Ssymank et al. 2011)

as “data deficient” possibly based on the record by Laut-

erbach (2002). This record is very doubtful as no records

of B. scutellata, much more common in Germany, were

mentioned in Lauterbach’s paper; therefore this record is

not taken into account in the present paper.

Brachyopa quadrimaculosa Thompson in Kaplan &

Thompson, 1981

Brachyopa quadrimaculosa Thompson in Kaplan &

Thompson, 1981: 208, 3 holotype and allotype in

ECTAU and 11 64, 2 99, in CNC, ECTAU, NHM

and USNM, not studied.

Figs 4E, 4F, 11E, 11F, 15C, 18F, 33

Fig. 18. (suggested).

Distribution. Originally described from Israel with a few

additional records from North Greece, the islands of Les-

vos and Samos, and a first record for Cyprus (database).

Biology. Adults were found in alluvial and Platanus ori-

entalis L. forest within Mediterranean Quercus frainet-

to Ten. and QO. pubescens forest, alluvial Populus forest

within Pinus brutia forest and Mediterranean maquis.

Found visiting flowers of Pyrus spinosa and Smyrnium

olusatrum L. (Kaplan & Thompson 1981; Speight 2020).

Also collected in alluvial A/nus orientalis forest within

mixed Platanus orientalis and Pinus brutia forest (col-

lection A. van Eck).

The flight period is from the 31%' of March until the 1“

of May and the species 1s collected at altitudes of 25—

550 m a.s.l. (database). The first European record dates

back to 1988 and all other records are from 2007 or later.

Population fluctuations. Too little is known about the

habitat preferences of this species to say anything about

the population fluctuations.

Remarks. This species is most likely to have the same

habitat preferences as Brachyopa minima, and is likely to

be affected by the same habitat threats on Greek islands,

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 343

Fig. 18. Head female, dorsal view. A. Brachyopa atlantea, female, Granada, Spain. B. B. bicolor, Maarn, the Netherlands. C. B. bi-

maculosa, Arkadia, Greece. D. B. cinerea, Komsomolsk-na-Amur, Russian Far East. E. B. insensilis, Novi Sad, Serbia. F. B. quad-

rimaculosa, Samos, Greece.

344

namely sheep grazing (Kizos et al. 2013) and forest fires

(Kalabokidis et al. 2013).

Red List. Not mentioned on any Red List. See further

comment under Brachyopa minima.

Brachyopa scutellaris Robineau-Desvoidy, 1844

Brachyopa_ scutellaris Robineau-Desvoidy, 1844: 39;

9 holotype in MNHNP, not studied.

Figs 2F, 7E, 9F, 13E, 17E, 20F, 32, 39D

Distribution. A west European species, regarded as Eu-

ropean endemic.

Biology. Found in humid deciduous forests, most nota-

bly alluvial and swamp forests.

Larvae are found in sap runs on Acer pseudoplatanus,

Alnus spp., Fraxinus excelsior, Populus tremula, Taxus

baccata L. and Ulmus glabra (Seguy 1961; Rotheray

1996; Pellmann 1998; Reemer et al. 2009). In a sap run

on Fraxinus excelsior in Bretagne, France, the larvae of

this species were accompanied by larvae of Ferdinandea

cuprea Scopoli and Volucella inflata Fabricius (Diptera:

Syrphidae) (J. van Steenis, pers. obs.).

Visiting flowers of Aegopodium podagraria, Anth-

riscus sylvestris, Cardamine pratensis, Cornus spp.

Crataegus spp., Heracleum Malus spp., Photinia spp.,

Prunus padus, Rubus fruticosus, Sorbus spp. and Vibur-

num opulus (de Buck 1990; Bygebjerg 2001; Reemer

et al. 2009; Mielczarek et al. 2019), as well as Acer spp.,

Chaerophyllum temulum L., Genista spp. Heracle-

um spp., Prunus serotina, Salix spp. and Smyrnium olu-

satrum (database). Adults are more often found on tree

trunks of Fagus spp., Quercus spp., and sap runs on Betu-

la spp. or hovering around Castanea sativa (Ricarte et al.

2014), and around Acer spp. (database).

The flight period (Fig. 39D) is from the beginning

of April until end of July with the extreme dates of the

20" of March and the 20" of August (database). A spe-

cies found at altitudes of 0-1250 m a.s.]. (Maibach et al.

1992; Ricarte et al. 2014; database). In France and Great

Britain this species shows large fluctuations in the num-

ber of records each year, while in several other countries

the number of records seems to be more stable.

Population fluctuations. This species can be found in

the same locality several years in a row, sometimes even

in forests seemingly without suitable external sap-runs.

The larvae are mostly associated with external sap-runs,

a habitat showing extreme fluctuations over time. This

makes this species will very likely also show strong pop-

ulation fluctuations.

Remarks. In Poland, large variation in the size and shape

of the sensory pit was found (Mielczarek et al. 2019),

which could indicate that Brachyopa plena is just a vari-

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

ant of B. scutellaris and not a separate species. There are

also other scenarios possible and the area where these

specimens were found would be the place to visit for fur-

ther study, to see if there is overlap in the distinguishing

characteristics between these two species.

Red List. Mentioned on several regional Red Lists un-

der “Near Threatened”, “Vulnerable” and even “Endan-

gered” (Bygebyerg 2004; Farkaé et al. 2005; Ssymank

et al. 2011). In Sweden it is listed as “not applicable”

(Artdatabanken 2019) but the reason why is not very

clear; its real threat category for Sweden could be “Near

Threatened” to “Endangered”. The corresponding habitat

types in the EU list are, with the threat category in brack-

ets G1.2a (LC), G1.2b (EN) and G1.4 (VU) (European

Commission 2016).

Brachyopa silviae Doczkal & Dziock, 2004

Brachyopa silviae Doczkal & Dziock, 2004: 50; ¢ ho-

lotype in NMM, 2 3’, 3 2 paratypes in private col-

lections, not studied.

Figs 4B, 11B, 33

Distribution. Known from its type locality in Germany

and recently reported from France and Serbia (Doczkal &

Dziock 2004; Speight et al. 2013; van Steenis et al. 2019)

and also known from Austria. It is an endemic species

for Europe.

Biology. Found near sap runs on a trunk of a Carpinus

betulus tree and in ancient Quercus-Fagus forests (van

Steenis et al. 2019) as well as in thermophilous Quercus

and mesophilous Fagus forests (Doczkal & Dziock 2004;

Speight et al. 2013).

Visiting flowers of Crataegus spp. and Pyrus spinosa

(Speight 2020) and Acer pseudoplatanus (database).

The species has been collected between the 3" of April

and the 12" of May at an altitude of 75-925 m a.s.l. (da-

tabase). All 10 records are post 1999.

Population fluctuations. This species has only observed

regularly in Germany. The records for Austria, France

and Serbia were mostly single specimens on a single oc-

casion. The German records are too few to see any sign

of extreme fluctuations.

Remarks. This is a very rare species found in three wide-

ly separated locations. Only the German population can

be considered to be stable. The localities are so far apart

that there will not be any exchange between them and, as

such, the distribution is extremely fragmented.

Red List. Only mentioned on the German Red List, clas-

sified as “data deficient” (Ssymank et al. 2011).

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 345

Brachyopa testacea (Fallén, 1817)

Rhingia testacea Fallén, 1817: 34, types in NHRS, not

studied.

Figs 1B, 8B, 12B, 16B, 19B, 34, 40A

Distribution. A widespread boreo-alpine species found

from northern Norway south to the Pyrenees and Bulgar-

ia and from Belgium east through the Alps and the Baltic

states into European Russia. It is also widely distributed

in the boreal zone of the Palaearctic region up to the Rus-

sian Far East.

Biology. The adult habitat consists of pine forests or

pine-dominated mixed forests (Lohr 1992; Bartsch et al.

2009; Reemer et al. 2009). Adults are also observed in

broadleaved dominated mixed forests, often while visit-

ing flowers (database).

Larvae and puparia have been found under bark of Pi-

cea stumps in association with tunnels of Lymexylidae

larvae (Coleoptera) (Nielsen 1992; Lohr 2002; Bartsch

et al. 2009; Krivosheina 2019).

Adults are often found near damaged coniferous trees,

especially stumps of Picea abies (Lohr 1992; Mutin

et al. 2016) but also further away from coniferous trees

in mixed forests foraging on flowering herbs and shrubs

of Prunus padus and Sorbus aucuparia L. (J. van Stee-

nis, pers. obs.). Other flowers visited are Acer pseudo-

platanus, Aegopodium podagraria, Anemone nemorosa,

Angelica archangelica L., Angelica sylvestris L., Anth-

riscus sylvestris, Cardaminopsis arenosa (L.) Lawalrée,

Crataegus spp., Malus spp., Meum spp., Myrrhis odorata

(L.) Scop. Prunus avium (as Cerasus avium in part of da-

tabase), P. spinosa, Ribes alpinum, Salix spp., Saxifraga

granulata L., Scorzonera humilis L., Stellaria holostea

L., Taraxacum spp., Valeriana spp. and Viburnum opulus

(Torp 1994; Bartsch et al. 2009; Speight 2020) and Pimp-

inella major (L.) Huds. and Spirea spp. (database).

The main flight period (Fig. 40A) is from the middle

of April until the end of July with extreme dates of the

2™ of April and 21 of August. Found at altitudes from

sea level up tol880 m a.s.l. (database). In all countries

recorded extensively during the 21“ century, but no re-

cent records from Denmark (since 1999) and Switzerland

(since 1996).

Population fluctuations. This species is dependent on

pine forests. The larvae are dependent on rather freshly

cut stumps. This habitat is heavily managed and will pro-

duce a constant amount of suitable larval habitat due to

regular tree felling. It seems this species does not show

strong population fluctuations.

Red List. This species is listed as “Least Concern” on

all regional Red Lists and also its habitat does not seem

to be threatened (Bygebjerg 2004; Ssymank et al. 2011;

Bonn zoological Bulletin 69 (2): 309-366

Henriksen & Hilmo 2015; European Commission 2016;

Artdatabanken 2019; Hyvarinen et al. 2019).

Brachyopa vernalis Van Steenis & Van Steenis, 2014

Brachyopa vernalis Van Steenis & Van Steenis, 2014:

13; 3 holotype in NBC, 7 @' paratypes in NBC,

PJSA, PMRL, PWSB, FSUNS, ZMUC, all types stud-

ied

Figs 4D, 11D, 15D, 22

Distribution. Only known from three localities on Crete

(Greece), based on material collected in 1997, 2008 (van

Steenis & van Steenis 2014) and 2012, and hence a Eu-

ropean endemic.

Biology. Found visiting flowers of Crataegus spp. and

Prunus spp. in Mediterranean deciduous forests and in a

forested part of a deep ravine.

This species was collected on the 28" of March, the

8" of April and the 8" of May at an altitudinal range of

350-900 m a.s.]. (database).

Population fluctuations. Nothing can be concluded

based on the data we have here, but as seen for some

other Mediterranean species of Brachyopa, its larvae are

most likely living in sap runs and as such, prone to show

large population fluctuations.

Remarks. Crete has been visited by renowned dipteran

collectors (Jan Lucas, Claus Claussen, etc.) in the past

and only recently nine specimens of this species have

been collected, indicating it should be classified as an

extremely rare species. It has been recorded at three lo-

calities in Crete, all in forested habitats. Only one local-

ity is within a protected area. As in many Mediterranean

areas this habitat is under threat due to overgrazing and

forest fires. This in combination with the restricted range

of occurrence makes this species very vulnerable to ex-

tinction.

Red List. Not mentioned on any Red List but, due to its

restricted distribution and the threats to its habitat, a can-

didate to be listed in one of the IUCN threat categories.

Brachyopa vittata Zetterstedt, 1843

Brachyopa vittata Zetterstedt, 1843: 687; type in ZIL,

not studied.

Figs 1C, 7F, 8C, 12C, 16C, 19C, 35, 40B

Distribution. A widespread species found from northern

Sweden south to the Pyrenees and northern Greece and

from the Netherlands east into European Russia and fur-

ther to the Russian Far East and Japan.

©ZFMK

346 Jeroen van Steenis et al.

Fig. 19. Basoflagellomere male, medio-lateral view. A. Brachyopa obscura, Hagadalen, Sweden. B. B. testacea, Bolgenachtall,

Germany. C. B. vittata, Belchen, Germany. D. B. zhelochovtsevi, Aktru, Altay, Russia. E. Hammerschmidtia ferruginea, Hinteral-

feld, France. F. H. ingrica, Tuva, Russia.

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 347

Fig. 20. Basoflagellomere male, medio-lateral view. A. Brachyopa dorsata, Belchen, Germany. B. B. panzeri, Dresden, Germany.

C. B. maculipennis, Novi Sad, Serbia. D. B. pilosa, Valkenburg, the Netherlands. E. B. plena, Kalavryta, Greece. F. B. scutellaris,

Cadier en Keer, the Netherlands.

348

Biology. Adult habitat is old growth Picea and Pinus for-

ests but also found in mixed swamp forest (Lohr 1992;

Bartsch et al. 2009; Reemer et al. 2009).

Larvae live in Picea spp. and Larix spp. stumps as

well as in standing trunks and stumps of Abies spp. with

tunnels of Hylecoetus flabellicornis (Coleoptera: Lymex-

ylidae), 7rypodendron lineatum, Ips sexdentatus (Bo-

erner, 1767) (Coleoptera: Curculionidae) and Zabrachia

minutissima (Zetterstedt, 1838) (Diptera: Stratiomyidae).

They are also accompanied by the saprophagous larvae of

Sylvicola cinctus (Diptera: Anisopodidae) (Krivosheina

2005, 2019).

Flowers visited include Aegopodium podagraria, An-

thriscus sylvestris, Caltha palustris, Crataegus laevi-

gata, Crataegus monogyna, Prunus avium, P. padus,

Salix spp., Sambucus nigra L., S. racemosa, Sorbus

aucuparia and Viburnum spp. (Séguy 1961; Barkemey-

er 1986; de Buck 1990; Réder 1990; Nielsen 1992; van

Steenis 2011; Speight 2020), as well as A/liaria petiolata,

Pimpinella major, Spirea spp. and Valeriana officinalis

L. (database). Adults are found on tree stumps and trunks

of a wide range of coniferous trees.

The flight period (Fig. 40B) is from the middle of April

until the middle of August (database). The altitudinal

range of this species is 10-2270 m as.l. (Barkemeyer

1986; Maibach et al. 1992; database). This species has

been recorded during all time periods in France and Ger-

many and in many other countries regularly after its first

discovery. Only in Sweden it was recorded around 1900

with the next records from 1999, 2009 and 2013, indicat-

ing strong population fluctuations.

Population fluctuations. As indicated for Brachyopa

testacea, this 1s a species dependent upon pine forests

and, as larvae, on rather freshly cut stumps. This habitat

is heavily managed and will produce a constant amount

of suitable larval habitat due to regular tree felling. It

seems this species does not show strong population fluc-

tuations in its central distributional range.

Remarks. This is a species of coniferous forests often

found near trunks and stumps defending a territory.

Red List. This species is listed from “Least Concern” to

“Endangered” on the regional Red Lists (Ssymank et al.

2011; Henriksen & Hilmo 2015; Artdatabanken 2019).

In Finland it is listed as “data deficient” (Hyvarinen et al.

2019). These categories contrast strongly with one an-

other because there are only very few records for each

country and most of these are from recent times, except

in Sweden where there are some very old records and

some recent ones too, indicating a possible absence of

many years. The species seems to be at its northern limits

in these countries, so the threat category seems to depend

on how important you judge the local populations. The

species should either be categorized as “data deficient”

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

in all three countries or in one of the threat categories

“Vulnerable” to “Critically Endangered”. In Central Eu-

rope the species seems to be widespread with stable pop-

ulations, and its habitat is classified as “Least Concern”

(European Commission 2016), so there seem to be signif-

icant differences in the threat category between Fennos-

candia and the rest of Europe.

Brachyopa zhelochovtsevi Mutin, 1998

Brachyopa zhelochovtsevi Mutin, 1998: 4; 3 holotype in

ZMSU, studied.

Figs 1D, 8D, 12D, 16D, 19D, 33

Distribution. Only known in Europe from two Finnish

records for this otherwise East-Palaearctic species, with

some records from the Altai.

Biology. Found in an ancient forest with fallen logs of

Abies spp., Betula spp. and Populus tremula (Haarto &

Kerppola 2009). Adults found near damaged coniferous

trees (Mutin et al. 2016). Flowers visited Ledum palustre

L. (Speight 2020).

Collected on the 24" and the 29" of June and on the 13"

of July. One old record from 1911 and the other two from

2008 (database).

Population fluctuations. Nothing can be concluded con-

cerning fluctuations in population size.

Remarks. This species is very similar to both B. obscu-

ra and B. testacea, and is easily overlooked in the field,

although B. obscura tends to be the more light-coloured

and B. zhelochovtsevi the most dark-coloured species.

The distribution of this species could be wider than cur-

rently known. As very little is known about its adult and

larval habitat no conclusions can be drawn on possible

threats.

Red List. For Finland the species is categorised as “data

deficient” (Hyvarinen et al. 2019).

The European species of the genus Hammerschmidtia

Hammerschmidtia ferruginea (Fallén, 1817)

Rhingia ferruginea Fallén, 1817: 34; type in NHRS, not

studied.

Hammerschmidtia vittata Schummel, 1834: 740; type in

NMW, (syn by Peck 1988), not studied.

Figs 1E, 6A, 8E, 12E, 16E—-G, 19E, 36, 40C

Distribution. A widespread species found from northern

Norway south to the Pyrenees and from central France

east through the Alps, the Balkan Peninsula and Poland

to European Russia. Also known from Scotland and

Georgia and further east to the Russian Far East. The re-

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 349

Fig. 21. Basoflagellomere, medio-lateral view A. Brachyopa atlantea, female, Granada, Spain. B. B. bicolor, male, Arkadia, Greece.

C. B. bimaculosa, male, Arkadia, Greece. D. B. cinerea, female, Komsomolsk-na-Amur, Russian Far East. E. B. grunewaldensis,

male, Arkadia, Greece. F. B. insensilis, male, Novi Sad, Serbia.

350

cord in NW France (Séguy, 1961) is a strange record and

needs verification.

Biology. The adult habitat consists of pine and birch tai-

ga in Scandinavia and Scotland, and mixed alpine forests

up to 1200 m a.s.l. with large stands of Populus tremu-

la (Nielsen 1992; Rotheray & McGowan 2000; Bartsch

et al. 2009).

The larval habitat has been intensively studied in Scot-

land and consists of sap accumulations in fallen logs of

Populus tremula or sap runs on the same tree (Rotheray

1991; Rotheray & McGowan 2000; Rotheray et al. 2009,

2014). The larvae live in recently fallen logs with sappy

decay, which lasts for 2 to 3 years. From one such log al-

most 1000 specimens were collected in emergency traps

(Rotheray et al. 2014). In other parts of the world lar-

vae have been found in similar conditions (Krivosheina

2003).

Adults visit flowers of Aegopodium podagraria, An-

gelica sylvestris, Anthriscus sylvestris, Conopodium

majus (Gouan) Loret, Crataegus spp., Prunus padus,

Pyrus communis, Ranunculus acris L., Rosa spp., Rubus

fruticosus, Salix spp., Sorbus aucuparia, Syringa spp.

and Valeriana spp. (de Buck 1990; Roder 1990; Nielsen

1992: Stubbs & Falk 1996; Nilsson et al. 2007; Ball &

Morris 2014; Speight 2020), as well as Chaerophyllum

temulum, Filipendula ulmaria, Heracleum sphondylium

L., Malus sylvestris, Prunus laurocerasus L., Sambucus

nigra, Spirea spp. and Viburnum opulus (database).

Its flight period (Fig. 40C) is from the end of April un-

til the beginning of August with extreme dates of the 2™

of April and the 19" of August. This species is found at

altitudes of 20-1925 m a.s.l. (database).

Population fluctuations. Extreme fluctuations were

found in the Scottish Highlands (Rotheray et al. 2008;

Ball & Morris 2014) and based on its larval biology it

is highly likely this species shows fluctuations over its

entire distributional range.

Remarks.This is a very characteristic species which

is unlikely to be overlooked in the field due to its size

and preference for flowering Apiaceae as an adult food

source.

Red List. In northern countries this species is listed as

“Least Concern” (Henriksen & Hilmo 2015; Artdata-

banken 2019; Hyvarinen et al. 2019), while it is “En-

dangered” to “Critically Endangered” in Germany and

Great Britain (Ssymank et al. 2011; Ball & Morris 2014).

In Scotland conservation actions are in place (Rotheray

et al. 2008), and these actions will probably have a posi-

tive impact on its occurrence in Great Britain.

In other parts of Europe, the specific habitat of the

species falls within EUNIS category G1.4 or possibly

G1.9 and G4.8 of which G1.4 is considered “Vulnerable”

Bonn zoological Bulletin 69 (2): 309-366

Jeroen van Steenis et al.

(European Commission 2016). In light of this, Hammer-

schmidtia ferruginea could also be threatened and would

possibly classify under the same category although the

species is not considered threatened in the Balkan Penin-

sula (Vuji¢ et al. 2001).

Hammerschmidtia ingrica Stackelberg, 1952

Hammerschmidtia ingrica Stackelberg, 1952: 37; 3 ho-

lotype and 2 33’, 1 2 paratypes in ZISP, studied.

Figs 1F, 5C, 6B, 8F, 12F, 19F, 37

Distribution. Described from European Russia with

many records from the surroundings of St Petersburg and

Moscow (Stackelberg 1952, database), and with a range

extending eastwards to the Russian Far East. (Mutin et al.

2016). Recently recorded in Finland.

Biology. Adults are found in mixed boreal forests with

overmature deciduous trees (Krivosheina 2003; Mutin

et al. 2016).

The larvae are found in sap accumulations under the

bark of Juglans mandshurica Maxim., Populus tremula

and Ulmus spp. (Krivosheina 2003). Adults were col-

lected in an emergence trap on a Populus tremula trunk

(Polevoi et al. 2018).

In the Russian Far East, it was found visiting flowers of

Cornus alba (as Swida alba in Mutin et al. 2016).

The flight period in Europe is from the 25" of April

until the 30" of June at altitudes between 25 and 400 m

a.s.1. (database).

Population fluctuations. The larvae seem to have simi-

lar habitat preferences to Hammerschmidtia ferruginea.

It is likely that both Hammerschmidtia species show sim-

ilar population fluctuations.

Remarks. The Finnish island where this species was

found is a former Soviet Military base, and several plant

species have been found there which originate from Rus-

sia. It is hypothesized that H. ingrica is an introduced

species now maintaining a population on the island

(Kerppola 2011). However, this is questionable because

it occurs in the nearby European part of Russia, and sim-

ilar habitats occur on both sides of the border.

It seems that the Nearctic Hammerschmidtia rufa Wil-

liston, 1882 and eastern-Palaearctic specimens of H. in-

grica have identical DNA, and thus it is proposed that

H. ingrica should be a junior synonym of the older name

H. rufa (Skevington et al. 2019). This synonymy was

proposed in a field guide without mentioning the descrip-

tive authority, nor has the type of H. ingrica been studied,

and so this change is not applied here.

Red List. As a supposed non-native species to Finland, it

is listed as “not applicable” in the Red List of this country

(Hyvarinen et al. 2019).

©ZFMK

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 351

DISCUSSION

This discussion will focus on the results given under

each species and summarize this in a generalized way.

For ease of reading no references are given here. The dis-

cussion focuses on the current knowledge and especially

gaps which need to be investigated more thoroughly to

understand more fully the possible effects of changing

habitat on population dynamics of the species.

The species of the genera Brachyopa and Hammer-

schmidtia are highly specialized in their larval habitat. In

general, different kinds of tree sap accumulations form

the larval habitat. This can be external sap runs caused

by physical damage or other larvae, or internal accumu-

lations of sap under bark of stumps or fallen logs. Most

of these habitats are within living trees, but accumula-

tions of sap on recently felled trees are also used by some

species. This habitat is restricted by a variety of factors

and its availability could fluctuate greatly over time. The

amount of suitable larval habitat increases after storms,

fires, infectious outbreaks causing damage to trees or

felling activity by forestry. These fluctuations are mostly

random and hard to predict, causing large fluctuations in

population densities. Moreover, each year, the sap-runs

tend to dry out in autumn, making survival of the larvae

a challenging process. Consequently, adaptations have

evolved in response to these uncertainties. The extensive

longevity and high desiccation tolerance in the larval

stage help to overcome the yearly fluctuations. The lon-

gevity can also span the period of tree recovery when

little larval habitat is present. Other strategies involve the

adults, and probably include high mobility and the ability

to identify the larval habitat at great distances, especially

in the females.

Within the genus Brachyopa there are basically two

larval biotopes, and species tend to have a preference

for either one. Some species are generalists, with larvae

occurring in a wide range of deciduous and coniferous

trees, whilst others tend to occur only in coniferous trees.

The latter are mostly larvae living in sap accumulations

under bark of stumps and trunks, perhaps a more stable

habitat than sap runs on living trees. The sap-run-depen-

dent species tend to have a wider range of host trees, in-

cluding deciduous and coniferous trees, although it seems

they do have some preference, for instance, Quercus spp.

being preferred by Brachyopa bicolor and Aesculus hip-

pocastanum by B. insensilis.

Most knowledge about larval habitat is gathered from

field observations rather than through extensive ecolog-

ical or behavioural studies. Only Hammerschmidtia fer-

ruginea, a true specialist on accumulations of sap under

bark of recently felled Populus tremula logs, has been

investigated in great detail. These studies suggested the

minimal forest area needed for survival as being at least

15 ha with large stands of Populus tremula in all life stag-

es. All other species need to be investigated as thorough-

Bonn zoological Bulletin 69 (2): 309-366

ly as H. ferruginea in order to establish what tree species

are needed, how large the forest area should be and how

near other forests need to be in order to ensure their fu-

ture survival.

It seems that no species of Brachyopa or Hammer-

schmidtia have become extinct in Europe yet. Two very

rare species in Europe (Brachyopa atlantea and B. zhelo-

chovtsevi) could be relicts with a larger range in the past.

Two other species (Brachyopa testacea and B. vittata)

could have benefitted from the increasing area of conif-

erous plantations in Western Europe. Most of the species

dependent upon deciduous forests have extended their

ranges northwards since the last ice age, along with the

reforestation of Europe in this period. The species thus

seem to be able to adapt to a changing environment, but

we do not know how quickly they are able to do this and

whether they will be able to continue to thrive as habitat

changes accelerate due to global warming and other hu-

man impacts.

In this paper we have compiled all information avail-

able to us and have provided data on distribution, habitat,

ecology, habitat threats and possible population fluctua-

tions. This could serve as a basis for compiling a nation-

wide or regional Red List and, most of all, to encourage

biologists to do more research on the ecology of the spe-

cies of these two genera.

Acknowledgements. We wish to thank the following per-

sons for loan of material and for other valuable help: Gunilla

Stahls (Helsinki, Finland), Cyrille Dussaix (France), Xavier

Lair (France), Jonathan Voise (France), Jean-David Chapelin

Viscardi (Laboratoire d’Eco-Entomologie, France), Damien

Hemeray (Réserve Naturelle de Saint Mesmin, France), Dieter

Doczkal (Gaggenau, Germany), Una FitzPatrick (National Bio-

diversity Data Centre, Waterford, Ireland), Pasquale Ciliberti

(Leiden, the Netherlands), Ruud van der Weele (Zoelmond, the

Netherlands), Snorre Henriksen (Artsdatabanken, Norway), To-

ril L. Moen (Artsdatabanken, Norway), Tore Nielsen (Sandnes,

Norway), Arjen Leendertse (Oslo, Norway), Lennart Carlsson

(Artportalen Sweden), Artur Larsson (The Species Fact Sys-

tem, Sweden), Sophia Ratcliffe (NBN Trust, UK) and Francis

Gilbert (UK). The first author wishes to thank Olga Ovchin-

nikova and Nikolai Paramonov (St Petersburg, Russia) and An-

drey Ozerov, Marina Krivosheina and Anatoly Shatalkin (Mos-

cow, Russia) for their generosity while visiting their museums.

The Dutch Uyttenboogaart-Eliasen foundation under numbers

SUB.2014.12.16, SUB.2017.12.05 and SUB.2019.05.21 and

the Royal Entomological Society Outreach fund 2018, provid-

ed funding for the visit of the the NHM, London; UMO, Ox-

ford; the ZMSU, Moscow and the ZISP, Saint Petersburg, are

acknowledged by the first author. The work of Jiri Hadrava was

supported by GAUK 1030119/2019.

©ZFMK

352 Jeroen van Steenis et al.

Fig. 22. Distribution map. Brachyopa atlantea, dot, B. minima, Fig. 23. Distribution map. Brachyopa bicolor (white <1950,

star; B. vernalis, square. (white <1950, white with black point white with black point >1950 <2000, black >2000, + datum un-

>1950 <2000, black >2000). known).

Fig. 24. Distribution map. Brachyopa bimaculosa, dot; B. ci- Fig. 25. Distribution map. Brachyopa dorsata. (white <1950,

nerea, square. (white <1950, white with black point >1950 white with black point >1950 <2000, black >2000, ? = uncertain

<2000, black >2000, ? = uncertain record). record, + datum unknown).

Fig. 26. Distribution map. Brachyopa grunewaldensis. (white Fig. 27. Distribution map. Brachyopa insensilis. (white <1950,

<1950, white with black point >1950 <2000, black >2000, ? = white with black point >1950 <2000, black >2000, + datum un-

uncertain record). known).

Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia 353

Fig. 28. Distribution map. Brachyopa maculipennis. (white Fig. 29. Distribution map. Brachyopa obscura. (white <1950,

<1950, white with black point >1950 <2000, black >2000, + da- white with black point >1950 <2000, black >2000).

tum unknown).

Fig. 30. Distribution map. Brachyopa panzeri. (white <1950, Fig. 31. Distribution map. Brachyopa pilosa. (white <1950,

white with black point >1950 <2000, black >2000, ? = uncertain white with black point >1950 <2000, black >2000, ? = uncertain

record, + datum unknown). record, + datum unknown).

Fig. 32. Distribution map. B. scutellaris, black dot; Brachyo- Fig. 33. Distribution map. Brachyopa quadrimaculosa, dot;

pa plena, red square. (white <1950, white with black/red point B. silviae, stars; B. zhelochovtsevi, square. (white <1950, white

>1950 <2000, black/red >2000, + datum unknown). with black point >1950 <2000, black >2000).

354 Jeroen van Steenis et al.

Fig. 34. Distribution map. Brachyopa testacea. (white <1950,

white with black point >1950 <2000, black >2000, + datum un-

known).

7m See

Fig. 35. Distribution map. Brachyopa vittata. (white <1950,

white with black point >1950 <2000, black >2000, + datum un-

known).

San oe

Fig. 36. Distribution map. Hammerschmidtia ferruginea. (white Fig. 37. Distribution map. Hammerschmidtia ingrica. (white

<1950, white with black point >1950 <2000, black >2000, ? = <1950, white with black point >1950 <2000, black >2000).

uncertain record, + datum unknown).

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Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia

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Faunistical overview of the European species of the genera Brachyopa and Hammerschmidtia Ses

Brachyopa testacea

200

Number of records

ee Se Be

NY BH WOON f£ DD

oo coc 8G GO 8

10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40

Week numbers

B Brachyopa vittata

Number of records

10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40

Week numbers

C Hammerschmidtia ferruginea

120

Number of records

10 12 14 16 18 20 22 24 26 28 #30 32 34 #36 38 40

Week numbers

Fig. 40. Flight diagram. Moving average over 2 weeks with number of records of males and females in each calendar week. Week

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ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:339EA3FD-EAE0-4BFE-9C6B-8E305C6FDD26

The snakes of Chad: results of a field survey and

annotated country-wide checklist

Jean-Francois Trape’’, Israé] Demba Kodindo’, Ali Sougoudi Djiddi’, Joseph Mad-Toingué! &

Clément Hinzoumbé Kerah*

' Institut de Recherche pour le Développement (IRD), Laboratoire de Paludologie et de Zoologie Médicale, UMR MIVEGEC,

B.P. 1386, Dakar, Sénégal

?Programme National de Lutte contre le Paludisme (PNLP), Ministére de la Santé Publique, de |’Action Sociale et de la Solidar-

ité Nationale, N’Djaména, Chad

>Programme National de Lutte contre le Paludisme (PNLP), Ministére de la Santé Publique, de |’Action Sociale et de la Solidar-

ité Nationale, N’Djaména, Chad

+Hopital Général de Référence Nationale, B.P. 130, N’Djaména, Chad

° Programme National de Lutte contre le Paludisme (PNLP), Ministére de la Santé Publique, de 1’Action Sociale et de la Solidar-

ité Nationale, N’Djaména, Chad

* Corresponding author: Email: jean-francois.trape@ird fr

'urn:Isid:zoobank.org:author:F8BE8015-09CF-420B-98D3-D255D142AA2D

2urn:Isid:zoobank.org:author:CC89C696-9A2A-49C7-82EE-C75858F756FO

3urn:Isid:zoobank.org:author:B175CEB7-969A-47E 1 -8B38-1El1OBF7ECD25

4urn:Isid:zoobank. org: author:352EF698-1235-4167-992C-1 BE3D53E1FDD

Surn:|sid:zoobank.org:author:2E7B97F6-E450-4C32-A 8AE-E347D0DCSA61

Abstract. From 2015 to 2017 we sampled snakes in most regions of the Republic of Chad, Central Africa. A total of 1,512

snakes belonging to 66 species were collected. Based on a full account of this collection, supplemented with additional

museum specimens and reliable literature reports, we present an annotated checklist of the 80 snake species currently

known from Chad, including 28 species that we added to the snake fauna of this country: Letheobia weidholzi, Myrio-

Pholis occipitalis, Tricheilostoma sundewalli, Crotaphopeltis hippocrepis, Dasypeltis sahelensis, Natriciteres olivacea,

Platyceps florulentus, Spalerosophis diadema cliffordi, Telescopus tripolitanus, Atractaspis dahomeyensis, Atractaspis

micropholis, Aparallactus lunulatus nigrocollaris, Boaedon longilineatus, Boaedon paralineatus, Boaedon perisilves-

tris, Boaedon subflavus, Lycophidion aff. capense, Malpolon moilensis, Micrelaps vaillanti, Prosymna ambigua, Prosym-

na greigerti, Psammophis afroccidentalis, Psammophis elegans, Psammophis mossambicus, Psammophis sudanensis,

Rhamphiophis rostratus, Naja savannula and Echis romani. Collecting localities for all specimens are provided and some

taxonomical and biogeographical issues are discussed.

Key words. Squamata, Ophidia, biogeography, country checklist, venomous snakes, Central Africa.

INTRODUCTION

The Republic of Chad is the fifth largest country in Af-

rica with an area of 1,284,000 km? between latitudes

7°N—23°N and longitudes 13°E—23°E. The northern

part of the country is Saharan (Fig. 1), the central part

is Sahelian (Fig. 2), or Sudano-Sahelian (Fig. 3), and the

southern part is Sudanese (Fig. 4) or Sudano-Congolese

(Fig. 5). South of 14°N elevation ranges from 280 m to

500 m a.s.l. in most parts of the country where the only

significant reliefs are those of the Guera in central Chad

(1,613 m a.s.l.) and the Monts de Lam in the southwest

(1,163 ma.s.l.). North of 14°N, the Ouaddai plateau rang-

es from 500 m to 1,300 ma.s.I., the Ennedi plateau culmi-

nates at 1,450 ma.s.l., and the Tibesti mountains (Fig. 6)

Received: 03.03.2020

Accepted: 04.11.2020

at 3,414 m asl. (Brami 2012). In northern Chad, the

Bodeélé depression is the lowest area of the country with

165 maz.s.l. and was occupied by Lake MegaChad at the

Holocene before drying up (Leblanc et al. 2006). Average

annual rainfall reaches a maximum of 1,200 mm south

of 8°N and decrease progressively along a South-North

gradient with 500 mm at 12°N and less than 5 mm north

of 18°N, except in the Tibesti mountains where locally

it may exceed 50 mm (Dubief 1963, Mahé et al. 2012).

The southern and central parts of the country have a rich

hydrological system, including Lake Chad, the Chari,

Ouham and Logone rivers, and numerous seasonal tribu-

taries. Each year during the rainy season (June—October)

large parts of the country south of 13°N are flooded.

Corresponding editor: P. Wagner

Published: 17.11.2020

368 Jean-Frang¢ois Trape et al.

Fig. 1. The Sahara desert at Ounianga Serir in northern Chad (18°55’N, 20°54’E) where Cerastes cerastes was collected.

Little data is available on the snakes of Chad. Rous-

sel & Villiers (1965) reported a list of two hundred

snakes belonging to 30 species from Gounou-Gaya

(09°37’N / 15°30’E) and Bongor (10°16’N / 15°22’E).

Graber (1966) reported a collection of 460 specimens

from Fort-Lamy, now N’Djamena (12°06’N / 15°02’E),

and other localities in central and northern Chad. Trape

(2015) reviewed the reptile fauna of northern Chad. Mu-

seum specimens from Chad were included in works on

certain genera or species, in particular by Roux-Esteéve

(1969, 1974), Broadley (1971), Guibé & Roux-Estéve

(1972), Hughes (1976, 1977, 1983, 1985), Broadley

(1984), Schatti (1985), Trape & Roux-Esteve (1990),

Broadley & Hughes (1993, 2000), Jakobsen (1997), Ras-

mussen (1997a, 1997b, 2005a, 2005b), Hahn & Wallach

(1998), Wister & Broadley (2003), Schatti & McCarthy

(2004), Trape & Mané (2006a), Trape et al. (2006, 2012,

2019), Crochet et al. (2008), Chirio et al. (2011), Broad-

ley et al. (2014, 2018), Trape & Mediannikov (2016),

and Wuster et al. (2018). Sindaco et al. (2013) provid-

ed square-degree distribution maps of Palearctic species

distributed in northern Chad. Some unpublished work-

ing documents for national parks management include

lists of snake species, but they are based on presumed

Bonn zoological Bulletin 69 (2): 367-393

distribution maps (e.g., those of Chippaux 1999), not on

specimens really collected or observed in national parks.

MATERIALS AND METHODS

In May 2015, the first author contacted the last author for

a field survey of the snakes of Chad. The Chad Ministry

of Health was interested by this initiative and decided

to provide logistic support and funds for a full research

programme on snakebites and the distribution of snake

species in all administrative regions of the country. The

Baibokoum area was selected by the Ministry of Health

for the first survey since it was known as the place with

the highest incidence and mortality from snakebite in

Chad. From September 2015 to December 2017 addition-

al surveys were conducted in most regions of the country.

Local people at villages were asked to collaborate with

the study and a total of 40 study areas were involved in

the collection of snakes (Table 1), some of them repre-

sented by a single village or study site, and some others

by several neighbouring villages (up to 18 villages for

Baibokoum area). Four of these study areas were located

between 07°00’N and 09°00’N, nine between 09°00’N

and 11°00’N, 12 between 11°00’N and 13°00’N, eight

©ZFMK

The snakes of Chad 369

Co eda! “seamen 2,

Fig. 2. The Sahel near Lake Chad at the end of the rainy season (13°48’N, 15°46’E). Psammophis sudanensis was the most abun-

dant species at this latitude as in most other Sahelian and Sudano-Sahelian areas of Chad. The other common species between 13°N

and 14°N were Psammophis rukwae, Eryx colubrinus, Atractaspis watsoni, Boaedon subflavus, Naja haje and Echis leucogaster.

between 13°00’N and 15°00’N, and seven north of

15°00’N (Fig. 7), where average annual rainfall ranges

approximatively from 1,300—1,100 mm, 1,100—800 mm,

800-400 mm, 400—200 mm, and 200—<5 mm, respec-

tively (Mahé et al. 2012).

Most specimens were deposited at the Programme

National de Lutte contre le Paludisme (PNLP) office in

N’Dyjaména. Selected specimens were deposited at the In-

stitut de Recherche pour le Développement (Dakar, Sen-

egal; acronym: IRD) or donated to the Museum national

d’Histoire naturelle (Paris, France; acronym: MNHN).

Specimens were identified to species according to re-

gional keys (Trape & Mané 2006a, Chirio & LeBreton

2007) and further taxonomic analysis. For recent changes

in snake generic names, we usually followed those adopt-

ed in the reptile database by Uetz et al. (2020).

The first author also examined specimens from Chad

of the MNHN collection, most of them collected either

by Decorse along the Chari River in 1903-1904 (Cha-

banaud 1917), or by Roussel and Stauch in the 1960s.

Most Roussel’s specimens were collected at Gounou-Ga-

ya, some others at Bongor (75 km north of Gounou-Ga-

ya), but all were published then preserved in part in the

Bonn zoological Bulletin 69 (2): 367-393

MNHN collection with Mayo-Kebbi as collecting locali-

ty, 1.e., the name of the province where the two localities

are located (Roussel & Villiers 1965). However, these

authors also provided for each species the vernacular

names of snakes, which differ between Gounou Gaya and

Bongor, thus allowing in most cases to establish which

species were collected in each locality.

RESULTS

We collected a total of 1,512 specimens belonging to 66

species. Fourteen other species occur in Chad, includ-

ing nine species from previous collections preserved at

MNHN in Paris and five species reported in the literature.

Altogether, the total number of snake species currently

known from Chad is 80. Coordinates of our collecting

localities are listed in Table 1, and those from MNHN

and literature are listed in Table 2.

©ZFMK

370 Jean-Frang¢ois Trape et al.

Table 1. Collecting localities of snakes in Chad (our study).

N Locality Latitude Longitude Altitude

1 Arningmalik 14°02’N 21°07°E 716m

2 Bahar 12°03’N oH a bea 511m

3 Baibokoum 07°44"N 15S°4VE 515m

4 Balani 09°42’N 15°00’°E 351m

5 Bereguit (7 km N) 11°39°N 19°08’E 502 m

6 Birim 13°26’N 14°44” E 287m

7 Bitanda 08°34’°N 15°59°E 417m

8 Bitea 13°30’N 20°SV’E 537m

9 Bon Amdaoud 10°41’°N 19°28°E 478m

10 Dyjarat Abounimir 11°01’N 20°00’°E 423m

11 Doureng 13°S54’N 21°00’E 615m

12. Ennedi NW 17°32’N 229° R 822 m

13. Fada 17°117N 21°35" 565m

14 Faya Largeau 17°55’N 19°06’E 242m

15 Fiengbac 09°51°N 15°04’E 325m

16 Goulmounbass 10°19°N 15°19’E 324m

17. Gouroungali 13°13’N 2120375 564 m

18 Gurl 12°40’°N 21°20°E 568 m

19 Hileborno 11°55’N 21°28°E 505 m

20 Kadam Digas 11°53’N k3°52°E 541m

21 + Kiékeé 10°33’N 19°49°E 413m

22 Laobida 09°13’N 15°07°E 425m

23° Leére 09°39°N 14°13°E 235m

24 Mahargal 12°07’N 21° 22-E 527m

25 Mao 14°08’°N 1S°18°E 305m

26 Masarma 12°33’N 16°35’°E 292m

27 Matafo 2 13°31’N 14°40°E 291m

28 Mataya L1E59°N 18°02’E 406 m

29 Moissala 08°20’N 17°49°E 385m

30 Mongo (13 km S) 12°04’°N 18°45°E 460 m

31 Moundou 08°33’N 16°04’ E 404 m

32 N’Djaména (Farcha) 12°06’N 14°58’°E 295 m

33 N’Djaména (Gass!) 12°03’N 15°08°E 298 m

34 Ouadi Haouach 16°08’N 21°07V’E 502 m

35 Ouadi Sofoya/Torboul 15°55’N 20°58’E 479 m

36 Oum Chalouba 15°48°N 20°46’°E 452m

37. Ounianga Serir 18°55’N 20°54’E 360 m

38 Tarhacha 13°38°N 20°35078 526m

39 Tikem 09°49°N 15°03’"E 335m

40 Zamagouin 09°32’N 14°57°E 380 m

Total

Family Typhlopidae, Gray 1845

Ecoregion

Sahel

Sahelo-Sudanese

Sudano-Congolese

Sudanese

Sahelo-Sudanese

Sahel

Sudanese

Sahel

Sudanese

Sahel

Sahara

Sahelian

Sahara

Sudanese

Sahel

Sahelo-Sudanese

Sudanese

Sahelo-Sudanese

Sahel

Sahelo-Sudanese

Sudano-Congolese

Sahel

Sudanese

Sahel

Sahara

Sahel

Sudanese

Literature records:

1974).

Afrotyphlops lineolatus (Jan, 1864)

Material: no specimen collected.

Other specimens (coll. MNHN): Fort-Lamy (= N’ Djamé-

na) (2), Chari (2).

N° of specimens

ANrRe NNR OO 4

ies)

1,512

N° of species

N= FSB NOK KF BRK OO

NDR lire

Nin

Fort-Lamy, Chari (Roux-Estéve

Afrotyphlops punctatus (Leach, 1819)

Material: 15 specimens.

Localities: Batbokoum (9), Bitanda (1), Bon Amdaoud

(3), Moundou (1), Zamagouin (1).

Bonn zoological Bulletin 69 (2): 367-393

©ZFMK

The snakes of Chad Seal

Fig. 3. The Sahelo-Sudanese savanna in eastern Chad (11°45’N / 21°10’E) near Bahar, Hileborno and Mahargal study villages.

The most common species collected in this area were Psammophis rukwae, Psammophis sudanensis, Crotaphopeltis hotamboeia,

Echis leucogaster and Atractaspis watsoni.

Other specimens

Mayo-Kebbi (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Fort-Lamy, Bisneye (Graber 1966), Fort Lamy,

Mayo-Kebbi (Roux-Esteve 1974).

(coll. MNHN): Fort-Lamy (4),

Letheobia weidholzi Wallach & Gemel, 2018

Material: 1 specimen.

Locality: Baibokoum (1).

Remarks: The Baibokoum specimen is the holotype of

Letheobia logonensis Trape, 2019, which we now con-

sider as a junior synonym of L. weidholzi which was

published independently a few months earlier, based on a

single old museum specimen from Garoua (Cameroon).

Our specimen was collected in a field near the Logone

River. A third known specimen of this species was col-

lected at Yola, Adamawa, Nigeria. It was erroneously at-

tributed to Letheobia praeocularis (Stejneger, 1894) by

Rasmussen (1997a) and Wallach & Gemel (2018). Both

Specimens are new country records and extend the range

of Letheobia weidholzi to Nigeria and Chad.

Bonn zoological Bulletin 69 (2): 367-393

Family Leptotyphlopidae Stejneger, 1892

Myriopholis adleri (Hahn & Wallach, 1998)

Material: no specimen collected.

Other specimens (coll. MNHN): Bongor (3).

Literature records: Bongor (Hahn & Wallach 1998, Trape

2002).

Remark: Bongor is the type locality and easternmost

record of this species distributed from Senegal to Chad

(Trape 2002, Trape & Mané 2006a). It was reported in

error from Birao in Central African Republic by Chirio &

Ineich (2006) (Trape unpublished).

Myriopholis boueti (Chabanaud, 1917)

Material: 12 specimens collected.

Localities: Bahar (3), near Béréguit (1), Bitea (1), Bon

Amdaoud (2), Guirli (1), Kiéké (1).

Other specimens (coll. MNHN): Maillao (1), N’Djaména

Literature records: Maillao, N’Djaména (Hahn & Wal-

lach 1998, as Leptotyphlops narirostris boueti).

©ZFMK

372

Table 2. Coordinates of snake records from Chad (literature data). The asterisks indicate approximate entries.

Locality

Abéché

Archei

Ati

Ati (35 km SW)

Aozou

Bachikélé

Baguirmi (region)

Bahr-el-Ghazal

Bardai

Batha

Bisneye

Bol

Bokoro

Bongor

Chari (River)

Dejemine Batha

Djintilo

Fada

Faya Largeau

Fitri (Lake)

Fort-Archambault (= Sarh)

Fort-Lamy (=N’ Djaména)

Goré

Gounou-Gaya

Iro (Lake)

Koalem

Koboué

Koskobo

Koudoubol

Kumao

Maillao

Mao

Mayo-Kebbi (region)

Mboura

Melfi

N’Djaména

Ngodem

Niellim

Ouadi Fama

Ouadi Rimé

Oued Basso

Oum Chalouba

Oum El Adam

Sarh

Tirreno (well)

Torboul (vicinity of)

Yambatchingsou

Yebbi-Bou

Zakouma

Bonn zoological Bulletin 69 (2): 367-393

Longitude

13°50’N

16°54’N

13°13’N

13°00’N

21°48’N

16°32’N

11°N*

14°30’N*

21°20’N

13°30’N*

12°40’N

13°28’N

12°22’N

10°16’N

09/11°N*

13°30’N*

12°49°N

17°117N

17°55’N

12°50’N

09°08’N

12°06’N

07°S55’N

09°37’N

10°06’N

09°49°N

be2o-N

09°29°N

13°24’N

07°36’N

11°35’N

14°08’N

09/10°N

07°35’N

11°03’N

12°06’N

}1°25"N

09°42’N

13522.N"

14°00’N

172302 N*

15°48’N

[12 Ni

09°08’N

21°34’N

15°57°N

09°11°N

20°55’N

10°53’N

Jean-Francois Trape et al.

Latitude

20°49°E

21°46°E

18°20’E

18°06’E

2a"

22 20-E

Loc Ee

LOU" E*

17°0VE

18°30’E*

16°10°E

14°44’E

17°03’E

155225

15/18°E*

18°30°E*

14°33’E

21°35’N

19°06’E

7°30

Loe227 7

1S°OV’E

16°38°E

15°30°E

19°26°E

17°42’E

22°03" E

19°} 5

14°43’E

15°36°E

15°16°E

1S"18"E

14/15°E

15° 355

[7° 35°E

1S°OL'E

15°04’E

17°48’E

20°34’ E*

18°00’E

de a2: Ee

20°46°E

ALi

18°22°E

17°19" E

21°S’E

15°10°E

18°05’E

19°490°E

Altitude

540 m

580 m

335m

334m

920 m

720 m

330 m*

285 m

1020 m

340 m

290 m

285 m

300 m

335m

290/370 m

340 m

290 m

565 m

242 m

285m

370 m

298 m

430 m

345 m

390 m

355m

790 m

382 m

285 m

575 m

300 m

305 m

350 m*

530 m

405m

298 m

305 m

365 m

435m

309 m

845 m

452m

490 m

370 m

1650 m

626 m

402 m

1385 m

420 m

Ecoregion

Sahel

Sahara

Sahel

Sahel/Sudanese

Sahel

Sahara

Sahel

Sudanese

Sahel/Sudanese

Sahel

Sahara

Sahel

Sudanese

Sahel

Sudano-Congolese

Sudanese

Sahara

Sudanese

Sahel

Sudano-Congolese

Sahelo-Sudanese

Sahel

Sudanese

Sudano-Congolese

Sudanese

Sahel

Sudanese

Sahel

Sahara

Sahel

Sahara

Sudanese

Sahara

Sahel

Sudanese

Sahara

Sudanese

©ZFMK

The snakes of Chad 373

Fig. 4. The Sudan Savanna and Salamat River at Zakouma National Park during the dry season (10°50’N, 19°47’E). Three study

villages (Djarat Abounimir, Bon Amdaoud and Kiéké) were located at the eastern, western and southern limits of the park, respec-

tively, where 25 snake species were collected.

Myriopholis lanzai Broadley, Wade & Wallach, 2014

Material: no specimen collected.

Other specimens (coll. MNHN): Faya (1).

Literature records: Faya Largeau (Le Berre 1989, as

Leptotyphlops macrorhynchus), Chad (Hahn & Wallach

1998, as Leptotyphlops cairi), Faya Largeau (Broadley

et al. 2014, Trape 2015).

Myriopholis occipitalis (Trape & Chirio, 2019)

Material: 1 specimen collected.

Locality: Moissala (1).

Literature record: Moissala (Trape & Chirio 2018).

Remarks: The type locality of this recently described

species is located in Central African Republic (Kouki,

07°09°N / 17°18’E), 150 km south of Moissala (Trape &

Chirio 2019).

Tricheilostoma sundewalli (Jan, 1861)

Material: 1 specimen collected.

Locality: Baibokoum (1).

Other specimen (coll. MNHN): Gounou-Gaya (1)

Literature record: Gounou-Gaya (Roussel & Villiers

1965, as Leptotyphlops bicolor).

Bonn zoological Bulletin 69 (2): 367-393

Remarks: First record for Chad. 7: bicolor, erroneously

reported from Chad by Roussel & Villiers (1965), seems

restricted to West Africa with Nigeria as easternmost lim-

it.

Family Boidae Gray, 1825

Eryx colubrinus (Linnaeus, 1758)

Material: 15 specimens collected.

Localities: Birim (2), Bitea (2), Doureng (3), Gourounga-

li (1), Guirli (4), Matafo 2 (1), Tarhacha (2).

Other specimen (coll. MNHN): Bol (1).

Literature records: Abéché, Bahr-el-Ghazal, Buisne-

ye, Mao (Graber 1966), Bachikélé, Ouadi Rimé (Trape

2015).

Eryx muelleri (Boulenger, 1892)

Material: 9 specimens collected.

Localites: Masarma (9).

Other specimens: Mayo Kebbi (1, coll. MNHN), Ouadi

Rimé (1, coll. IRD).

©ZFMK

374 Jean-Frang¢ois Trape et al.

Fig. 5. The Sudano-Congolese savanna in southern Chad near Moissala is strongly impacted by agricultural activities (08°05’N,

17°40’E). The most common snake species were Psammophis mossambicus, Psammophis sudanensis, Naja nigricollis and Lyco-

Dhidion semicinctum.

Literature records: Gounou-Gaya, Bongor (Roussel &

Villiers 1965), Fort-Lamy, Bahr-el-Ghazal (Graber

1966).

Remark: On 23 January 2003, the first author observed

several dozens of dessicated Eryx specimens around a

dried pool of the Ouadi Rimé (14°00°54’”’N, 18°00’12”E).

Several specimens were attributed to E. colubrinus in the

field and a voucher specimen 1s attributable to &. muel-

leri.

Family Pythonidae Fitzinger, 1826

Python regius (Shaw, 1802)

Material: 6 specimens collected.

Localities: Baibokoum (5), Laobida (1).

Literature records: Gounou-Gaya, Bongor (Roussel &

Villiers 1965).

Python sebae (Gmelin, 1788)

Material: 7 specimens collected.

Localities: Bitea (2), Hileborno (1), Kadam Digas (2),

Mataya (1), Zamagouin (1).

Other specimen (coll. MNHN): south of Abéché (1).

Bonn zoological Bulletin 69 (2): 367-393

Literature records: Gounou-Gaya, Bongor (Roussel &

Villiers 1965), Batha, Bokoro, Bol, Fort-Lamy, Nokou,

Ouaddai (Graber 1966), Lac Fitri (ORSTOM, unpub-

lished), Lac Iro (Pairault 1994), Zakouma (Dejace 2002).

Family Colubridae Oppel, 1811

Crotaphopeltis degeni (Boulenger, 1906)

Material: 23 specimens collected.

Localities: Djarat Abounimir (7), Fiengbac (1), Goul-

mounbass (11), Kiéké (2), N’ Djaména (1), Tikem (1).

Other specimen (coll. MNHN): Ngodem (3).

Literature record: Ngodem (Rasmussen 1997b).

Crotaphopeltis hippocrepis (Reinhardt, 1843)

Material: 14 specimens collected.

Localities: Baibokoum (2), Bitanda (1), Djarat Abouni-

mir7Gl)

Remark: First record for Chad (but appeared in error

on maps of Chippaux [1999] and Chippaux & Jackson

[2019]).

Crotaphopeltis hotamboeia (Laurenti, 1768)

©ZFMK

The snakes of Chad 375

Fig. 6. The Tibesti mountains near the Pic Toussidé (3315 m) in the background and the caldera of the Trou du natron in the fore-

ground (20°57°N, 16°33’E). Snake species currently known from the Tibesti include Echis leucogaster, Cerastes cerastes, Cerastes

vipera, Psammophis aegyptius and Platyceps saharicus.

Material: 122 specimens collected.

Localities: Bahar (18), Baibokoum (18), Bitanda (3),

Bon Amdaoud (10), Djarat Abounimir (48), Goulmoun-

bass (1), Hileborno (1), Kadam Digas (7), Kiéké (6),

Laobida (2), Mahargal (3), Moissala (2), Moundou (1),

Zamagouin (1).

Other specimens (coll. MNHN): Baguirmi (1), Maillao

(4).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Ati, Bisneye, Fort-Lamy (Graber 1966).

Dasypeltis confusa Trape & Mané, 2006

Material: 2 specimens collected.

Locality: Baibokoum (2).

Other specimen (coll. MNHN): Mayo Kebbi (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as Dasypeltis scabra scabra), Mayo Kebbi (Bates

2013).

Dasypeltis gansi Trape & Mané, 2006

Material: 14 specimens collected.

Localities: Baibokoum (8), Laobida (2), Moissala (2),

Zamagouin (2).

Bonn zoological Bulletin 69 (2): 367-393

Other specimen (coll. MNHN): Koudoubol (1).

Literature record: Bol, Koudoubol (Bates & Ineich,

2012).

Dasypeltis sahelensis Trape & Mané, 2006

Material: 7 specimens collected.

Localities: Bon Amdaoud (1), Goulmounbass (1), Guirli

(1), Kadam Digas (2), Mahargal (1), N’ Djaména (1).

Other specimens (coll. MNHN): N’Djaména (2).

Literature record: Fort-Lamy (Graber 1966, as Dasypel-

tis scabra).

Remarks: First record for Chad. All previous records of

this species were either from West Africa or Morocco

(Trape & Mané 2006b, Trape et al. 2012). We also attri-

bute to D. sahelensis the El Geneina specimen (Darfur,

Sudan) attributed to D. scabra by Colley (1946).

Dispholidus aff. typus (Smith, 1829)

Material: 6 specimens collected.

Localities: Baibokoum (5), Moissala (1).

Literature record: Gounou-Gaya (Roussel & Villiers

1965).

©ZFMK

376 Jean-Frang¢ois Trape et al.

= \>

a ®

3 Sah as

~< Ss = *

= 2

% RAR

“hee |

iva

a(S

poem | Se 4 =

=== — : za

| IR ARDENNE

a > TiN »

ah i . . x iy a

= J 1 mo RS

= no a i

fs of

| Aes Laie

if ‘ )

ES es ees

a | S

14E 16E 18E 20E 22E 24E

Fig. 7. Map of Chad with location of study areas. See Table 1

for locality numbers. Tikem and Balani, two close villages, and

Farcha and Gassi, two suburbs of N’Djaména, are represented

by a single number (4 and 33 respectively). Colours for vegeta-

tion areas: Congolese: dark green; Sudanese: green; Sahelian:

light green; Saharan: yellow for sandy areas, white for stony

areas, grey for rocky and mountainous areas.

Remarks: Molecular studies have shown that the

Boomslang is a complex of several species, with D. typus

restricted to southern South Africa (Eimermacher 2012).

Perret (1961) highlighted some pattern and colour differ-

ences between the material he collected in Cameroon and

the various subspecies described from D.R. Congo and

Southern Africa. He proposed the name occidentalis ssp

n. for his material. Our specimens from Chad match the

description of occidentalis.

Grayia smithii (Leach, 1818)

Material: no specimen collected.

Other specimens (coll. MNHN): Gounou-Gaya (1), Chari

H656 (1).

Literature record: Gounou-Gaya (Roussel & Villiers

1965, as Grayia tholloni).

Remarks: The Gounou-Gaya specimen (MNHN

1965.397), previously attributed to G. tholloni by Rous-

sel & Villiers (1965), is a male with only 15 rows of dor-

sal scales, 8(4) and 7(4) supralabials, 158 ventrals and 89

subcaudals. Despite its low number of dorsals, it clear-

ly belongs to G. smithii. The Chari specimen (MNHN

1978.1832) has 7(4) supralabials on each side of the

Bonn zoological Bulletin 69 (2): 367-393

head, 155 ventrals and a mutilated tail. It also presents a

low number of dorsals, only 16 rows at midbody.

Meizodon coronatus (Schlegel, 1837)

Material: 4 specimens collected.

Localities: Baibokoum (3), Laobida (1).

Literature record: Mayo-Kebbi (Roussel & Villiers 1965,

Roux-Esteéve 1969).

Meizodon regularis Fisher, 1856

Material: no specimen collected.

Literature record: Koskobo (Schatti 1985).

Meizodon semiornatus tchadensis (Chabanaud, 1917)

Material: 1 specimen collected.

Localities: Bahar (1),

Other specimen (coll. MNHN): Koalem (1).

Literature records: Koalem (Chabanaud 1917, holotype

de Zamenis tchadensis), Abéché, Fort-Lamy (Graber

1966, as Meizodon coronatus), Fort-Lamy (Roux-Esteve

1969, Schatti 1985).

Natriciteres olivacea (Peters, 1854)

Material: 1 specimen collected.

Locality: Birim (1).

Other specimens (coll. MNHN): Maillao (2).

Remarks: First records for Chad and Lake Chad area.

Philothamnus bequaerti (Schmidt, 1923)

Material: 2 specimens collected.

Localities: Baibokoum (1), Moissala (1).

Literature record: Sarh (Hughes 1985).

Philothamnus hughesi Trape & Roux-Esteéve, 1990

Material: no specimens collected.

Other specimen (coll. MNHN): Chari (1).

Literature record: Chad (Trape & Roux-Esteve 1990).

Remark: This specimen (MNHN 1904.0186) was col-

lected by J. Decorse during the 1902—1904 Chari — Lake

Chad expedition. There is no precise location but the

most likely origin of this specimen is between 8°N and

9°N on the banks of the upper Chari River which is is-

sued from the junction of Bamingui and Gribingui rivers.

Additional specimens of P. hughesi were collected at the

same latitude in Central African Republic (Chirio & In-

eich 2006).

Philothamnus irregularis (Leach, 1819)

Material: 22 specimens collected.

Localities: Baibokoum (18), Zamagouin (4).

Other specimen (coll. MNHN): Maillao (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Fort-Lamy (Graber 1966).

Philothamnus aff. semivariegatus (Smith, 1840)

Material: 3 specimens collected.

©ZFMK

The snakes of Chad SL.

Fig. 8. View of Baibokoum area where 40 species of snakes were collected within only ten days. The Logone occidentale River is

in the background, the rocky hill that dominates Baibokoum is in the foreground (07°44’N, 15°40’E).

Localities: Baibokoum (1), Moissala (1), Moundou (1).

Other specimen (coll. MNHN): Maillao (1).

Remarks: Philothamnus semivariegatus is now restricted

to southern Africa (Engelbrecht 2019) and further molec-

ular studies are needed to establish the status of Central

African populations. This species complex is represent-

ed by Philothamnus smithi Bocage, 1882, in West Afri-

ca (Trape & Baldé 2014) and possibly also in Chad and

the whole savannas areas north of the Congolese forest

block.

Platyceps florulentus (Geoffroy, 1827)

Material: 6 specimens collected.

Localities: Arningmalik (1), Bitea (3), Doureng (2).

Remarks: First record for Chad. Our six specimens, all

from Ouaddai plateau, show 21 rows of dorsal scales,

compared to 25 rows for the subspecies P. f perreti

(Schatti, 1988) from northern Cameroon and north-east-

ern Nigeria reliefs.

Platyceps saharicus Schatti & McCarthy, 2004

Material: No specimen collected.

Literature records: Aozou (Beck & Huard 1969, as Zame-

nis rhodorachis), Yebbi-Bou (Le Berre 1989, as Coluber

Bonn zoological Bulletin 69 (2): 367-393

rhodorachis), Yebbi-Bou (Schatti & McCarthy 2004),

Gouffre de Koboué (Geniez & Gauthier 2008), Aozou,

Yebbi-Bou, Koboué (Trape 2015, as Platyceps tesselata).

Scaphiophis albopunctatus Peters, 1870

Material: 11 specimens collected.

Localities: Baibokoum (6), Bon Amdaoud (2), Laobida

(3).

Other specimens (coll. MNHN): Mayo-Kebbi (1), Mail-

lao (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Fort-Lamy (Graber 1966), Maillao, Mayo-Kebbi

(Broadley 1994).

Spalerosophis diadema cliffordi (Schlegel, 1837)

Material: no specimen collected.

Other specimen (coll. MNHN): Ouadi Fama (1).

Remark: First record for Chad.

Telescopus obtusus (Reuss, 1834)

Material: No specimen collected.

Literature record: Oum El Adam (Wake & Kluge 1961,

as Tarbophis obtusus), Oum El Adam (Crochet et al.

2008, Trape 2015, as Telescopus dhara obtusus).

©ZFMK

378 Jean-Frang¢ois Trape et al.

Telescopus tripolitanus (Werner, 1909)

Material: 12 specimens collected.

Localities: Bahar (1), Bitea (2), Bon Amdaoud (9).

Remark: First record for Chad.

Telescopus variegatus (Reinhardt, 1843)

Material: 14 specimens collected.

Localities: Baibokoum (3), Laobida (9), Moissala (1),

Zamagouin (1).

Other specimen (coll. MNHN): Mayo-Kebbi (1).

Literature record: Gounou-Gaya (Roussel & Villiers

1965).

Family Lamprophiidae Ritzinger, 1843

Amblyodipsas unicolor (Reinhardt, 1843)

Material: 4 specimens collected.

Localities: Baibokoum (2), Moissala (1), Tikem (1).

Other specimen (coll. MNHN): Mayo-Kebbi (1).

Literature record: Gounou-Gaya (Roussel & Villiers

1965).

Aparallactus lunulatus nigrocollaris Chabanaud, 1916

Material: 4 specimens collected.

Locality: Baibokoum (4).

Remark: First record for Chad.

Atractaspis aterrima Gunther, 1863

Material: no specimen collected.

Other specimen (coll. MNHN): Fort-Archambaut (1).

Literature record: Chari (Rasmussen 2005a).

Atractaspis dahomeyensis Barboza du Bocage, 1887

Material: 4 specimens collected.

Locality: Baibokoum (4).

Remarks: First record for Chad. This West African spe-

cies seems to be very rare east of Nigeria where the

only other records are those from Sternfeld (1908) in

south-western Cameroon (Chirio & LeBreton 2007). At-

ractaspis dahomeyensis was erroneously reported from

Central African Republic by Chippaux (1999) (plots on

the distribution map are those of A. watsoni). Two of our

Baibokoum specimens were sequenced and proved simi-

lar to West African specimens (Portillo et al. 2019).

Atractaspis micropholis Gunther, 1872

Material: 2 specimens collected.

Localities: Arningmalik (1), Gouroungali (1).

Remarks: First record for Chad. The occurrence of this

species in OQuaddai extends 900 km eastward the known

distribution of this species previously reported from Sen-

egal to Nigeria (Trape et al. 2006, Trape & Mané 2006).

Atractaspis watsoni Boulenger, 1908

Material: 56 specimens collected.

Bonn zoological Bulletin 69 (2): 367-393

Localities: Bahar (3), Balani (2), Bitea (11), Bon Am-

daoud (3), Djarat Abounimir (9), Goulmounbass (1),

Guirli (1), Hileborno (3), Kadam Digas (14), Kiéké (1),

Mahargal (2), Masarma (1), Zamagouin (5).

Other specimens (coll. MNHN): Mayo Kebbi (1),

N’Dyjaména (2).

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as Atractaspis microlepidota), Fort-Lamy (Graber

1966), Maillao, Mayo-Kebbi, N’Djaména (Trape et al.

2006).

Boaedon longilineatus Trape, 2016

Material: 18 specimens collected.

Localities: Bahar (1), Bon Amdaoud (2), Djarat Abouni-

mir (6), Fiengbac (2), Goulmounbass (2), Hileborno (1),

Masarma (3), Zamagouin (1).

Other specimens (coll. MNHN): Chari (2), Mayo-Kebbi

(1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as B. fuliginosum forme lineatum), Fort-Lamy

(Graber 1966, as B. fuliginosum forme lineatum), Fieng-

bac, Goulmounbass, Zamagouin (Trape & Mediannikov

2016).

Remarks: This species recently described is currently

known from Cameroon and Chad (Trape & Mediannikov

2016). We also attribute to B. /ongilineatus part of the

specimens from El Geneina (Darfur, Sudan) attributed to

B. lineatus by Colley (1946).

Boaedon paralineatus Trape & Mediannikov, 2016

Material: 34 specimens collected.

Localities: Baibokoum (31), Bitanda (3).

Literature record: Baibokoum (Trape & Mediannikov

2016).

Remark: This species recently described is currently

known from Cameroon, Chad and Central African Re-

public (Trape & Mediannikov 2016, Trape unpublished).

Boaedon perisilvestris Trape & Mediannikov, 2016

Material: 2 specimens collected.

Locality: Baibokoum (2).

Literature record: Baibokoum (Trape & Mediannikov

2016).

Remark: This species recently described is currently

known from Chad, Cameroon, SE Nigeria, Gabon, Con-

go-Brazzaville, D. R. Congo, Central African Republic

and South Sudan (Trape & Mediannikov 2016, Nneji

et al. 2019, Trape unpublished).

Boaedon subfiavus Trape, 2016

Material: 125 specimens collected.

Localities: Bahar (8), Baibokoum (60), Balani (2), Bi-

tanda (5), Bitea (10), Bon Amdaoud (15), Doureng (1),

Goulmounbass (1), Kadam Digas (9), Laobida (4), Ma-

hargal (4), Moundou (3), Tikem (1), Zamagouin (2).

©ZFMK

The snakes of Chad 379

Literature record: Gounou-Gaya (Roussel & Villiers

1965, as B. fuliginosum “forme typique”), Fort-Lamy

(Graber 1966, as B. fuliginosum “forme fuliginosum’”’),

Baibokoum, Balani, Goulmounbass, Kumao, Malgan-

di, Moundou, Tikem, Yambatchingsou, Zamagouin

(Trape & Mediannikov 2016).

Remark: This species recently described is currently

known from Cameroon, Central African Republic and

Chad (Trape & Mediannikov 2016).

Gonionotophis grantii (Gunther, 1863)

Material: 1 specimen collected.

Locality: Baibokoum (1).

Literature record: a specimen of unknown origin is

mapped near Bongor in Chippaux (2006) and Chip-

paux & Jackson (2019).

Hemirhagerrhis nototaenia (Gunther, 1864)

Material: 2 specimens collected.

Localities: Baibokoum (1), Kiéké (1).

Other specimens (coll. MNHN): N’Djaména (1), Niellim

(1).

Literature record: N’Djaména (Broadley & Hughes

2000).

Limaformosa crossi (Boulenger, 1895)

Material: 12 specimens collected.

Localities: Baibokoum (10), Bitanda (1), Zamagouin (1).

Other specimen (coll. MNHN): Mayo-Kebbi (1).

Literature record: Gounou-Gaya (Roussel & Villiers

1965).

Remark: One specimen from Baibokoum was included

in the phylogeny and genus-level revision of the African

file snakes Gonionotophis and Mehelya (Broadley et al.

2018).

Lycophidion aff. capense (Smith, 1831)

Material: 3 specimens collected.

Localities: Bon Amdaoud (2), Kiéké (1).

Remark: First record for Chad. Our specimens are three

males with a single apical pit, a postnasal in contact

with the first supralabial, 17-17-15 dorsals, 180-187

ventrals and 32-37 subcaudals. The top of the head and

the snout are uniformly blackish, but there are limited

white vermiculations on the side of the head. The dor-

sal scales have a light apical spot increasing in size on

the lower lateral rows where they form a light border.

The ventrum is uniformly dark except a light border on

the more lateral part of the ventrals and white vermicula-

tions on the throat. These specimens probably belong to

an undescribed species since they differ from the nearest

East-African representative of the L. capense complex

(L. capense jacksoni) by a lower number of subcaudals

and a different colour pattern (Broadley & Hughes 1993,

Broadley 1996).

Bonn zoological Bulletin 69 (2): 367-393

Lycophidion semicinctum (Dumeéril, Bibron & Dumeéril,

1854)

Material: 20 specimens collected.

Localities: Baibokoum (8), Bitanda (3), Laobida (1),

Moissala (8).

Other specimens (coll. MNHN): Fort-Archambault (1),

Mayo-Kebbi (1).

Literature records: Fort-Archambault, Mayo-Kebbi

(Guibé & Roux-Esteve 1972), Mayo-Kebbi (Roussel &

Villiers 1965, as Lycophidion irroratum).

Lycophidion taylori Broadley & Hughes, 1993

Material: 2 specimens collected.

Localities: Bahar (1), Hileborno (1)

Other specimen (coll. MNHN): 20 km E of Abéché (1).

Literature record: Abéché (Broadley & Hughes 1993).

Malpolon moilensis (Reuss, 1834)

Material: 2 specimens collected.

Localities: Ennedi 17°32’N / 21°29°E (1), Ouadi

Haouach (1).

Literature record: Ennedi 17°32’N / 21°29’E (Trape

2015, as Rhagerhis moilensis).

Remarks: The Ennedi specimen was the first record for

Chad. We follow Figueroa et al. (2016) in reattributing

this species to the genus Malpolon.

Micrelaps vaillanti (Mocquard, 1888)

Material: 7 specimens collected.

Localities: Bon Amdaoud (4), Kiéké (1), Mahargal (2).

Remarks: First record for Chad. The occurrence of this

species in Sila and Salamat provinces, including the Zak-

ouma National Park, extends 1,200 km westward the

distribution of this species known from East Africa and

Kurdufan in Sudan (Rasmussen 2002).

Prosymna ambigua Bocage, 1876

Material: 1 specimen collected.

Locality: Moissala (1).

Remark: First record for Chad and northernmost record

of these wet Congolese savanna species.

Prosymna collaris (Sternfeld, 1908)

Material: 10 specimens collected.

Localities: Bahar (4), Balani (2), Djarat Abounimir (1),

Fiengbac (2), Moundou (1).

Other specimens (coll. MNHN): Mayo-Kebbi (3).

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as Prosymna meleagris), Abéché, Fort-Lamy (Gra-

ber 1966, as Prosymna meleagris), Maillao, Mayo-Kebbi

(Chirio et al. 2011, as Prosymna greigerti collaris).

Remarks: The occurrence of both collaris and greiger-

ti patterns at Bahar (Sila province), Djarat Abounimir

(Salamat province) and Moundou/Bitanda (Logone ori-

ental province) support the view that these two taxa are

best treated as separate species. As well documented in

©ZFMK

380 Jean-Frang¢ois Trape et al.

other parts of West and Central Africa (Chirio et al. 2011)

and confirmed in Chad, most of their respective ranges

are distinct (mainly sahelian for co//aris and sudanese for

greigerti).

Prosymna greigerti Mocquard, 1906

Material: 17 specimens collected.

Localities: Bahar (4), Baibokoum (4), Bitanda (1), Bon

Amdaoud (1), Djarat Abounimir (15), Kadam Digas (3),

Moissala (1).

Remark: First record for Chad, all previous literature re-

ports correspond to P. collaris.

Psammophis aegyptius Marx, 1958

Material: No specimen collected.

Other specimen (coll. MNHN): Dejemine Batha (1).

Literature records: Abéché, Bahr el Ghazal, Fort-Lamy

(Graber 1966, as Psammophis schokari), puits de Tiren-

no (Beck & Huard 1969, as Psammophis schokari).

Psammophis afroccidentalis Trape, Bohme & Median-

nikov, 2019

Material: 1 specimen collected.

Locality: Mao (1).

Literature record: Mao (Trape et al. 2019).

Remarks: This specimen was included tn the recent re-

view and molecular study of the Psammophis sibilans

group in Africa north of 12°S (Trape et al. 2019). It was

the only specimen from Chad belonging to Psammophis

afroccidentalis, a species new for Chad widely distribut-

ed in West Africa and previously confounded with P. sib-

ilans. The specimens from other areas of Chad classically

assigned to P. sibilans belong to P. rukwae or P. sudan-

ensis.

Psammophis elegans elegans (Shaw, 1802)

Psammophis elegans univittatus Perret, 1961

Material: 16 specimens collected, including 14 univitta-

tus.

Localities: Mao (2 elegans), Baibokoum (6 univittatus),

Bon Amdaoud (7 univittatus), Djarat Abounimir (1 uni-

vittatus).

Remarks: First record for Chad. Reported in error on

maps of Chippaux (2006) and Chippaux & Jackson

(2019). Interestingly Mao, north of Lake Chad, is the

only known locality in Chad and the easternmost record

for both P. afroccidentalis and the nominative subspecies

of P. elegans.

Psammophis lineatus (Duméril, Bibron & Duméril,

1854)

Material: 64 specimens collected.

Localities: Baibokoum (15), Bitanda (2), Goulmounbass

(42), Léré (2), Zamagouin (3).

Other specimen (coll. MNHN): Mayo-Kebbi (1).

Bonn zoological Bulletin 69 (2): 367-393

Literature record: Gounou-Gaya (Roussel & Villiers

1965, as Dromophis lineatus), Fort-Lamy (Graber 1966,

as Dromophis lineatus).

Psammophis mossambicus (Peters, 1882)

Material: 61 specimens collected.

Localities: Baibokoum (41), Bitanda (1), Laobida (6),

Moissala (12), Moundou (1).

Literature record: Fort-Archambault (Loveridge 1940, as

Psammophis sibilans phillipsii).

Remarks: Several specimens were included in the recent

review and molecular study of the Psammophis sibilans

group in Africa north of 12°S (Trape et al. 2019). This

study has shown that P. phillipsii is restricted to West Af-

rica and that P. mossambicus is distributed both in south-

ern Africa and north, east and south of the Congolese

forest block.

Psammophis praeornatus gribinguiensis (Angel, 1921)

Material: No specimen collected.

Literature records: Logone region (Loveridge 1940, as

Dromophis praeornatus gribinguiensis), Mayo-Kebbi

(Roussel & Villiers 1965, as Dromophis praeornatus),

Zakouma (Dejace 2002).

Psammophis rukwae Broadley, 1966

Material: 160 specimens.

Localities: Bahar (11), Baibokoum (30), Birim (7), Bitea

(7), Bon Amdaoud (3), Djarat Abounimir (37), Fiengbac

(2), Goulmounbass (8), Gouroungali (1), Hileborno (2),

Kadam Digas (5), Kiéké (10), Mahargal (11), Masarma

(8), Matafo 2 (2), Mataya (2), N’Djaména Farcha (4),

N’Djaména Gassi (5), Tikem (1), Zamagouin (4).

Literature records: Fort-Archambault (Loveridge 1940,

as Psammophis sibilans), Gounou-Gaya (Roussel & Vil-

liers 1965, as Psammophis sibilans sibilans forme typ-

ique), Fort-Lamy, Bokoro, Oum Chalouba (Graber 1966,

as Psammophis sibilans, pro parte).

Remarks: Several specimens were included in the recent

review and molecular study of the Psammophis sibilans

group in Africa north of 12°S (Trape et al. 2019). P. ruk-

wae ranges from East Africa to Chad and Cameroon and

is replaced by P. afroccidentalis in West Africa, with

P. sibilans restricted to Egypt, Sudan and Ethiopia.

Psammophis sudanensis Werner, 1919

Material: 174 specimens collected.

Localities: Arningmalick (4), Bahar (2), Baibokoum

(16), Balani (1), Bitea (30), Bon Amdaoud (25), Dyarat

Abounimir (45), Doureng (1), Goulmounbass (3), Guirli

(1), Hileborno (2), Kadam Digas (13), Kiéké (2), Ma-

hargal (15), Masarma (3), Moissala (8), Moundou (1),

Zamagouin (3).

Other specimens (coll. MNHN): Bol (1), N’ Djaména (6).

©ZFMK

The snakes of Chad 381

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as Psammophis sibilans sibilans pro parte), Fort-

Lamy (Graber 1966, as Psammophis sibilans pro parte).

Remarks: First record for Chad. Paradoxically, P. sudan-

ensis is the most common snake in the Sahel and Sudan

savannas of Chad. Almost all specimens have the lineated

head and dorsal pattern typical of this species but some

rare specimens are plain (e.g., IRD 2871.N from Arning-

malick and IRD 2884.N from Bitea). Several specimens

were included in the recent review and molecular study

of the Psammophis sibilans group in Africa north of 12°S

(Trape et al. 2019).

Rhamphiophis oxyrhynchus (Reinhardt, 1843)

Material: 55 specimens collected.

Localities: Bahar (1), Baibokoum (21), Bitanda (11), Bon

Amdaoud (8), Fiengbac (1), Goulmounbass (3), Kadam

Digas (3), Laobida (3), Moissala (2), Moundou (2).

Other specimens (coll. MNHN): Fort-Archambault (1),

Maillao (1), Mayo-Kebbi (4).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Fort-Lamy (Graber 1966), Sarh (Chirio & Ineich

1991).

Rhamphiophis rostratus Peters, 1854

Material: 1 specimen collected.

Locality: Bitea (1).

Remarks: First record for Chad, extending 950 km west-

ward the distribution of this species known from Kurdu-

fan in Sudan, and also distributed in eastern and southern

Africa.

Family Elapidae Boie, 1827

Elapsoidea laticincta (Werner, 1919)

Material: 2 specimens collected.

Locality: Baibokoum (2).

Literature record: Goré (Jakobsen 1997).

Remarks: The holotype designated by Werner is a female

from Kadugli (Sudan) with 150 ventrals, 13 subcaudals,

13 pale bands on the dorsum of body and tail. The head is

pale with forward prolongation of first dark nuchal band

onto frontal where it is forked (see picture of the holo-

type in Jakobsen [1997]). This species has been reported

from Sudan, South Sudan, D.R. Congo, Central African

Republic, Cameroon and Chad (Jakobsen 1997, Chirio &

LeBreton 2007). According to Broadley (1971, 1998)

and Jakobsen (1997) this species is possibly conspecific

with E. semiannulata moebiusi. However, according to

Jakobsen (1997) the two taxa can be distinguished on the

basis of the number of ventral scales (Jaticincta 139-151

in males and 140-150 in females, moebiusi 151-167 in

males and 148-161 in females) and the dorsal pattern

(laticincta 8—17 pale bands, usually with white reticulate

pattern, moebiusi 10—21 bands without reticulate pat-

tern). Two specimens from Baibokoum (one male and

Bonn zoological Bulletin 69 (2): 367-393

one female with 150 ventrals) fall in the range of varia-

tion of E. /aticincta and present head and dorsal patterns

similar to those of the holotype of E. Jaticincta.

Elapsoidea semiannulata moebiusi (Werner, 1897)

Material: 16 specimens collected.

Localities: Baibokoum (14), Moissala (2).

Other specimens (MNHN): Fort Archambault (1),

Mayo-Kebbi (2).

Literature records: Gounou-Gaya (Roussel & Villiers

1965, as Elapsoidea decosteri moebiusi), Fort-Archam-

bault, Mayo-Kebbi (Broadley 1971, 1998).

Remarks: Males (n = 10) have 152—157 ventrals and the

only female 153. The number of pale bands range from

10 to 14 (body only), and from 11 to 17 when tail is in-

cluded. The head pattern of the youngest specimens is

not different of those of the two specimens we attributed

to E. laticincta and the holotype from Kadugli. Further

studies are needed to clarify the status of populations

attributed to these two taxa in Chad and neighbouring

countries of Central Africa.

Naja haje (Linnaeus, 1758)

Material: 22 specimens collected.

Localities: Baibokoum (3), Birim (2), Bitanda (2), Bitea

(1), Bon Amdaoud (3), Doureng (1), Mao (3), Masarma

(1), Matafo 2 (4), Moissala (1), Moundou (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Abéché, Fort-Lamy (Graber 1966).

Naja nigricollis Reinhardt, 1843

Material: 27 specimens collected.

Localities: Baibokoum (8), Bon Amdaoud (4), Fiengbac

(1), Goulmounbass (1), Laobida (2), Moissala (9), Zama-

gouin (2).

Other specimens (MNHN): Fort-Lamy (1), Mayo-Kebbi

(1);

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Abéché, Fort-Lamy (Graber 1966).

Naja nubiae Wister & Broadley, 2003

Material: no specimen collected.

Other specimens (MNHN): Nord du Mont Ennedi (1),

Ouadi Basso (1).

Literature records: Archei, Ennedi,

(Wuster & Broadley 2003, Trape 2015).

Oued Basso

Naja savannula Broadley, Trape, Chirio & Wuster, 2018

Material: 1 specimen collected.

Locality: Mboura near Baibokoum (1).

Literature record: Mboura (Wiuster et al. 2018).

Remarks: First record for Chad and easternmost record

for this West African savanna species (Wuster et al.

2018). A218 cm long specimen collected on the roof of a

hut located on the banks of the Mbéré River which sepa-

rates Chad from Cameroon.

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382

Naja subfulva Laurent, 1955

Material: 2 specimens collected.

Localities: Birim (1), Bitanda (1).

Other specimen (coll. MNHN): Dyintilo (1).

Literature records: Fort-Archambault (Graber 1966, as

Naja melanoleuca), Lac Tchad (Buffrénil 1992, as Naja

melanoleuca).

Remarks: The Birim specimen, on the northern edge of

Lake Chad near Bor, is the northernmost record for this

species (see Wuster et al. 2018).

Family Viperidae Oppel, 1811

Bitis arietans (Merrem, 1820)

Material: 8 specimens collected and 2 specimens ob-

served but non preserved.

Localities: Baibokoum (3), Bitea (1), Bon Amdaoud (1),

Matafo 2 (1), Moissala (2).

Sight record: Ouadi Sofoya (A. S. Dyiddi, unpublished).

Photographic record: near Torboul (A. S. Dyjiddi, unpub-

lished).

Other specimens (coll. MNHN): Bol (1), Maillao (2),

N’Dyjaména (1).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Abéché, Ati, Fort-Lamy (Graber 1966), Zakouma

(Dejace 2002).

Causus maculatus (Hallowell, 1842)

Material: 18 specimens collected.

Localities: Batbokoum (8), Bitanda (1), Bon Amdaoud

(8), Laobida (1).

Other specimens (coll. MNHN): Fort-Archambault (1),

Mayo-Kebbi (1), Niellim (4).

Literature records: Gounou-Gaya (Roussel & Villiers

1965), Chari, Mayo-Kebbi, Melfi, N’Djaména, Sarh

(Hughes 1977), see also square degree map of Rasmus-

sen (2005b).

Causus resimus (Peters, 1862)

Material: 28 specimens collected.

Localities: Bahar (2), Bon Amdaoud (1), Djarat Abouni-

mir (20), Mahargal (2), N’ Djaména Gassi (2), Tikem (1).

Other specimens (coll. MNHN): Bol (2), Chari (1),

Mayo-Kebbi (3), Maillao (10), N’Djaména (13), Niellim

(4).

Literature records: Mayo Kebbi (Roussel & Villiers

1965), Abéché, Ati, Fort-Foureau, Fort-Lamy (Gra-

ber 1966, as Causus rhombeatus), Chari, Mayo-Kebbi,

N’Dyjaména (Hughes 1977), see also square degree map

of Rasmussen (2005b).

Cerastes cerastes (Linnaeus, 1758)

Material: 3 specimens collected.

Localities: Faya Largeau (1), Ounianga Serir (1), Oum

Chalouba (1).

Bonn zoological Bulletin 69 (2): 367-393

Jean-Francois Trape et al.

Literature records: Aozou, Yebbi-Bou (Pellegrin 1935),

Ennedi, Bahr-el-Ghazal (Graber 1966), Aozou, Yeb-

bi-Bou, Fada (Trape 2015).

Cerastes vipera (Linaeus, 1758)

Material: no specimen collected.

Literature records: Tibesti (Graber 1966), Fada (Trape

2015).

Echis leucogaster Roman, 1972

Material: 40 specimens collected.

Localities: Arningmalik (4), Bahar (2), Bitea (7), Dou-

reng (2), Fada (2), Guirli (1), Kadam Digas (4), Mahargal

(10), Masarma (6), Mongo (1), Oum Chalouba (1).

Other specimens: Fada (1, coll. MNHN), 35 km SW of

Ati (1, coll. IRD).

Literature records: Abéché, Ouaddai, Bahr-el-Ghazal,

Bisneye, Zaghaoua (Graber 1966, as Echis carinatus),

between Bardai and Aozou (Beck & Huard 1969, as

Echis carinata), between Bardai and Aozou, Fada (Trape

2015).

Remarks: Most specimens have a clear uniform venter,

but some specimens with a spotted venter, at least on each

side of the ventrals, were collected in southeastern Chad

(6 of 13 specimens from Bahar, Guirli and Mahargal).

Meristic data were similar to those of unspotted speci-

mens. In West Africa, specimens of E. /eucogaster with

a spotted venter are not rare in western Mali and central

Senegal (Trape & Mané 2017). Pending for comprehen-

sive molecular studies including all the various taxa and

populations of the Echis pyramidum complex in Africa

we prefer to keep binominals for E. /eucogaster.

Echis romani Trape 2018

Material: 155 specimens collected.

Localities: Baibokoum (127), Bitanda (6), Fiengbac (1),

Goulmounbass (1), Laobida (14), Zamagouin (6).

Other specimens (coll. MNHN): Maillao (1), Mayo-Keb-

bi (1).

Literature records: Gounou-Gaya, Bongor (Roussel &

Villiers 1965, as Echis carinatus), Maillao, Mayo-Kebbi

(Hughes 1976, as Echis ocellatus), Baibokoum, Bitan-

da, Fiengbac, Goulmounbass, Laobida, Yambatchingsou,

Zamagouin (Trape 2018).

Remark: This recently described species of the Echis

ocellatus complex is currently known from Nigeria,

Cameroon, Chad, Central African Republic and Sudan

(Trape 2018, Trape unpublished).

DISCUSSION

The two most important previous collections of snakes

from Chad covered both Sudanese (Roussel & Villiers

1965) and Sahelian (Graber 1966) areas of the country.

When adding museum specimens mentioned in works

©ZFMK

The snakes of Chad

on certain genera or species, or on the snake fauna of

the Saharan part of the country, the number of snakes

from Chad mentioned in the literature totalized about

700 specimens belonging to 56 species. We deleted ten

of these species (Tricheilostoma bicolor, Boaedon linea-

tus, Boaedon fuliginosus, Grayia tholloni, Lycophidion

irroratum, Psammophis schokari, Psammophis sibilans,

Psammophis phillipsi, Naja melanoleuca and Echis ocel-

latus) and reattributed the corresponding specimens to

the following species: Tricheilostoma sundewalli, Boae-

don longilineatus, Boaedon subflavus, Grayia smithii,

Lycophidion semicinctum, Psammophis aegyptius,

Psammophis rukwae, Naja subfulva and Echis romani.

Among the 1,512 specimens we collected, 66 species

were represented, including 27 species that have not

been reported before from Chad: Letheobia weildholzi,

Myriopholis occipitalis, Tricheilostoma sundewalli,

Crotaphopeltis hippocrepis, Dasypeltis sahelensis,

Natriciteres olivacea, Platyceps florulentus, Telescopus

tripolitanus, Aparallactus lunulatus — nigrocollaris,

Atractaspis dahomeyensis, Atractaspis micropholis,

Boaedon longilineatus, Boaedon paralineatus, Boaedon

perisilvestris, Boaedon subflavus, Lycophidion aff.

capense, Malpolon moilensis, Micrelaps_ vaillanti,

Prosymna ambigua, Prosymna greigerti, Psammophis

afroccidentalis, Psammophis elegans, Psammophis

mossambicus, Psammophis sudanensis, Rhamphiophis

rostratus, Echis romani, and Naja savannula. In addition,

we found in the MNHN collection one specimen of

Spalerosophis diadema cliffordi, another species not

reported before from Chad. Currently, 80 snake species

are known from Chad.

As expected, the richest snake fauna was observed in

the southern part of the country (07°30’N / 09°00’N)

where vegetation 1s Sudano-Congolese with annual rain-

fall reaching 1,100—1,300 mm and where 44 species were

collected and one additional species is known (Table 3).

In a radius of approximately 20 km around Baibokoum

(average rains 1,200 mm according to Mahé et al.[2012]),

villagers collected within ten days a total of 505 speci-

mens belonging to 40 species, one of the richest snake

fauna for an African savanna area (Fig 8). At Bandafas-

Si in southeastern Senegal (average rains: 1,100 mm)

and Mamoroubougou in southern Mali (average rains:

1,000 mm), two Sudan savanna area where 1,282 and

1,064 snakes were collected, 35 and 36 species were rep-

resented, respectively (Trape & Mané 2004, 2017).

The most abundant species south of 09°00’N, each

one representing at least 5% of the snakes collected,

were Echis romani, Boaedon subflavus, Pasmmophis

mossambicus, Rhamphiophis oxyrhynchus, Boaedon

paralineatus and Psammophis rukwae. The most re-

markable species were Prosymna ambigua and Boaedon

perisilvestris (northernmost limit of these wet Congolese

savanna species), Atractaspis dahomeyensis and Naja

savannula (easternmost limit of these West African sa-

Bonn zoological Bulletin 69 (2): 367-393

383

vanna species), and Letheobia weildholzi and Myriop-

holis occipitalis (rare new species). At Baibokoum the

most abundant species was the deadly viper Echis roma-

ni which represented 31% of the snakes collected. The

number and proportion of specimens of E. romani could

have been even higher since after a few days we asked

the villagers to stop collecting this species. Interesting-

ly, E. romani was found only in southwestern Chad and

its eastern limit in Chad and Central African Republic is

approximately 17°E (Chirio & Ineich 2006, Trape 2018).

In Chad this limit corresponds to the seasonnaly flooded

plains of the Logone and Chari rivers system. Howev-

er, eastward E. romani 1s also widely distributed in the

Kordofan province of Sudan (T. Mazuch, personnal com-

munication, 2019).

Between 09°00’N and 11°00’N, an area of Sudan sa-

vanna, a total of 36 species were collected and eleven

additional species are known (Table 3). The most abun-

dant species were Psammophis lineatus, Psammophis

sudanensis, Psammophis rukwae, Boaedon subflavus,

Echis romani and Crotaphopeltis hotamboeia. The most

remarkable species was Micrelaps vaillanti, a species

previously known only from East Africa and Sudan.

Between 11°00’N and 15°00’N the climate and vege-

tation are typically Sahelian. A total of 31 species were

collected and ten additional species are known (Table 3).

The most abundant species were Psammophis sudanen-

sis, Psammophis rukwae, Crotaphopeltis hotamboeia,

Atractaspis watsoni, Boaedon subflavus and Echis leu-

cogaster. The abundance of Crotaphopeltis hotamboe-

ia was associated to the seasonally flooded areas of the

Salamat province where Crotaphopeltis hippocrepis,

Crotatopheltis degeni and Causus resimus — three other

amphibian eaters — were also common. Interesting spe-

cies were Rhamphiophis rostratus, Platyceps florulentus,

Psammophis elegans univittatus, Atractaspis micropho-

lis and Natriciteres olivacea, which all present important

range extensions.

North of 15°00’N the climate and vegetation are Sahe-

lo-Saharan or Saharan. Our investigations were limited

and we collected or observed only four of the 13 species

that are known in this area where little data is available

(Trape 2015). The most common species is Echis leuco-

gaster which occurs both in Ouaddai, Ennedi and Tibes-

ti. Cerastes cerastes 1s also a common species. Probably

additional species, both Sahelian and Saharan, occur in

northern Ouaddai which has never been investigated.

Bauer et al. (2017) recently reviewed the reptile fauna

of Libya. In the two Saharan provinces of Libya closest

from Chad (Murzuq and Kufrah), nine species of snakes

have been reported, including six species also known

from northern Chad (Platyceps saharicus, Spaleroso-

phis diadema cliffordi, Malpolon moilensis, Psammophis

aegyptius, Cerastes cerastes and Cerastes vipera), one

palearctic species absent from Chad (Malpolon insigni-

tus), One species probably present in Chad but not col-

©ZFMK

384

Jean-Francois Trape et al.

Table 3. Latitudinal distribution of snakes in Chad (our study, 1,512 specimens collected). The 14 species not collected during

our study are indicated by a black square (m) with the number of MNHN or literature specimens in brackets. Black triangle (A)

indicates latitudinal occurrence of literature or MNHN specimens when not present at the same latitude in our collection. Latitudes

of northernmost records are based on whole data.

* Additional number of species when including literature data and MNHN collection are mentioned in parentheses.

Species TN 8°N 9°N 10°N 11°N 12°N 13°N 14°N >15°N Total Northernmost

record in Chad

Platyceps saharicus 0 0 0 0 0 0 0 0 m(3) (3) 21°48’N

Cerastes cerastes 0 0 0 0 0 0 0 A 3 3 21°48’N

Psammophis aegyptius 0 0 0 0 O m1) m(2) wml) am(1) (5) 21°34’N

Echis leucogaster 0) 0) 0 0) 4 20 9 4 3 40 21°30°N

Cerastes vipera 0 0 0 0 0 0 0 0 m2) w(2) 21°20’N

Myriopholis lanzai 0 0 0 0 0 0 0 0 ml) m1) 17°55’N

Malpolon moilensis 0 0) 0 0 0 0 0) 0) 2 2 17°327N

Naja nubiae 0 0 0 0 0 0 0 0 m(3) (3) 17°30°N

Telescopus obtusus 0 0 0 0 0 0 0 0 ml) m1) 17°12’N

Eryx colubrinus 0 0) 0 0 0 4 11 A A 15 16°32’N

Bitis arietans 3 2 A l A A 2 0) 2 10 15°S57°N

Psammophis rukwae 30 0 7 21 46 39 we 0 A 160 15°48°N

Spalerosophis diadema 0 0 0 0 0 0 0 0 ml) «m(1) 15°22’N

Eryx muelleri 0) 0 A A 0) 9 A A 0 9 14°30’N

Psammophis afroccidentalis 0 0 0 0 0 0 0 1 0 l 14°08’N

Psammophis elegans 6 0 0) 7 1 0) 0) 2 0) 16 14°08°N

Naja haje 3 4 A fs! 0 1 8 3 0) 2? 14°08’N

Platyceps florulentus 0 0 0 0 0 0 5 1 0 6 14°02’N

Atractaspis micropholis 0 0) 0) 0) 0) 0) 1 1 0) 2 14°02’N

Psammophis sudanensis 16 0) 4 30 60 21 3] 4 O 176 14°02’N

Boaedon subflavus 60 8 9 16 9 12 1] 0) O 125 13°54’N

Naja nigricollis 8 9 5 5 0) A A 0) 0) 27 13°50’°N

Meizodon semiornatus 0 0 0 0 0 1 A 0 0 1 13°50’N

Lycophidion taylori 0) 0) 0) 0) 1 1 0) 0) 0) 2 13°50’N

Prosymna collaris 0) 1 4 0) 1 4 A 0) 0 10 13°50’N

Atractaspis watsoni 0) 0) vi =) 26 7 1] 0 0) 56 13°30’N

Rhamphiophis rostratus 0) 0) 0) 0) 0) 0) 1 0) 0) 1 13°30’N

Myriopholis boueti 0 0 0 3 1 4 l 0 0 9 13°30’N

Python sebae 0) 0) 1 0) 4 0) 2 0) 0) 7 13°30’N

Telescopus tripolitanus 0 0) 0) 9 0) 1 2 0) 0) 12 13°30’N

Dasypeltis gansi 8 2 4 0 0 0 A 0 0 14 13°28’N

Causus resimus 0) 0) 2 1 20 5 A 0) 0) 28 13°28°N

Natriciteres olivacea 0) 0) 0 0 0 0 1 0) 0) 1 13°26’N

Naja subfulva 0) 1 A 0 0) 0) 1 0) 0) 2 13°26’N

Crotaphopeltis hotamboeia 18 7 3 17 56 2 A 0 hi 122 13°13°N

Dasypeltis sahelensis 0 0) 0) 2 2 3 0) 0 0 wi 12°40’°N

Afrotyphlops punctatus 9 2 1 3 0) 0) 0) 0) 0) 15 12°40’°N

Boaedon longilineatus 0) 0) 3 4 7 4 0 0) 0) 18 12°33’N

Micrelaps vaillanti 0) 0 0 5 0 2 0) 0) 0 w 12°07°N

Afrotyphlops lineolatus 0 0 0 O m(2) m(2) 0 0 O m(4) 12°06’N

Crotaphopeltis degeni 0) 0) 2 13 7 1 0) 0) 0 23 12°06’N

Scaphiophis albopunctatus 6 0) 3 2 0) A 0) 0) 0 1] 12°06’N

Hemirhagerrhis nototaenia 1 0) A 1 0 0) 0) 0) 0 2 12°06’N

Psammophis lineatus 15 2 5 42 0 A 0 0 0 64 12°06’N

Causus maculatus 8 1 1 8 A A 0) 0) 0) 18 12°06’N

Philothamnus irregularis 18 0) 4 0) 0 A 0) 0) 0 22 12°06’N

The snakes of Chad

Table 3. continued.

—

Rhamphiophis oxyrhynchus 21

Prosymna greigerti 4

Philothamnus aff. semivariegatus 1

Echis romani 127

Crotaphopeltis hippocrepis

Psammophis praeornatus

Lycophidion aff. capense

Myriopholis adleri

Python regius

Amblyodipsas unicolor wy)

Meizodon coronatus 3

Tricheilostoma sundewalli 1

Dasypeltis confusa 2

Dispholidus typus 5

Grayia smithii 0

Telescopus variegatus 3

Limaformosa crossi 10

Lycophidion semicinctum 8

—

ON rr Or OO OF CO OCOCOCOlUOCULr KKCLCUCOCUWNN NY

Elapsoidea semiannulata 14

Meizodon regularis 0

Psammophis mossambicus 41 14 6

Boaedon paralineatus 3

Atractaspis aterrima

Philothamnus bequaerti

Philothamnus hughesi

Myriopholis occipitalis

Prosymna ambigua

Elapsoidea laticincta

Letheobia weildholzi

Aparallactus lunulatus

Atractaspis dahomeyensis

Boaedon perisilvestris

Gonionotophis granti

Naja savannula

1oS)

Rare NOP HBR NTT OF OK

oOo 2.°Oo 2 2] O:&> =

SS OOS CO OS - OS - -S

Number of specimens 505 112 Il 214

Number of species 40 28 # £26 25

Cumulated number of species 44 36

by ecoregion* (+1) (+12)

385

3 1 0 0 0 55 12°06’N

6 4 0 0 0 17 12°03’N

0 0 0 0 0 3 11°35°N

A 0 0 0 0 155 11°35°N

11 0 0 0 0 14 11°O1’N

0 0 0 0 O m(2) 10°53’N

0 0 0 0 0 3 10°41’N

0 0 0 0 O m(3) 10°16’°N

0 0 0 0 0 6 10°16’N

0 0 0 0 0 4 09°47°N

0 0 0 0 0 4 09°37°N

0 0 0 0 0 l 09°37°N

0 0 0 0 0 2 09°37°N

0 0 0 0 0 6 09°37°N

0 0 0 0 O m(2) 09°37°N

0 0 0 0 0 14 09°37°N

0 0 0 0 0 12 09°37°N

0 0 0 0 0 20 09°37°N

0 0 0 0 0 16 09°37°N

0 0 0 0 O m(1) 09°29"N

0 0 0 0 0 61 09°13’°N

0 0 0 0 0 34 09°12’N

0 0 0 0 O m(1) 09°08’N

0 0 0 0 0 2 09°08’N

0 0 0 0 O m(1) 08°30’N (?)

0 0 0 0 0 1 08°20’N

0 0 0 0 0 2 07°55’N

0 0 0 0 0 1 07°44°N

0 0 0 0 0 4 07°44’N

0 0 0 0 0 2. 07°44’N

0 0 0 0 0 1 07°44’N

0 0 0 0 0 1 07°35°N

265 165 ~~ 114 16 10 1512

18 21 16 7 3 66

31 4 66

(+10) (+9) (414)

lected until now (Lytorhynchus diadema) and one spe-

cies with doubtfull mentions from Chad and southeastern

Libya (Psammophis schokari). Interestingly, no Echis

species has been reported from Murzuk and Kufrah dis-

tricts (Bauer et al. 2017).

Compared to Niger (51 species) and Mali (65 species)

(Trape & Mané 2015, 2017), two other large African

countries extending both in the Sahara, Sahel and Sudan

savanna, the snake fauna of Chad appears more diversi-

fied. Of 103 taxa (101 species and two additional sub-

species) known in at least one of these three countries,

Bonn zoological Bulletin 69 (2): 367-393

only 45 (43.7 %) were reported both from Mali and Chad

(Table 4). Among the other taxa, 28 taxa known in Chad

but not in Mali are typical Central African species or

East African “invaders” (Hughes 1985), 16 taxa known

in Mali but not in Chad are typical West African species,

and 15 taxa, including two taxa reported only from Niger

(Myriopholis cairi and Litorhynchus diadema), were not

collected in Chad (three taxa) or in Mali (14 taxa) proba-

bly or possibly due to unsufficient sampling.

Compared to Cameroon (Chirio & Lebreton 2007), all

species known from this country north of 08°N were also

©ZFMK

386

Jean-Francois Trape et al.

Table 4. Comparison of the snake fauna of Chad, Niger and Mali. Data for Niger and Mali are from Trape & Mané (2015, 2017).

Species

Afrotyphlops lineolatus

Afrotyphlops punctatus

Letheobia weildholzi

Myriopholis adleri

Myriopholis algeriensis

Myriopholis boueti

Myriopholis cairi

Myriopholis lanzai

Myriopholis occipitalis

Rhinoguinea magna

Rhinoleptus koniagui

Tricheilostoma bicolor

Tricheilostoma sundewalli

Eryx colubrinus

Eryx muelleri

Python regius

Python sebae

Afronatrix anoscopus

Bamanophis dorri

Crotaphopeltis degeni

Crotaphopeltis hippocrepis

Crotaphopeltis hotamboeia

Dasypeltis confusa

Dasypeltis gansi

Dasypeltis latericia

Dasypeltis sahelensis

Dispholidus aff. typus

Grayia smithii

Litorhynchus diadema

Meizodon coronatus

Meizodon regularis

Meizodon semiornatus tchadensis

Natriciteres olivacea

Philothamnus bequaerti

Philothamnus hughesi

Philothamnus irregularis

Philothamnus aff. semivariegatus

Platyceps florulentus

Platyceps saharicus

Scaphiophis albopunctatus

Spalerosophis diadema cliffordi

Chad Niger Mali

x x KK

x x KK MK

x Kx x

x mK MRK KK KK KM

Bonn zoological Bulletin 69 (2): 367-393

x x Ke

x x Ke MK

x x KK MK

a a oe as

Species

Telescopus obtusus

Telescopus tripolitanus

Telescopus variegatus

Amblyodipsas unicolor

Aparallactus lunulatus nigrocollaris

Atractaspis aterrima

Atractaspis dahomeyensis

Atractaspis micropholis

Atractaspis watsoni

Boaedon fuliginosus

Boaedon lineatus

Boaedon longilineatus

Boaedon paralineatus

Boaedon perisilvestris

Boaedon subflavus

Gonionotophis granti

Hemirhagerrhis nototaenia

Limaformosa crossi

Lycophidion aff. capense

Lycophidion albomaculatum

Lycophidion irroratum

Lycophidion semicinctum

Lycophidion taylori

Malpolon moilensis

Micrelaps vaillanti

Polemon neuwiedi

Prosymna ambigua

Prosymna collaris

Prosymna greigerti

Psammophis aegyptius

Psammophis afroccidentalis

Psammophis elegans elegans

Psammophis elegans univittatus

Psammophis lineatus

Psammophis mossambicus

Psammophis phillipsi

Psammophis praeornatus gribingu-

1ensis

Psammophis praeornatus praeor-

natus

Psammophis rukwae

Psammophis schokari

x mK KR KM KK MK

x x Ke MK x mK KK KK MK

x xm KK KK KK MK

x x Ke

x x KK MK

Chad Niger Mali

x x Km KK

©ZFMK

The snakes of Chad 387

Table 4. Continued.

Species Chad Niger Mali

Psammophis sudanensis x x

Rhamphiophis oxyrhynchus xX xX x

Rhamphiophis rostratus xX

Elapsoidea laticincta xX

Elapsoidea semiannulata moebiusi xX xX xX

Naja haje x xX xX

Naja katiensis xX

Naja nigricollis xX xX xX

Naja nubiae xX xX

Naja savannula xX xX xX

Naja senegalensis x x

Naja subfulva xX

Bitis arietans x x x

Causus maculatus xX xX xX

Causus resimus xX

Cerastes cerastes x x x

Cerastes vipera xX x xX

Echis jogeri xX

Echis leucogaster xX xX xX

Echis ocellatus x x

Echis romani xX

collected in Chad, with the exception of only three spe-

cies: Psammophylax togoensis, which is rare in West and

Central Africa, Naja katiensis, a species common in the

West African Sudan savanna but reaching its eastern lim-

it in Cameroon near the Nigerian border, and Philotham-

nus heterodermus, a forest species with a single record

in Cameroon north of 08°N (Chirio & LeBreton 2007).

A fourth species not found in Chad, Afronatrix anosco-

pus, was mapped in error from northern Cameroon by

these authors (M. LeBreton, pers. comm.), then by Chip-

paux & Jackson (2019). Likewise, when excluding Sa-

helo-Saharan species, most species distributed in Chad

are also known from Cameroon, with only four species

likely to reach their westernmost limit in central Chad:

Myriopholis occipitalis, Micrelaps vaillanti, Rhamphio-

Dhis rostratus and Lycophidion taylori.

Snakes presenting a high risk of death for humans in

case of bite were distributed in all regions of the coun-

try and represented 17.7 % of the total number of snakes

collected. They belonged to (a) four viperid species:

Echis romani (10.3 %), Echis leucogaster (2.6 %), Bitis

arietans (0.6 %), and Cerastes cerastes (0.2 %), (b) four

elapid species: Naja nigricollis (1.8 %), Naja haje (1.5

Bonn zoological Bulletin 69 (2): 367-393

%), Naja subfulva (0.1 %) and Naja savannula (0.1 %),

and (c) one colubrid species: Dispholidus aff. typus (0.4

%). Atractaspids (4.1 %), in particular Atractaspis wat-

soni, were also common and they are known to be occa-

sionally responsible for fatal envenomations (Spawls &

Branch 2020). The distribution of Echis romani appears

limited to the southwest of the country where it 1s clear-

ly a major medical problem. Several dozens of cases of

Echis romani bites are hospitalized each year at Baibok-

oum. Although antivenoms were provided to district

hospitals by the Ministry of Health, until recently they

were not adapted to the species of snakes encountered in

Chad (they were manufactured in India where non-afri-

can snakes were used in their production) and modalities

of administration were often unsatisfactory, with unsuf-

ficient dosage in case of severe envenomation. In Chad

as in other countries of tropical Africa there is an urgent

need to improve access to effective antivenoms and to

train health workers for adequate management of snake-

bite.

Acknowledgements. We are grateful to the Chad Ministry of

Public Health for its logistic and financial support. We address

our warmest thanks to Dr Matckoké Gong-Zoua who strong-

ly advocated the project, judiciously selected Baibokoum for

our first survey, and closely followed up the advancement of

research.

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APPENDIX I

List of collected specimens, locality, and collection

number (IRD Dakar and PNLP N’Djaména)

Afrotyphlops punctatus. Baibokoum: 2051.N, 2151.N,

2258.N, 2259.N, 2261.N, 2296.N, 2303.N, 2304.N, 2305.N;

Bitanda: 2605.N; Bon Amdaoud: 1967.N, 3041.N, 3066.N;

Moundou (Belaba): 2622.N; Zamagouin: 2561.N.

Amblyodipsas unicolor. Baibokoum: 2209.N, 2286.N; Mois-

sala: 2710.N; Tikem (Goundwaye): 2555.N.

Aparallactus lunulatus nigrocollaris. Baibokoum: 2158.N,

2178.N, 2366.N, 2403.N.

Atractaspis dahomeyensis. Baibokoum: 2197.N, 2278.N,

2293.N, 2307.N.

Atractaspis micropholis. Arningmalik: 1833.N; Gourounga-

li: 1873.N.

Atractaspis watsoni. Bahar: 2987.N, 2988.N, 3003.N; Bala-

ni: 2523.N, 2565.N.; Bitea: 1843.N, 1854.N, 1863.N, 1866.N,

2877.N, 2878.N, 2896.N, 2897.N, 2928.N, 2929.N, 2930.N;

Bon Amdaoud: 3056.N, 3061.N, 3113.N; Djarat Abounimir:

1938.N, 3138.N, 3139.N, 3140.N, 3157.N, 3158.N, 3159.N,

3165.N, 3166.N; Goulmounbass: 2649.N; Guirli: 2921.N;

Hileborno: 3274.N, 3275.N, 3276.N; Kadam Digas: 1822.N,

1823.N, 2826.N, 2827.N, 2830.N, 2836.N, 2837.N, 2841.N,

2845.N, 2854.N, 2856.N, 2858.N, 2859.N, 2863.N; Kiéké:

3033.N; Mahargal: 2939.N, 2940.N; Masarma: 2821.N;

Zamagouin: 2517.N, 2526.N, 2539.N, 2743.N, 2748.N.

Bitis arietans. Baibokoum: 2052.N, 2372.N, 2422.N; Bitea:

2911.N; Bon Amdaoud: 3047.N; Matafo 2: 2788.N; Moissa-

la: 3277.N, 3278.N.

Boaedon longilineatus. Bahar: 2977.N; Bon Amdaoud:

3068.N, 3085.N; Djarat Abounimir: 1939.N, 3155.N, 3156.N,

3160.N, 3161.N, 3162.N; Fiengbac: 2521.N, 2553.N; Goul-

mounbass: 2626.N, 2627.N; Hileborno: 2923.N; Masarma:

2809.N, 2818.N, 2823.N; Zamagouin: 2558.N.

Boaedon paralineatus. Baibokoum: 2012.N, 2015.N, 2016.N,

2018.N, 2028.N, 2029.N, 2069.N, 2074.N, 2081.N, 2089.N,

2094.N, 2111.N, 2113.N, 2117.N, 2138.N, 2153.N, 2155.N,

2159.N, 2160.N, 2162.N, 2164.N, 2184.N, 2194.N, 2206.N,

2208.N, 2217.N, 2243.N, 2311.N, 2315.N, 2338.N, 2505.N;

Bitanda: 2575.N, 2576.N, 2606.N.

Boaedon perisilvestris. Baibokoum: 2143.N, 2191.N.

Boaedon subflavus. Bahar: 1892.N, 2984.N, 2986.N, 3007.N,

3008.N, 3009.N, 3010.N, 3015.N; Baibokoum: 2004.N,

2009.N, 2017.N, 2027.N, 2030.N, 2044.N, 2045.N, 2046.N,

2047.N, 2049.N, 2050.N, 2055.N, 2082.N, 2086.N, 2090.N,

2102.N, 2105.N, 2108.N, 2109.N, 2110.N, 2116.N, 2144.N,

2154.N, 2161.N, 2163.N, 2165.N, 2166.N, 2181.N, 2182.N,

2187.N, 2188.N, 2189.N, 2196.N, 2198.N, 2199.N, 2200.N,

2207.N, 2212.N, 2214.N, 2247.N, 2248.N, 2275.N, 2284.N,

2287.N, 2317.N, 2323.N, 2324.N, 2325.N, 2333.N, 2339.N,

2360.N, 2362.N, 2367.N, 2370.N, 2387.N, 2388.N, 2391.N,

2399.N, 2400.N, 2401.N; Balani: 2566.N, 2567.N; Bitanda:

Bonn zoological Bulletin 69 (2): 367-393

2578.N, 2587.N, 2601.N, 2603.N, 2614.N; Bitea: 1835.N,

1837.N, 1844.N, 1846.N, 1857.N, 1871.N, 2875.N, 2879.N,

2898.N, 2906.N; Bon Amdaoud: 1946.N, 1951.N, 1956.N,

1959.N, 1960.N, 1964.N, 3048.N, 3057.N, 3058.N, 3070.N,

3094.N, 3106.N, 3116.N, 3121.N, 3123.N; Doureng: 2865.N;

Goulmounbass: 2629.N; Kadam Digas: 2773.N, 2829.N,

2833.N, 2839.N, 2848.N, 2849.N, 2850.N, 2857.N, 2864.N;

Laobida: 2729.N, 2731.N; Laobida (Malgandi): 2571.N;

Laobida (Yamba-Tchangsou): 2518.N; Mahargal: 2935.N,

2965.N, 2966.N, 2967.N; Moundou: 2618.N, 2623.N; Moun-

dou (Belaba): 2624.N; Tikem: 2520.N; Zamagouin: 2741.N,

271 IN

Causus maculatus. Baibokoum: 2021.N, 2048.N, 2070.N,

2099.N, 2213.N, 2239.N, 2255.N, 2310.N; Bitanda: 2579.N;

Bon Amdaoud: 3049.N, 3050.N, 3077.N, 3081.N, 3089.N,

3096.N, 3104.N, 3111.N; Laobida (Malgandi): 2515.N.

Causus resimus. Bahar: 2989.N; Balani: 2536.N; Bon Amd-

aoud: 3069.N; Djarat Abounimir: 1903.N, 1908.N, 1910.N,

1923.N, 1924.N, 1930.N, 1941.N, 3126.N, 3127.N, 3128.N,

3129.N, 3130.N, 3131.N, 3132.N, 3133.N, 3141.N, 3167.N,

3168.N, 3169.N, 3170.N; Mahargal: 1874.N, 1886.N;

N’Djaména Gassi: 1993.N, 2789.N; Tikem (Goundwaye):

2537.N.

Cerastes cerastes. Faya Largeau: 2779.N; Oum Chalouba

(Houk): 3280.N; Ounianga Sérir: 2777.N.

Crotaphopeltis degeni. Djarat Abounimir: 3142.N, 3143.N,

3144.N, 3145.N, 3146.N, 3163.N, 3164.N; Fiengbac: 2564.N;

Goulmounbass: 2638.N, 2639.N, 2640.N, 2641.N, 2642.N,

2643.N, 2644.N, 2645.N, 2646.N, 2647.N, 2648.N:; Kiéké:

3032.N, 3039.N; N’Djaména: 3281.N; Tikem: 2510.N.

Crotaphopeltis hippocrepis. Baibokoum: 2041.N, 2076.N; Bi-

tanda: 2590.N; Djarat Abounimir: 1901.N, 1905.N, 1906.N,

1907.N, 1909.N, 1917.N, 1920.N, 1925.N, 1926.N, 1931.N,

1940.N.

Crotaphopeltis hotamboeia. Bahar: 2991.N, 2992.N, 2993.N,

2994.N, 2995.N, 2996.N, 2997.N, 2998.N, 2999.N, 3000.N,

3001.N, 3002.N, 3004.N, 3005.N, 3006.N, 3011.N, 3012.N,

3013.N; Baibokoum: 2024.N, 2125.N, 2152.N, 2201.N,

2219.N, 2257.N, 2262.N, 2328.N, 2350.N, 2358.N, 2361.N,

2364.N, 2368.N, 2389.N, 2395.N, 2397.N, 2402.N, 2420.N;

Bitanda: 2592.N, 2593.N, 2615.N; Bon Amdaoud: 1953.N,

1954.N, 1961.N, 2760.N, 3055.N, 3062.N, 3073.N, 3098.N,

3114.N, 3124.N; Djarat Abounimir: 1915.N, 1935.N, 3147.N,

3148.N, 3229.N, 3230.N, 3231.N, 3232.N, 3233.N, 3234.N,

3235.N, 3236.N, 3237.N, 3238.N, 3239.N, 3240.N, 3241.N,

3242.N, 3243.N, 3244.N, 3245.N, 3246.N, 3247.N, 3248.N,

3249.N, 3250.N, 3251.N, 3252.N, 3253.N, 3254.N, 3255.N,

3256.N, 3257.N, 3258.N, 3259.N, 3260.N, 3261.N, 3262.N,

3263.N, 3264.N, 3265.N, 3266.N, 3267.N, 3268.N, 3269.N,

3270.N, 3271.N, 3272.N; Goulmounbass: 2630.N; Hilebor-

no: 1898.N; Kadam Digas: 2765.N, 2774.N, 2828.N, 2835.N,

2844.N, 2852.N, 2860.N; Kiéké: 3023.N, 3024.N, 3026.N,

3029.N, 3031.N, 3035.N; Laobida: 2525.N, 2732.N; Ma-

hargal: 1875.N, 2964.N, 2968.N; Moissala: 1990.N, 3282.N,

3313.N; Moundou: 2621.N.; Zamagouin: 2742.N.

Dasypeltis confusa. Baibokoum: 2142.N, 2290.N.

©ZFMK

The snakes of Chad 391

Dasypeltis gansi. Baibokoum: 2008.N, 2167.N, 2168.N,

2218.N, 2266.N, 2270.N, 2343.N, 2347.N; Laobida: 2548.N,

2549.N; Moissala: 3283.N, 3284.N; Zamagouin: 2559.N,

2754.N.

Dasypeltis sahelensis. Bon Amdaoud: 3074.N; Goulmoun-

bass: 2650.N; Guirli: 2918.N; Kadam Digas: 1824.N, 1826.N;

Mahargal: 2936.N; N’Djaména: 3285.N.

Dispholidus aff. typus. Baibokoum: 2061.N, 2106.N, 2185.N,

2297.N, 2376.N; Moissala: 1988.N.

Echis leucogaster. Arningmalik: 1830.N, 1834.N, 2873.N,

2874.N; Bahar: 1896.N, 2990.N; Bitea: 1848.N, 1856.N,

1868.N, 1870.N, 2900.N, 2901.N, 2910.N; Doureng: 1829.N,

2867.N; Fada: 3287.N, 3288.N:; Guirli: 2920.N; Kadam Di-

gas: 2766.N, 2776.N, 2846.N, 2853.N; Mahargal: 1877.N,

1883.N, 1885.N, 1887.N, 2958.N, 2959.N, 2960.N, 2961.N,

2962.N, 2963.N; Masarma: 1808.N, 2812.N, 2817.N, 2822.N,

2824.N, 2825.N; Mongo (vicinity): 2508.N; Oum Chalouba:

3286.N.

Echis romani. Baibokoum: 2011.N, 2013.N, 2014.N, 2026.N,

2034.N, 2035.N, 2038.N, 2039.N, 2042.N, 2043.N, 2057.N,

2078.N, 2079.N, 2080.N, 2085.N, 2096.N, 2100.N, 2101.N,

2115.N, 2124.N, 2126.N, 2127.N, 2128.N, 2133.N, 2134.N,

2135.N, 2139.N, 2140.N, 2141.N, 2157.N, 2169.N, 2176.N,

2190.N, 2230.N, 2268.N, 2272.N, 2318.N, 2322.N, 2331.N,

2332.N, 2334.N, 2335.N, 2336.N, 2337.N, 2351.N, 2354.N,

2357.N, 2373.N, 2423.N, 2424.N, 2425.N, 2426.N, 2427.N,

2428.N, 2429.N, 2430.N, 2431.N, 2432.N, 2433.N, 2434.N,

2435.N, 2436.N, 2437.N, 2438.N, 2439.N, 2440.N, 2441.N,

2442.N, 2443.N, 2444.N, 2445.N, 2446.N, 2447.N, 2448.N,

2449.N, 2450.N, 2451.N, 2452.N, 2453.N, 2454.N, 2455.N,

2456.N, 2457.N, 2458.N, 2464.N, 2465.N, 2466.N, 2467.N,

2468.N, 2469.N, 2470.N, 2471.N, 2472.N, 2473.N, 2474.N,

2475.N, 2476.N, 2477.N, 2478.N, 2479.N, 2480.N, 2481.N,

2482.N, 2483.N, 2484.N, 2485.N, 2486.N, 2487.N, 2488.N,

2489.N, 2490.N, 2491.N, 2492.N, 2493.N, 2494.N, 2495.N,

2496.N, 2497.N, 2498.N, 2499.N, 2500.N, 2501.N, 2502.N,

2503.N, 2504.N, 2506.N, 2507.N; Bitanda: 2573.N, 2583.N,

2586.N, 2595.N, 2609.N, 2610.N; Fiengbac: 2562.N: Goul-

mounbass: 2628.N: Laobida: 2550.N, 2713.N, 2717.N,

2720.N, 2724.N, 2725.N, 2727.N, 2728.N, 2730.N, 2733.N,

2734.N; Laobida (Berete): 2545.N; Laobida (Yamba-Ma-

loum): 2546.N; Laobida (Yamba-Tchangsou): 2547.N; Zama-

gouin: 2542.N, 2543.N, 2544.N, 2560.N, 2740.N, 2746.N.

Elapsoidea laticincta. Batbokoum: 2215.N, 2302.N.

Elapoisea semiannulata moebuisi. Baibokoum: 2031.N,

2071.N, 2174.N, 2210.N, 2227.N, 2237.N, 2274.N, 2282.N,

2291.N, 2295.N, 2299.N, 2300.N, 2301.N, 2346.N; Moissala:

1992.N, 3289.N.

Eryx colubrinus. Birim: 2791.N, 2792.N; Bitea: 1838.N,

1845.N; Doureng: 2869.N, 2895.N, 3019.N; Gouroungali:

1872.N; Guirli: 2914.N, 2915.N, 2916.N, 2917.N; Matafo 2;

2784.N; Tarhacha: 2903.N, 2904.N .

Eryx muelleri: Masarma: 1802.N, 1803.N, 1805.N, 1810.N,

2810.N, 2811.N, 2814.N, 2815.N, 2819.

Gonionotophis granti. Baibokoum: 2195.N.

Bonn zoological Bulletin 69 (2): 367-393

Hemirhagerrhis nototaenia. Baibokoum: 2065.N; Kiéké:

3030.N.

Letheobia weildhozi. Baibokoum: 2285.N.

Limaformosa crossi. Baibokoum: 2007.N, 2060.N, 2084.N,

2107.N, 2249.N, 2319.N, 2352.N, 2353.N, 2359.N, 2385; Bi-

tanda: 2612.N; Zamagouin: 2738.N.

Lycophidion aff. capense. Bon Amdaoud: 3045.N, 3059.N;

Kiéké: 3037.N.

Lycophidion semicinctum. Baibokoum: 2019.N, 2216.N,

2273.N, 2276.N, 2277.N, 2288.N, 2306.N, 2419.N; Bitan-

da: 2572.N, 2574.N, 2611.N; Laobida: 2735.N:; Moissala:

1980.N, 1982.N, 2709.N, 3292.N, 3293.N, 3294.N, 3295.N,

3312.N.

Lycophidion taylori. Bahar: 2985.N; Hileborno: 2924.N.

Malpolon moilensis Ennedi (17°32’N / 21°29’E): 3309.N;

Ouadi Haouach: 3296.N.

Meizodon coronatus. Baibokoum: 2010.N, 2246.N, 2250 N;

Laobida: 2535.N.

Meizodon semiornatus tchadensis. Bahar. 2969.N.

Micrelaps vaillanti. Bon Amdaoud: 3075.N, 3115.N, 3117.N,

3122; Kiéké: 3034.N; Mahargal: 2937.N, 2938.N.

Mpyriopholis boueti. Bahar: 2932.N, 2933.N, 2934; Béréguit

(vicinity of): 2778.N; Bitea: 1865.N; Bon Amdaoud: 1944.N,

3110.N; Guirli: 2919.N; Kiéké: 3020.N.

Mpyriopholis occipitalis. Moissala: 3273.N.

Naja haje. Baibokoum: 2114.N, 2229.N, 2240.N; Birim:

2800.N, 2801.N; Bitanda: 2596.N, 2598.N; Bitea: 2913.N;

Bon Amdaoud: 1965.N, 3080.N, 3090.N; Doureng: 1828.N;

Mao: 2803.N, 2804.N, 2805.N; Masarma: 1801.N; Matafo 2:

2781.N, 2782.N, 2783.N, 2785.N; Moissala: 3297.N; Moun-

dou: 2620.N.

Naja_nigricollis. Baibokoum: 2112.N, 2118.N, 2192.N,

2221.N, 2235.N, 2309.N, 2379.N, 2398.N; Bon Amdaoud:

1947.N, 1966.N, 3065.N, 3072.N; Fianga (env): 2509.N;

Goulmounbass: 2631.N; Laobida: 2712.N, 2719.N; Moissa-

la: 1970.N, 1974.N, 1975.N, 1981.N, 1984.N, 1991.N, 2708.N,

3298.N, 3299.N; Zamagouin: 2736.N, 2739.N.

Naja savannula. Baibokoum (Mboura): 2281.N.

Naja subfulva. Birim: 2802.N; Bitanda: 2600.N.

Natriciteres olivacea. Birim: 2790.N.

Philothamnus bequaerti. Baibokoum: 2294.N.; Moissala:

1972.N.

Philothamnus irregularis. Baibokoum: 2003.N, 2072.N,

2098.N, 2170.N, 2171.N, 2193.N, 2211.N, 2256.N, 2312.N,

2313.N, 2314.N, 2316.N, 2320.N, 2321.N, 2377.N, 2386.N,

2405.N, 2411.N.; Zamagouin: 2556.N, 2557.N, 2737.N,

2745.N.

©ZFMK

392 Jean-Frang¢ois Trape et al.

Philothamnus semivariegatus Baibokoum: 2298.N; Moissa-

la: 2707.N; Moundou: 2616.N.

Platyceps florulentus. Arningmalik:1831.N; Bitea: 1864.N,

2883.N, 2905.N; Doureng: 1827.N, 2868.N.

Prosymna ambigua. Moissala: 1973.N.

Prosymna collaris. Bahar: 1891.N, 2970.N, 2971.N, 2972.N;

Balani: 2538.N, 2568.N; Djarat Abounimir: 3137.N; Fieng-

bac: 2551.N, 2552.N; Moundou: 2580.N.

Prosymna greigerti. Bahar: 2973.N, 2974.N, 2975.N, 2976.N;

Baibokoum: 2033.N, 2093.N, 2104.N, 2180.N; Bitanda:

2608.N; Bon Amdaoud: 3118.N; Djarat Abounimir: 3134.N,

3135.N, 3136.N; Kadam Digas: 2763.N, 2834.N, 2855.N;

Moissala: 1978.N.

Psammophis afroccidentalis. Mao: 2808.N.

Psammophis elegans elegans. Mao: 2806.N, 2807.N.

Psammophis_ elegans univittatus. Baibokoum: 2005.N,

2036.N, 2097.N, 2122.N, 2183.N, 2222.N; Bon Amdaoud:

1955.N, 2761.N, 3082.N, 3083.N, 3092.N, 3100.N, 3125.N;

Djarat Abounimir: 1932.N.

Psammophis lineatus. Baibokoum: 2040.N, 2092.N, 2120.N,

2132.N, 2203.N, 2204.N, 2225.N, 2228.N, 2265.N, 2369.N,

2375.N, 2383.N, 2394.N, 2421.N, 2463.N:; Bitanda: 2577.N,

2602.N; Goulmounbass: 2659.N, 2660.N, 2661.N, 2662.N,

2663.N, 2664.N, 2665.N, 2666.N, 2667.N, 2668.N, 2669.N,

2670.N, 2671.N, 2672.N, 2673.N, 2674.N, 2675.N, 2676.N,

2677.N, 2678.N, 2679.N, 2680.N, 2681.N, 2682.N, 2683.N,

2684.N, 2685.N, 2686.N, 2687.N, 2688.N, 2689.N, 2690.N,

2691.N, 2692.N, 2693.N, 2694.N, 2695.N, 2696.N, 2697.N,

2698.N, 2699.N, 2700.N; Léré: 2756.N, 2757.N; Zamagouin:

2534.N, 2747.N, 2752.N.

Psammophis mossambicus. Baibokoum: 2006.N, 2053.N,

2054.N, 2066.N, 2067.N, 2068.N, 2083.N, 2087.N, 2088.N,

2123.N, 2129.N, 2130.N, 2136.N, 2145.N, 2146.N, 2148.N,

2172.N, 2175.N, 2177.N, 2186.N, 2202.N, 2224.N, 2226.N,

2238.N, 2244.N, 2245.N, 2252.N, 2260.N, 2264.N, 2269.N,

2341.N, 2342.N, 2408.N, 2409.N, 2410.N, 2412.N, 2418.N,

2459.N, 2460.N, 2461.N, 2462.N; Bitanda: 2581; Laobida:

2529.N, 2714.N, 2715.N, 2716.N, 2718.N, 2722.N; Moissala:

1971.N, 1977.N, 1983.N, 1989.N, 2704.N, 2705.N, 2706.N,

3300.N, 3301.N, 3302. N, 3303.N, 3304.N; Moundou: 2619.N.

Psammophis rukwae. Bahar: 1894.N, 1895.N, 1897.N,

2978.N, 2979.N, 2980.N, 2981.N, 2982.N, 3016.N, 3017.N,

3018.N; Baibokoum: 2020.N, 2022.N, 2023.N, 2056.N,

2059.N, 2062.N, 2064.N, 2121.N, 2131.N, 2147.N, 2150.N,

2173.N, 2179.N, 2205.N, 2223.N, 2241.N, 2242.N, 2254.N,

2267.N, 2271.N, 2329.N, 2330.N, 2340.N, 2344.N, 2345.N,

2371.N, 2378.N, 2381.N, 2416.N, 2417.N; Birim: 2793.N,

2794.N, 2795.N, 2796.N, 2797.N, 2798.N, 2799.N: Bitea:

1836.N, 1840.N, 1847.N, 1852.N, 1860.N, 2885.N, 2902.N;

Bon Amdaoud: 1949.N, 2762.N, 3078.N; Djarat Abounimir:

1914.N, 1916.N, 1919.N, 1928.N, 1937.N, 3151.N, 3152.N,

3153.N, 3154.N, 3201.N, 3202.N, 3203.N, 3204.N, 3205.N,

3206.N, 3207.N, 3208.N, 3209.N, 3210.N, 3211.N, 3212.N,

3213.N, 3214.N, 3215.N, 3216.N, 3217.N, 3218.N, 3219.N,

Bonn zoological Bulletin 69 (2): 367-393

3220.N, 3221.N, 3222.N, 3223.N, 3224.N, 3225.N, 3226.N,

3227.N, 3228.N; Fiengbac: 2531.N, 2563.N; Goulmounbass:

2651.N, 2652.N, 2653.N, 2654.N, 2655.N, 2656.N, 2657.N,

2658.N; Gouroungali: 2926.N; Hileborno: 1899.N, 1900.N;

Kadam Digas: 2764.N, 2831.N, 2832.N, 2838.N, 2851.N;

Kiéké: 1942.N, 1943.N, 2758.N, 2759.N, 3021.N, 3022.N,

3025.N, 3027.N, 3038.N, 3040.N; Mahargal: 1878.N, 1881.N,

1888.N, 2945.N, 2946.N, 2947.N, 2948.N, 2949.N, 2950.N,

2951.N, 2952.N; Masarma: 1806.N, 1807.N, 1809.N, 1812.N,

1813.N, 2813.N, 2816.N, 2820.N; Matafo 2: 2786.N, 2787.N;

Mataya: 1815.N, 1816.N; N’Djaména (Farcha): 1997.N,

1998.N, 1999.N, 2000.N; N’Djaména (Gassi): 1994.N,

1995.N, 1996.N , 2001.N, 2002.N; Tikem (Goundwaye):

2554.N; Zamagouin: 2522.N, 2744.N, 2749.N, 2753.N.

Psammophis_ sudanensis. Arningmalik: 1832.N, 2870.N,

2871.N, 2872.N; Bahar: 1893.N, 3014.N; Baibokoum:

2149.N, 2156.N, 2231.N, 2232.N, 2234.N, 2280.N, 2283.N,

2289.N, 2292.N, 2308.N, 2365.N, 2380.N, 2392.N, 2393.N,

2396.N, 2404.N; Balani: 2527.N; Bitea: 1839.N, 1841.N,

1842.N, 1849.N, 1850.N, 1851.N, 1853.N, 1855.N, 1858.N,

1859.N, 1862.N, 1869.N, 2876.N, 2880.N, 2884.N, 2886.N,

2887.N, 2888.N, 2889.N, 2890.N, 2891.N, 2892.N, 2893.N,

2894.N, 2899.N, 2907.N, 2908.N, 2909.N, 2912.N, 2931.N;

Bon Amdaoud: 1945.N, 1948.N, 1950.N, 1952.N, 1957.N,

1958.N, 1962.N, 1969.N, 3044.N, 3046.N, 3053.N, 3054.N,

3060.N, 3071.N, 3076.N, 3079.N, 3087.N, 3091.N, 3093.N,

3095.N, 3105.N, 3107.N, 3108.N, 3109.N, 3112.N; Dja-

rat Abounimir: 1902.N, 1904.N, 1911.N, 1912.N, 1913.N,

1918.N, 1921.N, 1922.N, 1927.N, 1929.N, 1933.N, 1934.N,

1936.N, 3149.N, 3150.N, 3171.N, 3172.N, 3173.N, 3174.N,

3175.N, 3176.N, 3177.N, 3178.N, 3179.N, 3180.N, 3181.N,

3182.N, 3183.N, 3184.N, 3185.N, 3186.N, 3187.N, 3188.N,

3189.N, 3190.N, 3191.N, 3192.N, 3193.N, 3194.N, 3195.N,

3196.N, 3197.N, 3198.N, 3199.N, 3200.N; Doureng: 2866.N;

Goulmounbass: 2632.N, 2633.N, 2634.N; Guirli: 2922.N;

Hileborno: 2925.N, 3307.N; Kadam Digas: 1818.N, 1819.N,

1820.N, 1821.N, 1825.N, 2769.N, 2770.N, 2771.N, 2772.N,

2840.N, 2842.N, 2843.N, 2862.N; Kiéké: 3028.N, 3036.N;

Mahargal: 1876.N, 1879.N, 1880.N, 1882.N, 1884.N, 1889.N,

2941.N, 2942.N, 2943.N, 2944.N, 2953.N, 2954.N, 2955.N,

2956.N, 2957.N; Masarma: 1804.N, 1811.N, 1814.N; Mois-

sala: 1976.N, 1979.N, 1985.N, 1987.N, 2701.N, 2702.N,

3305.N, 3306.N, 3311; Moundou (Tayé): 2613.N; Zamagou-

in: 2528.N, 2569.N, 2750.N.

Python regius. Baibokoum: 2119.N, 2355.N, 2356.N, 2406.N,

2407.N; Laobida (Dobarbian): 2780.N.

Python sebae. Bitea: 1867.N, 2927.N; Hileborno: 3308.N;

Kadam Digas: 2775.N, 2861.N; Mataya: 1817.N; Zamagou-

in: 2530.N.

Rhamphiophis oxyrhynchus. Bahar: 2983.N; Baibokoum:

2025.N, 2063.N, 2075.N, 2077.N, 2091.N, 2095.N, 2103.N,

2137.N, 2220.N, 2233.N, 2251.N, 2253.N, 2263.N, 2349.N,

2363.N, 2382.N, 2384.N, 2390.N, 2413.N, 2414.N, 2415.N;

Bitanda: 2582.N, 2584.N, 2585.N, 2588.N, 2589.N, 2591.N,

2594.N, 2597.N, 2599.N, 2604.N, 2607.N; Bon Amdaoud:

1968.N, 3063.N, 3064.N, 3088.N, 3099.N, 3101.N, 3102.N,

3103.N; Fiengbac: 2511.N; Goulmounbass: 2635.N, 2636.N,

2637.N; Kadam Digas: 2767.N, 2768.N, 2847.N; Laobida:

2711.N, 2723.N; Laobida (Yamba-Tchangsou): 2533.N; Mois-

sala: 2703.N, 3310.N; Moundou (Belaba): 2617.N, 2625.N.

©ZFMK

The snakes of Chad 393

Rhamphiophis rostratus. Bitea: 1861.N.

Scaphiophis albopunctatus. Baibokoum: 2037.N, 2236.N,

2279.N, 2326.N, 2327.N, 2348.N; Bon Amdaoud: 1963.N,

3084.N; Laobida (including Malgandi and Yamba-Tchang-

sou): 2721.N ,2514.N , 2519.N.

Bonn zoological Bulletin 69 (2): 367-393

Telescopus tripolitanus. Bahar: 1890.N; Bitea: 2881.N,

2882.N; Bon Amdaoud: 3042.N, 3043.N, 3051.N, 3052.N,

3067.N, 3086.N, 3097.N, 3119.N, 3120.N.

Telescopus variegatus. Baibokoum: 2032.N, 2058.N, 2374.N;

Laobida: 2512.N, 2513.N, 2570.N, 2726.N; Laobida (Baibag-

la): 2516.N, 2524.N, 2540.N, 2541.N; Laobida (Yamba-Ma-

loum): 2532.N; Moissala: 1986 N; Zamagouin: 2755.N.

Tricheilostoma sundewalli. Baibokoum: 2073.N.

©ZFMK

BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (2): 395—411

2020 - O’Shea M. et al.

https://do1.org/10.20363/BZB-2020.69.2.397

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub: 7EEF9824-1088-4C06-8B30-S5F949D41 F050

Discovery of the second specimen of

Toxicocalamus ernstmayri O’ Shea et al., 2015 (Squamata: Elapidae),

the first from Papua Province, Indonesia,

with comments on the type locality of ZT. grandis (Boulenger, 1914)

Mark O’Shea!-*, Paul Blum? & Hinrich Kaiser?

' Faculty of Science and Engineering, University of Wolverhampton, Wulfruna Street, Wolverhampton, WV1 ILY, UK

? Habsburgerstrape 99, D-79104 Freiburg im Breisgau, Germany

> Department of Vertebrate Zoology, Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn,

Germany

> Department of Biology, Victor Valley College, 18422 Bear Valley Road, Victorville, California 92395, USA

* Corresponding author: Email: m.osheaQwlv.ac.uk

'urn:Isid:zoobank.org:author: DEF 1489F-5BCD-4402-96A7-E9263E7BDFD9

2urn:lsid:zoobank.org:author: D96A E0C6-E5 12-433 A-8B60-CE6C28B13B28

3urn:|sid:zoobank.org:author:3283F957-68 1 7-4C69-8C3 1 -324D49AF735A

Abstract. Examination of historical specimens from western New Guinea in the Zoologische Staatssammlung Munich,

Germany, led to the discovery of only the second specimen of the rarely encountered Star Mountains Worm-eating Snake,

Toxicocalamus ernstmayri. This specimen is the first record of the species from the Indonesian part of New Guinea,

extending its known range northwestward by 150 km. We also question the long-accepted collection locality for another

poorly known species, 7’ grandis and document that it was most likely collected further up the Setekwa River at a higher

elevation, in habitat more conducive to the ecology of a terrestrial to semi-fossorial genus and in keeping with the known

mainland distribution of Toxicocalamus.

Keywords. Indonesia, Jayawijaya Range, Sudirman Range, Utekwa River, Setekwa River, rare snake.

INTRODUCTION

Toxicocalamus is an endemic New Guinea genus of

secretive, semi-fossorial or terrestrial snakes that occurs

throughout the island in both the sovereign state of

Papua New Guinea (PNG), which occupies the eastern

half of the island, and western New Guinea (WNG),

the Indonesian half of New Guinea that includes the

provinces Papua and West Papua. These snakes have

also been recorded from a number of satellite islands off

the coast of PNG, including Seleo (Sandaun Province),

Walis and Tarawai (East Sepik Province), and Karkar

(Madang Province). Zoxicocalamus also has an island

radiation in the archipelagos of Milne Bay Province,

PNG, including six species in the d’Entrecasteaux

Archipelago (Good-enough, Fergusson, and Normanby

Islands), the Louisiade Archipelago (Misima, Sudest, and

Rossel Islands), and on Woodlark Island. Sixteen species

are currently recognised, but we expect that this figure

will increase considerably due to a recent resurgence of

interest in the genus that has already led to the description

Received: 03.08.2020

Accepted: 09.11.2020

of seven species since 2009 (Kraus 2009, 2017, 2020;

O’Shea et al. 2015, 2018a).

Toxicocalamus ernstmayri O’Shea et al., 2015 was

described from a female holotype (MCZ R-145946)

collected by former kiap' Fred Parker on 23 December

1969 at Wangbin (5.2408° S, 141.2589° E, elev. 1468 m;

Fig. 1), a small hamlet near Tabubil in the Star

Mountains, North Fly District, Western Province,

PNG. It was accessioned into the collection of the

Museum of Comparative Zoology, Harvard University,

Cambridge, Massachusetts, USA (MCZ), as a specimen

of Micropechis ikaheca’ Lesson, 1830, and it remained

misidentified until it was examined by the first author

during a research visit to the MCZ collection in 2014.

With a snout-to-vent length (SVL) of 1.1 m and a total

length (TTL) of 1.2 m, the holotype is the largest known

specimen of Toxicocalamus, a genus which rarely

1 Kiap is a word in tok pisin (a Papuan creole language), derived from

the German for captain and referring to a pre-Independence patrol

officer in PNG.

2 The correct spelling is ikaheca rather than the commonly used

ikaheka, according to Lesson’s original description.

Corresponding editor: W. Bohme

Published: 17.11.2020

396

ens ees

Mark O’ Shea et al.

sop d eM

mace |

“A

f E

Fig. 1. Note to the reader: This figure comprises a left panel (above) and a right panel at the top of the facing page. Shown is

a 1942 map of southwestern New Guinea, including the mountain ranges from which the existing records of Toxicocalamus

ernstmayri and T. grandis were reported. Numbered red circles indicate localities for (1) the holotype of 7? ernstmayri (MCZ

R-145946), (2) the sighting of 7’ ernstmayri at the Ok Tedi Mine (O’Shea et al. 2018b), and (3) the locality where ZSM 55/2015

was collected. The vertical white frame on the main map identifies the location of the Wollaston Expedition of 1912-13, which

nearly reached Carstensz Pyramid, now Puncak Jaya (white triangle). The highlighted yellow line is the border between Papua New

Guinea to the east and Indonesian West New Guinea to the west. The inset is an 1884 map showing Dutch, German and British

boundaries, with the position of the main map, relative to the island of New Guinea, northern Australia, and eastern Indonesia,

indicated by the horizontal white frame.

exceeds 600 mm TTL. The only other species of near

equal size is 7’ grandis (Boulenger, 1914), whose single

specimen is housed in The Natural History Museum,

London, United Kingdom (BMNH) and accessioned as

BMNH 1946.1.18.34. It was ostensibly collected on the

Setekwa River’, southern Papua Province, WNG (Fig. 1)

in 1912, and possesses an SVL of 960 mm and a TTL

of 1040 mm. A second, live individual of 7? ernstmayri

was identified in 2018 from photographs, which are of

an unsexed adult (approximate TTL 850 mm, estimated

3 When dealing with colonial and local place names, it is common

that differences in names or spelling exist. Sometimes this is

because a colonial power insisted on renaming places that already

had local names, as a sign of superiority, oppression, or to honor

their leadership, other times honest transcription errors derived from

communication problems between the local population and colonial

officials crept in, especially when dealing with oral names that were

never intended to be written down and which may sound different

when spoken by different groups of indigenous people or even

individual persons. The names of the Setekwa and Utekwa Rivers

in WNG we use here are examples of the latter, and they can also be

spelled as Setakwa and Oetakwa.

Bonn zoological Bulletin 69 (2): 395-411

from the known size of tire tracks) as it moved slowly

and unmolested across an area of active mine workings at

the Ok Tedi Mine (5.2150° S, 141.1442° E, elev. 1670 m;

Fig. 1) on 9 October 2015 (O’Shea et al. 2018b). The

two locations, Wangbin and the Ok Tedi Mine, are only

13.2 km apart and 7 ernstmayri was presumed to be a

localised species found only in the Star Mountains of

Western and Sandaun Provinces, PNG.

During a visit to the Zoologische Staatssammlung

Munich, Germany (ZSM), the first author examined a

small collection of snakes from the mountains of WNG

made by the second author in the 1970s. This collection

included two specimens of Toxicocalamus that had

tentatively been identified as 7 grandis. While the

identity of one of these (ZSM 54/2015) still has to be

determined, the other (ZSM 55/2015) represents the first

known specimen of 7 ernstmayri from the western half

of the island of New Guinea, and we herein document it

as such.

©ZFMK

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 397

ead mt

oie

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Age

eres

DY Fea)

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Fig. 1. Continued: right panel.

MATERIALS AND METHODS

Measurements

Our length measurements and our assessment of

Toxicocalamus scales follow the methods described by

O’Shea et al. (2018a). SVL was obtained by running

a non-elastic string from the tip of the snout along the

ventral medial axis of the body, the string then being

placed against a cloth tape-measure taped to a workbench

with attention being paid to accuracy of measurement,

fide Natusch & Shine (2012). Tail length (TL) was easily

measured by laying the tail along the tape-measure. TTL is

the sum of SVL+ TL, and TL as a percentage of TTL was

calculated as TL/TTL x 100. Other abbreviations include

V (ventrals), SC (subcaudals), SCR (subcaudal ratio,

calculated as SC divided by V+SC), SL (supralabials),

and IL (infralabials).

Scale counts

Scale counts recorded on the body included dorsals,

ventrals, and subcaudals. The dorsal scale rows were

counted transversely across the body at three points,

one head length posterior to the head, at midbody, and

one head length anterior to the cloaca. These counts in

Bonn zoological Bulletin 69 (2): 395-411

Toxicocalamus are usually 15-15-15, with the exceptions

of 7! preussi (Sternfeld, 1913) with 13-13-13 and

7. longissimus Boulenger, 1896 with 17-17-17. Dorsal

scales of Zoxicocalamus are smooth without apical pits.

Ventral scales, or gastrosteges, were counted beginning

with the first broad scale on the anterior part of the body

that contacts a scale of the lowest dorsal scale row on both

sides, the count then continuing to the scale immediately

anterior to the cloacal plate. In 7? pumehanae O’Shea

et al., 2018, this scale is divided into a pair of pre-

cloacal scales. The condition of the cloacal plate,

entire or paired, is also noted as this has taxonomic

implications in Toxicocalamus. The condition of the

subcaudal scales is also of taxonomic importance since

all Toxicocalamus except for 7: holopelturus McDowell,

1969 exhibit paired subcaudals. Subcaudal scales were

counted along one side of the tail beginning with the

scale immediately posterior to the vent and continuing

to the scale immediately anterior to the tail tip; the tail

tip was not included in the count. The subcaudal counts

of specimens with truncated tails are suffixed with a plus

sign (+) indicating the specimen once possessed at least

the number of scales counted (e.g., 54+ indicates that the

specimen’s tail was truncated posterior to scale 54). If

present, the shape of the tail tip is recorded as sharply

pointed, rounded, or laterally compressed.

©ZFMK

398

Sex and sexual dimorphism

Sex was determined by the examination of the gonads,

presence of ova, the presence of everted hemipenes, or

the presence of the retractor penis magnus muscle. In

some species of Joxicocalamus, especially the more

slender, short-tailed semi-fossorial species 7. preussi and

7. buergersi (Sternfeld, 1913), sex can be determined

from relative tail length and subcaudal scale counts, with

males exhibiting tails more than twice as long as those of

females. Females also often exhibit proportionally longer

bodies and higher ventral counts than conspecific males.

Head scale patterns

Head scalation provides extremely important clues for

species determination in the genus 7oxicocalamus. Eight

of the 16 species, including 7. ernstmayri and T: grandis,

exhibit the classic colubrid-elapid dorsal nine-plate

arrangement (O’Shea 2005: 12) with distinct and separate

pairs of internasals (IN), prefrontals (PF), supraoculars

(SO) and parietals (P) with a single central frontal (F).

The other eight species exhibit some degree of head scute

fusion, either of the internasal and prefrontal or of the

prefrontal and preocular (PR), or possesses a pair of large

anterior head scutes comprising the fused internasal,

prefrontal, and preocular. One species even exhibits

fusion of the supraoculars and frontal into a single broad

scale across the top of the head. Other important dorsal

scales on the head include nasals (N), which may be

completely divided by a large naris (nostril) or almost

entire with a small countersunk naris in the centre, a rostral

(R), preoculars (PR, if not fused with the prefrontals),

postoculars (PO) with occasional fusion of the upper PO

to the supraocular or the lower PO to a supralabial (SL),

and the number and status of the anterior and posterior

temporals (AT and PT, respectively). Supralabial counts

are provided, and we report which of them contact the

orbit (eye) and which 1s the largest. Toxicocalamus 1s

almost unique amongst terrestrial New Guinea elapids in

not possessing a temporolabial scale*, a diamond-shaped

scale protruding downwards between the penultimate

and ultimate supralabials. On the ventral side of the head

we list the number of infralabials (IL) on either side,

noting which contact the anterior and posterior genials

(AG and PG, respectively), and whether these scales are

themselves in contact at the mental groove or whether the

posterior genials are separated by an intergenial (IG). The

first pair of ILs is elongate and the only pair that meet at

4 The other terrestrial New Guinea elapid lacking a temporolabial scale

is Pseudonaja, which is unlikely to be confused with Toxicocalamus

for numerous reasons, not least its very large eyes. All other terrestrial

Papuan elapid genera (Acanthophis, Aspidomorphus, Cryptophis,

Demansia, Furina, Micropechis, Oxyuranus, and Pseudechis),

exhibit an obvious temporolabial scale.

Bonn zoological Bulletin 69 (2): 395-411

Mark O’ Shea et al.

the mental groove, anterior to the AGs and posterior to

the triangular mental (M) at the front of the lower jaw.

Specimen illustrations

Specimens were photographed using the basic methods

explained in Kaiser et al. (2018), but with dual

photographic set-ups and relatively high-end DSLR

equipment to ensure visual clarity in photographs of

specimens with very dark, shiny surfaces. All images

were uploaded to Aperture 3.6° on a MacBook Pro (OS

X Mavericks ver. 10.10). The figures used in this paper

were then obtained on a MacPro desktop computer (OS

X Sierra ver. 10.12), using Adobe Photoshop CC 2019

and a Wacom Cintigq 13” HD Touch.

RESULTS AND DISCUSSION

Basic morphology and pholidosis

ZSM 55/2015 (Fig. 2A, D) was collected in June 1976

at Dingerkon (4.4508°S, 140.0347°E, elev. 1600 m),

Pegunungan Bintang Regency, Papua Province, WNG.

This locality is on the Eipomek River in the Jayawiyaya

(formerly Orange) Range, the mountain § range

immediately to the west of the Star Mountains (Fig. 1).

The specimen was accessioned into the ZSM collection

in 2015. ZSM 55/2015 is a female (SVL 765 mm + TL

87 mm = TTL 851 mm). Its scale counts are identical or

close to those of the holotype of 7! ernstmayri (Fig. 2B, E;

different values in the holotype provided in parentheses),

including a dorsal scale count of 15-15-15; 202 ventrals;

a divided cloacal plate; 30 (29) paired subcaudals; SL=6,

with SL3 and SL4 contacting the orbit (Fig. 3A, A’, B, B’);

IL = 6, with IL1—IL3 in contact with the anterior genials

and IL3 and IL4 in contact with the posterior genials; an

intergenial scale separating the posterior genitals 1s pre-

sent (Fig. 4A, A’, B, B’); “colubrid-elapid dorsal nine-

plate arrangement” of two internasals, two prefrontals,

a frontal between two supraoculars, and two parietals

on the head; single preocular, in contact with SL2 and

SL3; prefrontal and supraocular have broad contact with

the nasal; postocular single (paired) in contact with SL4

and SLS, supraocular, and anterior temporal (Fig. 5A,

A’, B, B’, C, C’, D, D’); temporal arrangement 1+2 (left:

1+1, right: 1+2). In this listing of scale characteristics,

the only differences between ZSM 55/2015 and the

holotype of 7! ernstmayri are one subcaudal scale, the

single versus paired postocular condition, and the fusion

of the posterior temporals on the left side of the head in

the holotype.

5 Apple have discontinued and no longer support Aperture. It will

also run on OS X High Sierra (10.13) and OS X Mojave (10.14)

but not OS X Catalina (10.15). An alternative application is Adobe

Lightroom.

©ZFMK

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 399

The ZSM specimen appears to exhibit a subterminal

mouth (an “underbite”’), with the lower jaw appearing to

extend beyond the upper jaw, combined with an apparent

compression of the snout, certainly on the right side

(Figs. 5A, A’, B, B’, 6). The latter 1s likely an artefact

of preservation, such that the snake was stored in a

container with its snout pressed against the container’s

Ze2 Se,

peer

AP Oe

; ©.

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(SSsttesss 7

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inner surface. However, the front of the snout does appear

to be slightly malformed as seen by the continuation of

the prefrontal-internasal suture anteriorly onto the rostral

to form a vertical division (Fig. 6). Whether this slight

abnormality was the cause or a post-fixation contributory

factor to shaping the head as we see it now is open to

conjecture.

Fig. 2. Whole body views and colour patterning in three specimens of 7oxicocalamus. Dorsal views include those of (A) ZSM

55/2015; (B) the holotype of 7? ernstmayri (MCZ R-145946); and (C) the holotype of 7: grandis (BMNH 1946.1.18.34). Ventral

views (D-E) are listed in the same order as the dorsal views. The circular images show closeups of dorsal scale patterns and are

provided to illustrate the observed pattern reversal. Whereas the pattern in ZSM 55/2015 (G) and T. ernstmayri (H) 1s characterized

by dorsal scales with dark centers and light edging, there is no such prominent patterning in 7 grandis (1). Images not to scale.

Photos by Mark O’Shea.

Bonn zoological Bulletin 69 (2): 395-411

©ZFMK

400 Mark O’ Shea et al.

Fig. 3. Dorsal views of the heads of 7oxicocalamus specimens from New Guinea, presented as both photographic and line-

drawing illustrations. The drawing in (B’) features the classic colubrid-elapid nine-plate arrangement (light grey), comprising

paired internasals (IN), prefrontals (PF), supraoculars (SO), and parietals (P), and single frontal (F), and eleven scales bordering

the parietals (mid-grey), including anterior temporals and upper posterior temporals. The drawings in (A’) and (C’) follow the

same pattern. Shown are (A, A’) the first West New Guinea specimen of 7) ernstmayri (ZSM 55/2015), (B, B’) the holotype of

T. ernstmayri (MCZ R-145946), and (C, C’) the holotype of 7) grandis (BMNH 1946.1.18.34). Images not to scale. Photos and

line drawings by Mark O’Shea.

Comparisons with Toxicocalamus grandis

Differences in scalation between the two extant

specimens of 7. ernstmayri (MCZ R-145946, ZSM

55/2015), and the single known specimen of 7: grandis

(BMNH 1946.1.18.34; Figs. 2C, F, 3; characteristics in

parentheses) include broad contact between the preocular

and the nasal scales (point contact on the left side and

exclusion by contact between SL2 and the prefrontal

on the right side; Fig. 5E, E’, F, F’), eleven temporal

and post-temporal scales bordering the parietals (nine

Bonn zoological Bulletin 69 (2): 395-411

scales), and SL6 only narrowly separated from the upper

posterior temporal (SL6 widely separated by broad

contact between the anterior temporal and the lower

posterior temporal). The only character in which ZSM

55/2015 agrees with 7? grandis and not T. ernstmayri

is the presence of a single postocular where the type

of 7. ernstmayri has a pair of postoculars. Whilst this

is perhaps an important difference in the grand scheme

of Zoxicocalamus taxonomy, when weighed against the

number of characters in which ZSM 55/2015 agrees with

©ZFMK

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 401]

a IS

Fig. 4. Ventral views of the heads of Toxicocalamus specimens from New Guinea, presented as both photographic and line-

drawing illustrations. The drawing in (B’) includes scales identified by lettering, including mental (M), numbered infralabials

(IL), anterior genials (AG) in contact along the mental groove, posterior genials (PG) separated by an intergenial (IG), and the first

gastrostege (V'). The drawings in (A’) and (C’) follow the same pattern. Shown are (A, A’) the first West New Guinea specimen

of 7. ernstmayri (ZSM 55/2015), (B, B’) the holotype of 7! ernstmayri (MCZ R-145946), and (C, C’) the holotype of 7) grandis

(BMNH 1946.1.18.34). Images not to scale. Photos and line drawings by Mark O’Shea.

7: ernstmayri and, given the propensity for scale fusions

in the genus, its importance is diminished.

In its colouration, ZSM 55/2015 is remarkably similar

to the holotype of 7) ernstmayri. In the original list of

specimens donated to the ZSM both ZSM 54/2015

and ZSM 55/2015 were classified as T. grandis, but in

BMNH 1946.1.18.34, the only known specimen of that

species, the dorsal pattern comprises fairly uniformly

coloured scales (Fig. 21), whereas in both specimens of

7. ernstmayri (MCZ R-145946, ZSM 55/2015; Fig. 2G,

Bonn zoological Bulletin 69 (2): 395-411

H, respectively) the pattern is striking, comprising light

dorsal scales edged with dark pigmentation.

Natural history and ethnology

The second author participated in a 1976 ethnological

and ethnobiological expedition (Fig. 7), conducted by

the Museum fiir V6olkerkunde (Ethnological Museum)

in Berlin and led by the medical anthropologist

©ZFMK

402 Mark O’Shea et al.

——

noe

Fig. 5. Lateral views of the heads of 7oxicocalamus specimens from New Guinea, presented as both photographic and line-

drawing illustrations in right and left aspect. The drawings in (C’) and (D’) include scales identified by lettering, including rostral

(R), mental (M), nasals (N), internasals (IN), prefrontals (PF), preoculars (PR), supraoculars (SO), postoculars (PO), anterior

temporals (AT), posterior temporals (PT), numbered supraoculars (SL), and numbered infralabials (IL). The drawings in (A’, B’)

and (E’, F’) follow the same pattern. Shown are the first West New Guinea specimen of 7! ernstmayri (ZSM 55/2015) in right (A,

A’) and left (B, B’) lateral views, the holotype of 7? ernstmayri (MCZ R-145946) in right (C, C’) and left (D, D’) lateral views, and

the holotype of 7’ grandis (BMNH 1946.1.18.34) in right (E, E’) and left (F, F’) lateral views. Images not to scale. Photos and line

drawings by Mark O’Shea.

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 403

Fig. 6. Frontal view of the head of the first West New Guinea specimen of 7) ernstmayri (ZSM 55/2015) as a photo (A) and a

line drawing (A’), illustrating the deeply scored and deformed rostral (R), divided nasals (N), internasals (IN), prefrontals (PF),

supralabials (SL), mental (M), and infralabials (IL). Photo and line drawing by Mark O’Shea.

Wulf Schiefenhével®, to study the Eipo people of

the remote Eipomek Valley in central mountainous

WNG (Schiefenhovel 1997). We would therefore be

remiss if in our account of ZSM 55/2015 we did not

include information on how a snake like 7. ernstmayri

is perceived by the indigenous human population. We

therefore expand our specific report on this snake to

include its relevance to the local residents, who are very

much a part of the natural environment in New Guinea.

ZSM 55/2015 was discovered and killed in a village

garden (Fig. 8) during daylight hours on 18 June 1976.

Snakes of the genus 7oxicocalamus are believed to be

exclusively vermivorous (O’Shea et al. 2015), and they

appear to be especially common in highland gardens,

possibly because of the abundance of giant earthworms

(Annelida: Megascolecidae) in well-turned, irrigated,

and composted montane vegetable plots operating for

35,000-60,000 consecutive years (Schiefenhovel 2001).

The high density of Zoxicocalamus in these habitats is

supported by the large number (165 specimens = 32% of

all known specimens) collected in the heavily populated

and intensively farmed Wahgi Valley (Simbu and Jiwaka

Provinces, PNG) by Australian kiap and herpetologist

Fred Parker, Divine Word missionary Father Otto (Shelly)

Schellenberger (1914—2007), and other field collectors.

That the snake was active during the day is also not

unusual, certainly the larger and more terrestrial species

(including 7. ernstmayri and T. pachysomus) appear to

be diurnally active, as evidenced by the observation of

7. ernstmayri moving unhurriedly across mine-workings

at Ok Tedi in broad daylight (O’ Shea et al. 2018b).

6 On an earlier ethnological/zoological expedition to New Guinea,

the “Papua Expedition 1966” by the Zoological Institute at Ludwigs-

Maximilians-Universitat Munich (Schultze-Westrum 1968), the

expedition leader Thomas Schultze-Westrum was bitten by a

Miuller’s crowned snake (Aspidomorphus muelleri). The symptoms

and treatment of this snakebite, the only known record of a snakebite

from this genus, were documented and published by Schiefenhovel

(1969).

Bonn zoological Bulletin 69 (2): 395-411

The dead snake was delivered to the second author

by a Dingerkon villager named Ewinde, who carried it

in secrecy and protectively wrapped in three layers of

leaves so that other villagers would not see it. The Eipo

are apparently frightened by snakes, which they call

kwatema, but they were especially averse to this species

which they call amau, considering it highly dangerous’

and capable of causing death, and even to look upon it

is considered highly undesirable. The second author was

warned to be very careful with the dead snake, especially

to avoid pricking himself on its sharp tail tip, the

keratinized sting-like terminal scale, because that could

prove fatal. Thus, the dead snake was positioned on a flat

rock and photographed surreptitiously (Fig. 9).

Where is the type locality of Toxicocalamus grandis?

The Jayawijaya Range, where ZSM 55/2015 was

collected, is adjacent to the Star Mountains of Western

Province, where the holotype of 7’ ernstmayri was

collected in 1969 and from where the 2018 sighting was

documented (Fig. 1). The elevation for these observations

ranges from 1468 m at Wangbin, the type locality of

7. ernstmayri, to 1600 m at Dingerkon, the collection

locality of ZSM 55/2015, and to as high as 1670 m at the

Ok Tedi Mine. Whereas these specimens and sightings

are accurately pinpointed localities, “Launch Camp” on

the Setekwa River, where the holotype of 7’ grandis was

supposedly collected, has not previously been located

with any certainty.

The 7: grandis holotype (BMNH 1946.1.18.34) was

collected by the British explorer Alexander Frederick

7 The only toxinological study of Toxicocalamus venom was conducted

on 7: longissimus from Woodlark Island, Milne Bay Province, PNG

(Calvete et al. 2012). Its venom was found to contain high levels of

potentially dangerous 3-finger toxins (3FTx). However, there are no

human snakebites due to Zoxicocalamus on record and the reasons

why a vermivorous snake should possess relatively toxic venom are

unknown.

©ZFMK

404 Mark O’Shea et al.

Das engere Untersuchungsgebict.

+ Missionsstation mit Landepiste

—=~—Marsch der ersten Expeditionsgruppe 1974

@ Siedlungen mit Forschungsstationen, 1974 — 1976 begriindet

ENO Bunturwe

- 4 O Siteruk

Fig. 7. Map of the 1976 expedition to the Eipomek Valley, West New Guinea, Indonesia, modified from Ploeg (2004: 38). The red

dot marks Dingerkon, where the specimen of Toxicocalamus ernstmayri (ZSM 55/2015) was collected. The red circle indicated the

broader area in which expedition members studied the language and culture of the Eipo community, as well as the area’s natural

history. Scale is present above the map.

Richmond “Sandy” Wollaston (1875-1930; Fig. 10A)

and the British zoologist Cecil Boden Kloss® (1877-1949;

Fig. 10B) during the Wollaston Expedition? to Dutch

New Guinea in 1912-13. The expedition journeyed up

8 Cecil Boden Kloss learnt his trade as a museum conservator in

the natural history museum in Kuala Lumpur, Malaya, from 1908,

and he would go on to become Director of the Raffles Museum, in

Singapore (1923-1932). It is likely his presence on the Wollaston

Expedition ensured that the zoological specimens were correctly and

expertly fixed and curated.

9 This was Wollaston’s second expedition to New Guinea. His first

was the British Ornithologists’ Union expedition of 1910-11. He was

attempting to reach Mt. Carstensz (now Puncak Jaya), at 4994 m the

highest peak in New Guinea in the Nassau Mountains (now Sudirman

Range) in Dutch New Guinea. The 1910-11 expedition ascended the

Mimika River but failed to reach Mt. Carstensz, whereas the 1912—

13 expedition used the Setekwa and Utekwa Rivers and came very

close to succeeding.

Bonn zoological Bulletin 69 (2): 395-411

the Setekwa River branch of the Utekwa River, following

the same initial route and using the same campsites as

the Van der Bie Expedition’® of two years earlier, which

were referred to as “Base Camp” and “Canoe Camp”

(Wollaston 1933). While Wollaston gave no clue to the

location of his own site, called Launch Camp, the English

naturalist Albert Stewart Meek (1871-1943; Fig. 10C),

who had accompanied the earlier Van der Bie Expedition,

did refer to a likely location for this camp when he wrote:

10 Dutch military officers J.J. van der Bie and P.F. Postema, along with

the naturalist Joannes Maximiliaan Dumas (1856-1931), explored

the Setekwa and Utekwa River on a multipurpose military mission

in 1910-11 (LeCroy & Jansen 2011). This expedition also included

the English naturalist collector A.S. Meek (see below).

©ZFMK

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 405

Fig. 8. An overgrown garden plot in Dingerkon, West New Guinea, where the recently identified specimen of Toxicocalamus

ernstmayri (ZSM 55/2015) was collected. The snake was observed in the grass during the day and killed by a villager. Photo by

Paul Blum.

“At the mouth of the Oetakwa River we disembarked

our baggage into launches. The stores for the Dutch

expedition filled nine big boats and my stores another

big boat. This string of boats was taken in tow by a

steam launch, and like a great snake it wound its way

up the river, a full day's journey. This was the end of

navigable water for the steam launch. At this stage,

which was called the Launch Stage, I encountered

Captain Van der Bie and discussed my arrangements

with him. Then two days’ journey further up the river

by canoe brought us to what was called the Canoe

Stage.” (Meek 1913: 211f)

With Meek’s term “stage” clearly synonymous to a site

where expeditions are staged (1.e., a camp or landing

stage), it is most likely that Base Camp and Launch Camp

are one and the same location, with deep enough water

for a motor launch and two days downstream from Canoe

Camp (see Wollaston’s map; Fig. 12). This would suggest

that the camp from which the expedition originated

lay in the very low reaches of the Setekwa River, with

an elevation of only 20-30 m. The distribution of

Toxicocalamus can be loosely summarised as “highland

or island” but from the above account it might be assumed

that, unlike other mainland New Guinea Joxicocalamus,

Bonn zoological Bulletin 69 (2): 395-411

especially unlike 7’ ernstmayri, T. grandis defies that rule

and 1s a southern lowland species.

However, there is a problem with this supposition.

In her compilation of her husband’s posthumously

published letters and diaries!'! Mary Wollaston added the

following note:

“December 8. Up river to “Canoe Camp’

At this point in the diary A.F-R. [Sandy Wollaston]

makes the following note: ‘On March 9, 1913,

coming down the river from Canoe Camp to Base

Camp, my canoe upset in a dangerous rapid, so that

I was nearly drowned, and I lost the greater part of

my baggage, cameras, medicine chest, maps and

diaries. Now I have to begin to write over again

my diary from December 8, to March 9 — so far as I

can remember it. A.F:R.W. March 19, 1913.”

(Wollaston 1933: 135)

11 After a life time of living dangerously, which included two

expeditions to New Guinea, one to East Africa, participation in

the first ever attempt to ascend Mt. Everest with George Mallory

(1886-1924), and Royal Naval service in both the Great War and the

Russian Civil War, Sandy Wollaston was shot dead by a deranged

student at Cambridge University on 3 June 1930 (Wollaston 2003).

©ZFMK

406 Mark O’ Shea et al.

Since Wollaston and other naturalist collectors of his

era were more interested in birds, beetles, or butterflies

than reptiles and amphibians it is likely that they were

not as diligent with their recording of specific collection

localities for herpetological specimens. Given that

Wollaston had lost his diary and been forced to rewrite

his journey, from the Setekwa and Utekwa Rivers uphill

to an elevation of 4700 m on the slopes of Mt. Carstensz

(today Puncak Jaya) and then downhill, weeks after

the events had taken place, it is not surprising that no

mention was made of an obscure snake.

Furthermore, listing this snake along with a great

many other herpetological specimens from the Wollaston

Expedition (Boulenger 1914; O’Shea 2013) as originating

from the expedition’s launching point, Launch Camp,

is no different than when the Italian naturalist collector

Luigi Maria d’Albertis (1841-1901) listed the collection

locality for many of the herpetological specimens

collected quite far upriver on the Fly River during his

three expeditions (1875-77) as Kataw (or Katau),

which was actually his base camp on the south coast,

a mooring in the mouth of the Binaturi River, southern

Western Province, PNG, and demonstrably not their true

collection localities (d’Albertis 1879, 1880; O’Shea &

Kaiser 2018). Therefore, without proof that 7’ grandis

really does occupy the lower reaches of the Setekwa

River and should be aligned ecologically with this

Bonn zoological Bulletin 69 (2): 395-411

Fig. 9. The freshly killed Toxicocalamus ernstmayri (ZSM 55/2015), photographed by Paul Blum on 18 June 1976.

“

ar. $ " - aay

lowland locality, there is a higher probability that it was

obtained in an area that is ecologically a better match for

a species so similar to the montane 7! ernstmayri. We

consider the likeliest collection area to be much further

upstream, on the southern versant of the Sudirman Range,

and Wollaston would have collected it on the trip during

which he lost his diary, between 8 December 1912 and 9

March 1913.

The two main mountain ranges of Papua Province,

WNG, that combined form the Maoke Mountains,

formerly Snow Mountains, are the Jayawijaya Range in

the east, and the Sudirman Range to the west (Fig. 1). The

Jayawijaya Range, formerly known as the Orange Range,

extends for 380 km westward from the Star Mountains,

which straddle the border between Western and Sandaun

Provinces, PNG, and Papua Province, WNG. The highest

point in the Jayawiyaya Range is Puncak Mandala,

formerly Juliana Summit (4760 m). The Sudirman Range,

formerly the Nassau Range, is located to the west of the

Jayawijaya Range, and it extends the central cordillera

a further 692 km westwards, with its highest point at

Puncak Jaya, formerly the Carstensz Pyramid (4884 m),

a peak so high it was snow-capped until the early 1960s

and which still retains some small, but rapidly shrinking,

glaciers (Loffler 1982). Both ranges provide a wide

range of habitats and exhibit considerable vertebrate

diversity and endemicity (Allison 2007; Beehler 2007;

©ZFMK

Discovery of the second specimen of Toxicocalamus ernstmayri, the first from Papua Province, Indonesia 407

= Tie, ‘

~ &

Fig. 10. Portraits of (A) Alexander Frederick Richmond “Sandy” Wollaston (1875-1930) photographed in Dutch New Guinea in

1912, and (B) Cecil Boden Kloss (1877-1949) photographed in the field (date and location unknown). Both gentlemen display the

attire and character typical of early 20" Century explorers. Note their similarities: both bearded, both behatted, both with belted

field kit, both with walking canes (Wollaston always carried his ice-axe), both in cut-off shorts and puttees, both photographed

surrounded by field camp debris in an “active pose,” with one leg forward. Images courtesy of (A) Royal Geographical Society and

(B) Kevin Tan, National University of Singapore.

Brongersma & Venema 1962). The Jayawiaya and

Sudirman Ranges are separated, at an elevation of 1600—

1700 m, by the 80 km long and 20 km wide Baliem River

Valley, another biodiversity hotspot which was explored

by the 3% Archbold Expedition of 1938-39 (Archbold

et al. 1942), and other expeditions have followed

subsequently. The Baliem Valley has been called “an

important zoogeographic divide and a potential important

area of interchange” with regards to mammals (Helgen

2007: 736) and it may also act as a barrier between the two

montane herpetofaunas. If 7? ernstmayri and T. grandis

are ecologically similar species, large diurnal members

of a genus that feeds exclusively on annelids, especially

large earthworms, it is possible that they evolved through

allopatric speciation, 7’ ernstmayri in the Jayawijaya and

Star Mountains, and 7? grandis in the Sudirman Range. A

third relatively large, stocky and poorly known species,

T: pachysomus Kraus, 2009, is known from its holotype,

collected in the Cloudy Mountains at the southeastern

end of the Owen Stanley Range. It may also occupy a

similarly montane vermivorous niche, albeit at a lower

elevation of 715 m.

The discovery of 7! ernstmayri in the WNG mountains

and our sleuthing of historical records to better align

T. grandis with the ecology expected of a large

Toxicocalamus \end further support to the ‘highlands

Bonn zoological Bulletin 69 (2): 395-411

or islands’ biogeographic hypothesis for TZoxicocalamus

diversity. Our findings also provide important insights

into how these species may have evolved on the New

Guinea mainland, via allopatric speciation, one mountain

chain at a time, with the mountain ranges acting like

archipelagos in the sky, separating populations with

lowland or submontane valleys. The apparent allopatric

mountain-derived speciation in 7. ernstmayri and

7: grandis means that some of the widely distributed

montane species on mainland New Guinea may in reality

represent species-complexes, and with this in mind we

are currently examining 7: Joriae (Boulenger, 1898),

7. stanleyanus Boulenger, 1903, and 7! preussi more

closely. Toxicocalamus appears to provide a small yet

interesting example for the evolution of biodiversity on

the world’s largest tropical island.

Acknowledgements. The authors would like to thank Martyn

Low and Peter Ng (Lee Kong Chian Natural History Museum,

Singapore) and Kevin Tan (National University of Singapore),

for locating and providing, respectively, the photograph of Cecil

Boden Kloss. We also thank Marinus Hoogmoed (RMNH),

Ursula Bott (ZFMK), and Aaron Bauer (Villanova University)

for their help with tracking down a variety of references. We

thank Wolfgang Bohme and Gernot Vogel for their reviews

of the manuscript. The first author would like to give special

thanks to Frank Glaw and his colleagues at the ZSM for their

©ZFMK

408 Mark O’ Shea et al.

DUTCH EXPLORERS CANP, OETAKWA RIVER.

Fig. 11. Two photographs from the book A Naturalist in Cannibal Land by Albert Stewart Meek (1871-1943). (A) “Dutch

Explorers’ Camp, Oetakwa River” shows the lower reaches of the Oetakwa (Utekwa) River. This is either the unnamed camp

(Fig. 12: Location 3) at the confluence of the Utekwa and Setekwa Rivers, or Base Camp (Fig. 12: Location 4) at the confluence

of the Setekwa and Mamoa Rivers, since the Setekwa is a branch of the Utekwa'’. The river is wide and probably deep enough for

a motor launch, and canoes and European skiff-like boats for the journey up-stream are visible in the image. This location could

also be the same as Launch Camp, the location Wollaston listed as his purported collection locality for the holotype of 7. grandis.

(B) Meek’s campsite in the Maoke Mountains (historically known as the Snow Mountains) in 1910-11, captioned “My camp under

the Snow Mountains, Dutch New Guinea”. Meek is seen sitting on the tree stump. This photograph was taken on Meek’s second

venture into Dutch New Guinea, up the Eilanden (Island) River further to the east, so the camp is located in the Jayawijaya (then

Orange) Range, the eastern portion of the Maoke Mountains, while the Utekwa and Setekwa Rivers lead to the Sudirman (then

Nassau) Range, the western portion of the Maoke Mountains (see Fig. 1).

12 Meek (1913: 213) referred to Canoe Camp as being on “the right-hand branch of the Oetakwa,” which is the Setekwa River.

Discovery of the second specimen of Zoxicocalamus ernstmayri, the first from Papua Province, Indonesia 409

THE GEOGRAPHICAL JOURNAL I914

104.62

Mt Lemaire

10134

Betak, Aa a

Sketch Map to illustrate

EXPLORATIONS ©

IN '

DUTCH NEW GUINEA

A.F.R WoLLASTON.M.A,M.B.

1912-13. $

Scale 1: 600,000 or LInch « 12-6 Stat. Miles

5 ° 10 20

Route

Heights in: foot.

This map is from the author's plane table and prismatic

compass traverses, adjusted to ositions . shown thus >.

detarmined astronomically by Capt Van der Bie's

Expedition, 1910. a ;

Heights olen the route are from eae pom readings.

others are from clinometer angles,or taken from Dutch maps

Published tp the Royal Geographical Society

-DUTCH NEW GUINEA.

WOLLASTON.

Fig. 12. Map of the Explorations in Dutch New Guinea by A.F.R. Wollaston in 1912-13. This is the approximate area identified by

the white frame in Fig. 1. In the lowlands below the mountains there are six camps or locations indicated (numbered red circles):

(1) an unnamed camp at the mouth of the Utekwa River; (2) an anchorage on a wide bend in the Setekwa branch of the river; (3)

an unnamed camp at the confluence of the Utekwa and Setekwa Rivers; (4) Base Camp at the confluence of the Setekwa with

the Mamoa River; (5) River Camp on the Setekwa River; and (6) Canoe Camp at the base of the mountains. From Canoe Camp

the expedition struck out across land. It is proposed that “Launch Camp” is either synonymous with Base Camp (from where the

expedition was launched), or it could be the unnamed camp at the Utekwa-Setekwa confluence.

410

hospitality and the generous use of their facilities during his

2015 visit.

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