Bonn zoological Bulletin 69 (1): 1-9

2020 - Luu V.Q. et al.

https://do1.org/10.20363/BZB-2020.69.1.001

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:lsid:zoobank.org: pub: BOD2E47A-27A B-423B-A912-3649502BO00B8

New records and an updated list of reptiles from Ba Vi National Park,

Vietnam

Vinh Quang Luu"", Tuong Sy Dinh’, Oanh Van Lo*, Truong Quang Nguyen‘ & Thomas Ziegler*

"2.3 Faculty of Forest Resources and Environmental Management, Vietnam National University of Forestry, Xuan Mai,

Chuong My, Hanoi, Vietnam

‘Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet,

Hanoi, Vietnam

‘Graduate University of Science and Technology, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay,

Hanoi, Vietnam

°Cologne Zoo, Riehler Strasse 173, D-50735 Cologne, Germany

* Institute of Zoology, University of Cologne, Ziilpicher Strasse 47b, D-50674 Cologne, Germany

* Corresponding author: Email: qvinhfuv@yahoo.com.au

'urn:|sid:zoobank.org:author:052B40C7-8AFB-43A5-AF22-713DA7B5BBDD

> urn:Isid:zoobank.org:author:A0589B58-E392-4796-8601-317BOB555EAB

>urn:|sid:zoobank.org:author:D1531821-C4CC-451C-9E9B-3514042AD137

*urn:|sid:zoobank.org:author:822872A6-1C40-461F-AAOB-6A20EEQO6ADBA

°ur:|sid:zoobank.org:author:F7B14B87-EC39-43 14-82F8-1A6A250C3944

Abstract. We report eight new records of reptiles from Ba Vi National Park, Hanoi, Vietnam: Gekko palmatus, Boi-

ga guangxiensis, Gonyosoma prasinum, Lycodon futsingensis, L. ruhstrati abditus, Opisthotropis lateralis, Hebius cha-

paensis, and Pareas hamptoni. Our findings bring the total number of reptiles recorded from Ba Vi National Park to 50.

Key words. Reptiles, new records, distribution, Ba Vi National Park.

INTRODUCTION

Ba Vi National Park (NP) is located in Ba Vi District of

Hanoi and Luong Son and Ky Son districts of Hoa Binh

Province, with a total area of 12,023 ha. There are three

high peaks in the national park: the highest is Dinh Vua at

1,296 m above sea level (a.s.1.), followed by Tan Vien at

1,226 ma.s.l. and Ngoc Hoa at 1,120 ma.s.l. (Fig. 1). The

Ba Vi NP is characterized by evergreen forest and mixed

forest of coniferous and broadleaf at elevations above

600 ma.s.l. (Tran et al. 2001). In Ba Vi District, previous

studies documented a total of 42 species of reptiles and

most of them were recorded from Ba Vi National Park

(Nguyen et al. 2009). As a result of recent herpetological

field surveys we herein present eight new records of rep-

tiles from Ba Vi National Park.

MATERIAL AND METHODS

Field surveys were conducted in the Ba Vi NP by Vinh

Q. Luu, Oanh V. Lo, Ngoan V. Ha, Huy Q. Tran, Tuong

S. Dinh, Linh K. Luong, Nghia V. Ha and Le D. Phan

Received: 31.05.2019

Accepted: 12.01.2019

(hereafter V. Q. Luu et al.) in July, October and Novem-

ber 2018. Survey sites were selected at elevations rang-

ing from 400 to 800 m a.s.I. Three survey transects were

set up at three sites in the mixed forest of coniferous and

broadleaf plants: the Transect 1 along Ngoc Hoa stream

at elevations of ca. 400 m a.s.1., the Transect 2 in the for-

mer French Camping area at elevations of 600 m a.s.l.,

and the Transect 3 in the forest near Ruins of Old French

Church at elevations of ca. 800 m a.s.l. Specimens were

collected by hand or using a snake hook. Specimens were

euthanized in a closed vessel with a piece of cotton wool

containing ethyl acetate (Simmons, 2002), fixed in 80%

ethanol for four to stx hours, then later transferred to 70%

ethanol for permanent storage. The specimens were sub-

sequently deposited in the collection of the Vietnam Na-

tional University of Forestry (VNUF), Hanoi, Vietnam.

Taxonomic identification mainly followed Smith (1943),

Ziegler et al. (2007, 2008, 2018), Nguyen et al. (2009),

Vogel et al. (2009), Luu et al. (2013), Hecht et al. (2013),

Do et al. (2016), Gawor et al. (2016), Nguyen et al.

(2016), Le et al. (2018), and Pham et al. (2018).

Corresponding editor: W. Bohme

Published: 20.02.2020

2 Vinh Quang Luu et al.

a ok

Fig. 1. Map of Ba Vi National Park (black circle) in Hanoi City, northern Vietnam.

Abbreviations

SVL = snout-vent length: from tip of snout to anterior

margin of cloaca

TaL = tail length: from posterior margin of cloaca to tip

of tail

HL = head length: from the tip of snout to back of man-

dible

HW = head width: the widest portion of the head. Bilat-

eral scale counts were given as left/right.

RESULTS

Family Gekkonidae Gray, 1825

Gekko palmatus Boulenger, 1907

Palm Gecko / Tac ke chan vit (Fig.2a)

Specimens examined (n=3). One adult male VNUF

R.2018.19 (field number: BV.18.19) collected on 29

July 2018 in the fire protection and prevention station

(21°04’529N/105°22’719”E, at an elevation of 400 m

a.s.l.) and two adult females VNUF R.2018.12 (field

number: BV.18.12) collected on 26 July 2018 in the

ancient church area (21°04’409N/105°21’902”E, at an

elevation of 800 m as.l.) and VNUF R.2018.09 (field

number: BV.18.09) collected on 10 July 2018 in Ngoc

Bonn zoological Bulletin 69 (1): 1-9

Hoa cave (21°05’159” N/105°22’701”’E, at an elevation

of 400 m a.s.1.) by V. Q. Luu et al.

Morphological characters. The specimens from Ba Vi

NP agreed well with the description of Rosler et al. (2011):

SVL 71.3 mm (male) and 72.2—74.2 mm (females), TaL

12.9-78.6 mm (the female VNUF R.2018.12 with lost

tail); head longer than wide (HL 21.5-—37.8 mm, HW

13.4-14.6 mm in females; HL 19.9 mm, HW 14.7 mm

in the male); rostral wider than high (RW 2.5-—3.5 mm,

RH 0.9-1.4 mm in females; RW 2.2 mm, RH 1.2 mm in

the male); nostril in contact with rostral; interorbitals 31—

33; preorbitals 18-19; supralabials 11-13; infralabials

10-11; scale rows at midbody 121—125; turbercle rows

at midbody 7—10 in the female and 8 in the male; turber-

cles absent on dorsal surface of limbs; ventral scale rows

at midbody 41-50; scales in a line from mental to the

front of cloacal slit 166 in the male, 171—176 in females):

subdigital lamellae under first finger 11-12, under fourth

finger 12—15, under first toe 12—13, under fourth toe 13—

14; precloacal pores 26 in the male, absent in females;

postcloacal tubercle 1/1.

Coloration in life. Dorsal surface of head, body and

tail greyish with dark blotches on head and nape; 4-6

larger blotches on dorsum; flanks and limbs with small

light spots; dorsal surface of tail of the female VNUF

R.2018.12 with eight light bands and of the female

©ZFMK

New records and an updated list of reptiles from Ba Vi National Park, Vietnam eS)

VNUF R.2018.09 with 10 light bands, ventral side of tail

yellowish cream with black dots.

Ecological notes. The adult female VNUF R.2018.12

was found on the wall of the ancient church at 22:13.

Temperature was 23.9 °C and humidity was 71%. The

adult male was collected in a house at 24:00 while crawl-

ing on the wall. The female VNUF R.2018.09 was found

on the roadside cliff at 20:43 with the relative tempera-

ture being 26.5 °C and humidity about 55%.

Distribution. In Vietnam, this species was recorded from

Lao Cai Province in the North southwards to Quang Binh

Province (Nguyen et al. 2009, Hecht et al. 2013, Gawor

et al. 2016, Pham et al. 2018; Uetz et al. 2019). This is

the first record of Gekko palmatus for Ba Vi NP and for

Hanoi City.

Remarks. The specimens from Ba Vi differ from the de-

scription of Rosler et al. (2011) by having fewer scale

rows at midbody (121-125 versus 139-156).

Family Colubridae Oppel, 1811

Boiga guangxiensis (Wen, 1998)

Guangxi Cat Snake / Ran rao quang tay (Fig. 2b)

Specimen examined. One adult female, VNUF R.2018.7

(field number: BV.18.7) collected on 6 October 2018 in

the ancient church area (21°04’421”°N/105°21°865”’E, at

an elevation of 801 ma.s.l.) by V. Q. Luu et al.

Morphological characters. The specimen from Ba Vi

NP agreed well with the description of Ziegler et al.

(2007): SVL 1290 mm, TaL 435 mm; head longer than

wide (HL 31 mm, HW 21.1 mm), distinct from neck; pu-

pil round; internasal shorter than prefrontal; loreal 1/1;

preocular 1/1; postoculars 2/2; anterior temporals 2/2,

posterior temporals 2/3; supralabials 8/8, third to fifth in

contact with the eye, eighth largest: infralabials 13/12,

third to fifth in contact with the eye, eighth largest; first

to fourth (left side) and first to third (right side) bordering

chin shields; dorsal scale rows 23—21—15, smooth; ven-

trals 270; cloacal single; subcaudals 145, divided.

Coloration in life. Dorsum pale brown, with irregular

black cross-bars, venter greyish-white.

Ecological notes. The specimen was found at 20:09

while crawling on the forest ground near a tourist road.

Distribution. In Vietnam, this species has been recorded

from Lao Cai Province southwards to Dong Nai and Tay

Ninh provinces (Nguyen et al. 2009; Do et al. 2016; Phan

et al. 2018). This is the first record of Boiga guangxiensis

for Ba Vi NP and for Hanoi City. Elsewhere, this spe-

cies 1s known from southern China, Cambodia and Laos

(Nguyen et al. 2009; Neang et al. 2017; Uetz et al. 2019).

Bonn zoological Bulletin 69 (1): 1-9

Gonyosoma prasinum (Blyth, 1854)

Green bush ratsnake / Ran soc xanh (Fig. 2c)

Specimen examined. One adult female, WNUF

R.2018.30 (field number: BV3.18.10) — collect-

ed on 15 November 2018 in the ancient church area

(21°04°363”N/105°21°886”E at an elevation of 805 m

a.s.1.) by V. Q. Luu et al.

Morphological characters. The specimen from Ba Vi

NP agreed with the description of Hecht et al. (2013),

SVL 820 mm, Tal 330 mm; head longer than wide (HL

30.9 mm, HW 16 mm), head distinct from neck; pu-

pil round; internasal suture 1.6 mm; prefrontal suture

4.3 mm; loreal 1/1, not touching the eye; preocular 1/1;

postoculars 2/2; anterior temporals 2/2, posterior tempo-

rals 2/2; supralabials 9/9, fourth to sixth in contact with

the eye, eighth largest; infralabials 10/10; first to fourth

(both sides) bordering chin shields; dorsal scale rows 21—

19-15, keeled; ventrals 197; cloacal divided; subcaudals

106, divided.

Coloration in life. Dorsal surface of head, back and tail

green. The upper lip, lower throat, venter and lower sur-

face of tail light green. Each side of the ventrolateral fold

has a pale whitish stripe that runs from the neck to cloaca.

Ecological notes. The specimen was found in the eve-

ning on the wall of the ancient church.

Distribution. In Vietnam, this species was reported

from Lao Cai Province in the North southwards to Gia

Lai Province (Nguyen et al. 2009; Hecht et al. 2013; Le

et al. 2018). This 1s the first record of Gonyosoma prasi-

num for Ba Vi NP and for Hanoi City. Elsewhere, the

species 1s known from India, Southern China, Myanmar,

Laos, Thailand, Malaysia (Nguyen et al. 2009; Uetz et al.

2019).

Remarks. The specimen from Ba Vi differs from those in

the descriptions of Smith (1943) and Hecht et al. (2013)

by having more dorsal scale rows at neck (21-19-15 ver-

sus 19-19-15).

Hebius chapaensis (Bourret, 1934)

Sapa Flat-nosed Snake / Ran binh mii sa pa (Fig. 2d)

Specimen examined. One adult female, VNUF R.2018.8

(field number: BV.18.8) collected on 15 November 2018

(21°04’821”N/105°22’190”’E, at an elevation of 402 m

a.s.l.), by V. Q. Luu et al.

Morphological characters. The specimen from Ba

Vi NP agreed with the description of Le et al. (2018):

SVL 440 mm, TaL 140 mm; head longer than wide (HL

13.6 mm, HW 8.82 mm), distinct from the neck; pupil

©ZFMK

4 Vinh Quang Luu et al.

Fig. 2. Dorsal and dorsolateral views of the eight new records of reptiles from Ba Vi National Park, Hanoi, Vietnam. a. Gekko

palmatus (VNUF R.2018.12). b. Boiga guangxiensis (VNUF R.2018.7). ¢. Gonvosoma prasinum (VNUF R.2018.30). d. Hebius

chapaensis (VNUF R.2018.8). e. Lycodon futsingensis (VNUF R.2018.5). f. Lycodon ruhstrati abditus (VNUF R.2018.10). g.

Opisthotropis lateralis (VNUF R.2018.37). h. Pareas hamptoni (VNUF R.2018.18).

Bonn zoological Bulletin 69 (1): 1-9 ©ZFMK

New records and an updated list of reptiles from Ba Vi National Park, Vietnam 5

round; loreal 1/1, not touching the eye; preoculars 2/2;

postoculars 2/2: anterior temporals 1/1, posterior tempo-

rals 2/2; supralabials 9/9, fifth to sixth in contact with the

eye, seventh largest; infralabials 10/10, first to fifth (both

sides) bordering chin shields; dorsal scale rows 17—17—

17, feebly keeled; scales of the outer row enlarged; ven-

trals 170; cloacal divided; subcaudals 70, divided.

Coloration in life. Dorsal surface of head, body and tail

blackish grey, with two broader light yellow dorsolateral

stripes along the body; ventral surface and lower surface

of tail black.

Ecological notes. The specimen was found in the eve-

ning in a stream while being kept by a crab.

Distribution. In Vietnam, this species was reported from

Lao Cai, Son La, and Yen Bai provinces. This is the first

record of Hebius chapaensis for Ba Vi National Park and

for Hanoi City. Elsewhere, the species is known from

China (Uetz et al. 2019).

Remarks. Pararhabdophis chapaensis was original-

ly described from Sa Pa, Lao Cai Province by Bourret

(1934) and it was considered as a poorly known species,

known only from northwestern Vietnam and Yunnan

Province of China. This species was recently transferred

to the genus Hebius by Kizirian et al. (2018).

Lycodon futsingensis (Pope, 1928)

Futsing Wolf Snake / Ran khuyét fut-sing (Fig.2e)

Specimen examined. One adult male, VNUF R.2018.5

(field number: BV.18.5) collected on 6 October 2018 in

the ancient church area (21°04’383”°N/105°21°856”E, at

an elevation of 800 m a.s.I.) by V. Q. Luu et al.

Morphological characters. The specimen from Ba

Vi NP agreed well with the description of Vogel et al.

(2009): SVL 680 mm, Tal 160 mm; head distinct from

neck; pupil round; nasal divided; loreal 1/1, not touching

the eye; preocular 1/1; subocular absent; postoculars 2/2;

anterior temporals 2/2, posterior temporals 3/3; supral-

abials 8/8, third to fifth in contact with the eye, sixth larg-

est; infralabials 10/10, first to third (left side) and first to

fifth (right side) bordering chin shields; dorsal scale rows

17-17-15, smooth; ventrals 204; cloacal single; subcau-

dals 74, divided.

Coloration in life. Dorsum chocolate brown with 30

white brown bands on the body and 13 bands on the tail.

Ventral surface white with dirty brown marbling, dark

brown posteriorly.

Bonn zoological Bulletin 69 (1): 1-9

Ecological note. The specimen was found at 20:39 on

the forest ground. The relative temperature was about

22.6 °C and the humidity 60%.

Distribution. In Vietnam, this species was reported from

Lao Cai Province southwards to Da Nang City. This is the

first record of Lycodon futsingensis for Ba Vi NP and for

Hanoi City. Elsewhere, the species is known from China,

Laos, Japan, Taiwan, Myanmar (Hecht et al. 2013; Luu

et al. 2013; Nguyen et al. 2018; Uetz et al. 2019).

Lycodon ruhstrati abditus (Vogel, David, Pauwels, Su-

montha, Norval, Hendrix, Vu & Ziegler, 2009)

Mountain Wolf Snake / Ran khuyét dém (Fig.2f)

Specimen examined. One adult male, VNUF R.2018.10

(field number: BV.18.10) collected on 26 July 2018 in the

camping area (21°04’526’’N/105°22’189”E, at an eleva-

tion of 672 ma.s.l.) by V. Q. Luu et al.

Morphological characters. The specimen from Ba Vi

NP agreed with the description of Vogel et al. (2009),

SVL 696 mm, TaL 190 mm; TL 886 mm; body elongate;

head moderately distinct from neck, head longer than

wide (HL 19.4 mm, HW 12.2 mm) rather flattened; snout

projecting anteriorly beyond lower jaw; pupil vertically

oval; tail tapered and thin; loreal 1/1; loreal not in con-

tact with eye; supralabials 8/8, third to fifth in contact

with the eye, sixth largest; infralabials 9/8, first to fifth

(left side) and first to fourth (right side) bordering chin

shields; posterior chin shields a little shorter than anterior

ones; preocular 1/1; postoculars 2/2; anterior temporals

1/1, posterior temporals 3/2; dorsal scale rows 17-17-15,

keeled; ventrals 229; subcaudals 100, divided; cloacal

single.

Coloration in life. Dorsal surface of body greyish black

with 26 cross-bars, including two white bands near the

neck and 24 brown bands on body. Ventral surface white

with some small brown spots posteriorly. Dorsal surface

of tail greyish brown with 16 cream rings, extending to-

wards the lower surface of the tail.

Ecological notes. The specimen was found at 21:18 in

the shrub near a forest path. The surrounding habitat was

secondary forest mixed with bamboos. The relative tem-

perature was 25.1 °C and the humidity was 71%.

Distribution. In Vietnam, this species was previously

known from Vinh Phuc and Quang Binh provinces. This

is the first record of Lycodon ruhstrati abditus for Ba Vi

NP and for Hanoi City. Elsewhere, this species is known

from China and Laos (Vogel et al. 2009; Luu et al. 2013;

Uetz et al. 2019).

©ZFMK

6 Vinh Quang Luu et al.

Remarks. The specimen from Ba Vi NP differs from the

description of Vogel et al. (2009) by having more ven-

trals (229 versus 214—224) and the first body band start-

ing at ventral 24 (versus at ventrals 12—17).

Opisthotropis lateralis Boulenger, 1903

Tonkin Mountain Keelback / R&n tran bén (Fig. 2g)

Specimen examined. one adult male, VNUF R.2018.37

(field number: BV3.18.07) collected on 15 November

2018 (21°04’821”N/105°227190”E, at an elevation of

400 ma.s.l.) by V. Q. Luu et al.

Morphological characters. The specimen from Ba Vi

NP agreed with the description of Hecht et al. (2013):

SVL 470 mm, TaL 85 mm; head length larger than wide

(AL 17.5 mm, HW 10.3 mm), rostral broader than high;

internasals paired; prefrontal single; frontal longer than

wide, shorter than parietals, twice as broad as supraocu-

lar; nostrils directing upwards, in the upper part of single

nasal; internasal suture 1 mm: prefrontal suture 2.4 mm;

loreal 1/1, not touching the eye; preocular 1/1; postocu-

lars 2/2: anterior temporal 1/1, posterior temporals 2/2:

supralabials 9/9, fifth to sixth in contact with the eye,

eighth largest; infralabials 10/10, first to fourth (both

sides) bordering chin shields; dorsal scale rows 17—17—

17, keeled; ventrals 182; cloacal divided; subcaudals 50,

divided.

Coloration in life. Dorsal surface of head and body dark

greyish brown, ventral surface yellowish white.

Ecological notes. The specimen was found at night in a

stream after heavy rain.

Distribution. In Vietnam, this species was reported from

Cao Bang, Lang Son, Vinh Phuc, Quang Ninh, Bac Gi-

ang, Hai Duong, and Hoa Binh provinces (Nguyen et al.

2009; Hecht et al. 2013; Gawor et al. 2016). This is the

first record of Opisthotropis lateralis for Ba Vi National

Park and for Hanoi City. Elsewhere, the species is report-

ed from China (Nguyen et al. 2009; Uetz et al. 2019).

Family Pareatidae Romer, 1956

Pareas hamptoni (Boulenger, 1905)

Hampton’s Slug Snake / Ran h6 may ham-ton (Fig. 2h)

Specimens examined (n=2). One adult female VNUF

R.2018.18 (field number: BV.18.18) collected on 28 July

2018 in the orchid garden (21°04’529”N, 105°22’719”E,

at elevation of 719), and one adult male VNUF R.2018.04

(field number: BV.18.04) on 6 October 2018 in the an-

cient church area (21°04’397°°N/105°21°845”E, at an el-

evation of 400 maz.s.I.) by V. Q. Luu et al.

Bonn zoological Bulletin 69 (1): 1-9

Morphological characters. The specimen from Ba Vi

NP agreed with the description of Ziegler et al. (2007);

Pham et al. (2018); Nguyen et al. (2018); SVL 453-

480 mm, TaL 141-160 mm; body strongly compressed;

head distinct from neck; head longer than wide (HL

15.8-17.3 mm, HW 8.7—11.1 mm); nasal undivided; lo-

real 1/1, not touching the eye; preoculars 2/2; postoculars

2/2; suboculars 2/2, long and slender; anterior temporals

2/2, posterior temporals 3/2; supralabials 8/7; infralabials

8/8; mental groove absent; dorsal scales smooth in the

male and feebly keeled in the female; dorsal scale rows

15-15-15; ventrals 188-189; cloacal single; subcaudals

89-100, divided.

Coloration in life. Dorsal surface of head and body red-

dish brown, with vertical black body bands; ventral scales

from chin to lower surface of tail orange with black spots

in the female, dorsal surface of tail with black stripe.

Ecological notes. The female was found at 20:30 on the

road in the heavy rain and the male was found at 20:48

on the roadside.

Distribution. In Vietnam, this species has been record-

ed from Lao Cai Province in the North southwards to

Lam Dong and Dong Nai provinces (Nguyen et al. 2009;

Nguyen et al. 2018; Phan et al. 2018; Le et al. 2018). This

is the first record of P. hamptoni for Ba Vi NP and for

Hanoi City. Elsewhere, the species is known from Chi-

na, Myanmar, Laos, and Cambodia (Nguyen et al. 2009;

Uetz et al. 2019).

DISCUSSION

Our new findings of reptiles from Ba Vi National Park

bring the total species number of reptiles in this national

park to 50 (see Table 1, Apendix). In recent years, some

taxonomic changes have been made concerning reptiles

in Vietnam. Nguyen et al. (2009) reported Ophisau-

rus harti (Boulenger, 1899) from Ba Vi NP but it was

re-identified as Dopasia ludovici by Nguyen et al. (2011).

In this study, we provide the first record of Hebius cha-

paensis but did not find any H. khasiensis (Boulenger,

1890). Therefore, the previous record of H. khasiensis in

Ba Vi NP needs to be confirmed on the basis of voucher

specimens because H. chapaensis and H. khasiensis are

morphologically similar to each other.

In terms of conservation concern, among 50 recorded

species of reptiles, five species were listed in the IUCN

Red List (2019), eight species were listed in the Vietnam

Red Data Book (2007) and three species were listed in

the Governmental Decree No. 06 (2019).

©ZFMK

New records and an updated list of reptiles from Ba Vi National Park, Vietnam 7

ACKNOWLEDGEMENTS

We are grateful to the directorates of the Ba Vi National Park

for supporting our field work and issuing relevant permits. We

thank Ha V. Ngoan, Luong K. Linh, Ha V. Nghia, Huy Q. Tran,

Le D. Phan and K60 students of the Forest Resources Man-

agement for their assistance in the field. We thank E. Sterling

(New York) and K. Koy (Berkeley) for providing the map. This

research is partially supported by the Vietnam Academy of Sci-

ence and Technology (Project Code QTBY01.01/19-20) to T.Q.

Nguyen.

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zoogeography of the genus Gekko Laurenti, 1768 with the

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ma, Including the Whole of the Indo-Chinese Sub-Region.

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(2001) A survey of medicinal plants in Ba Vi National Park,

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Vogel G, David P, Pauwels OSG, Sumontha M, Norval G, Hen-

drix R, Vu NT, Ziegler T (2009) A revision of Lycodon ruh-

strati (Fischer 1886) auctorum (Squamata Colubridae), with

the description of a new species from Thailand and a new

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©ZFMK

APPENDIX

Table 1. Updated list of reptiles recorded from Ba Vi NP.

Data sources: 1: Nguyen et al. (2009); 2: This study; 3: Nguyen et al. (2011).

Vinh Quang Luu et al.

Decree 06 (2019) = Governmental Decree No 06/2019/ND-CP by the Government of Vietnam on the management of endangered

wild flora and fauna. Group IB: prohibited exploitation and use for commercial purpose and Group IIB: limited exploitation and

use for commercial purpose; RBVN (2007) = Vietnam Red Data Book. Part I. Animals. Descriptions of nationally endangered

species of wild animals. CR = Critically Endangered, EN = Endangered, VU = Vulnerable; IUCN (2019) = The IUCN Red List

of Threatened Species. CR = Critically Endangered, EN = Endangered, VU = Vulnerable, LR/nt = Lower Risk/Near Threatened,

* new provincial record; ** most probably Pelodiscus variegatus, see Farkas et al. (2019).

Species name Data source | IUCN (2019) | RBVN (2007) | Decree 06 (2019)

REPTILIA ——|

Squamata

Sauria

Agamidae

Acanthosaura lepidogaster (Cuvier, 1829) 12

Draco maculatus (Gray, 1845) 1

Pseudocalotes brevipes (Werner, 1904)

Physignathus cocincinus Cuvier, 1829 1 VU

Gekkonidae 1

Gekko palmatus Boulenger, 1907*

Gekko reevesii (Gray, 1831) l VU

Hemidactylus frenatus Dumérin & Bibron,1836 2

Scincidae

Eutropis longicaudatus (Hallowell, 1857)

Tropidophorus baviensis Bourret, 1939 1,2

Tropidophorus hainanus Smith, 1923 1

Anguidae =|

Dopasia ludovici (Mocquard, 1905) Nea es

Serpentes

Colubridae

Ahaetulla prasina (Boie, 1827)

Boiga guangxiensis Wen, 1998* 2

Boiga multomaculata (Bote, 1827)

Calamaria pavimentata Duméril, Bibron & Dumeéril, 1854 |

Calamaria septentrionalis Boulenger, 1890 VU

Coelognathus radiatus (Bote, 1827) VU

Gonyosoma boulengeri (Mocquard, 1897) 1

Gonyosoma prasinum (Blyth, 1854)* VU

Hebius chapaensis (Bourret, 1934)* 2

Hebius khasiensis (Boulenger, 1890)

Hebius sauteri (Boulenger, 1909) 1

Lycodon futsingensis (Pope, 1928)*

Lycodon meridionalis (Bourret, 1935) | Pe

Bonn zoological Bulletin 69 (1): 1-9 ©ZFMK

New records and an updated list of reptiles from Ba Vi National Park, Vietnam

Table 1. Continued

Species name

Lycodon ruhstrati abditus Vogel, David, Pauwels, Sumon-

tha, Norval, Hendrix, Vu & Ziegler, 2009*

Lycodon subcinctus Boie, 1827

Data source

IUCN (2019)

RBVN (2007) | Decree 06 (2019)

Oligodon cinereus (Gunther, 1864)

Oligodon eberhardti Pellegrin, 1910

Ptyas korros (Schlegel, 1837)

Ptyas major (Gunther, 1858)

Ptyas multicinctus (Roux, 1907)

Ptyas nigromarginata (Blyth, 1854)

Homalopsidae

Hypsiscopus plumbea (Boie, 1827)

Natricidae

Opisthotropis lateralis Boulenger, 1903*

Rhabdophis callichroma (Bourret, 1934)

Rhabdophis subminiatus (Schlegel, 1837)

Xenochrophis flavipunctatus (Hallowell, 1860)

Pseudoxenodontidae

Pseudoxenodon bambusicola Vogt, 1922

Elapidae

Bungarus fasciatus (Schneider, 1801)

Naja atra Cantor, 1842

Z| Za

IIB

Ophiophagus hannah (Cantor, 1836)

Sinomicrurus macclellandi (Reinhardt, 1844)

Pareidae

Pareas hamptoni (Boulenger, 1905)*

Pareas margaritophorus (Jan, 1866)

Viperidae

Ovophis monticola (Gunther, 1864)

Protobothrops mucrosquamatus (Cantor, 1839)

Trimeresurus albolabris Gray, 1842

Testudines

Geoemydidae

Cuora mouhotii (Gray, 1862)

Mauremys sinensis (Gray, 1834)

Trionychidae

| &

Z| Zz

IIB

Pelodiscus sinensis (Wiegmann, 1835)**

Bonn zoological Bulletin 69 (1): 1-9

©ZFMK

BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (1): 11-26

2020 - Filipiak A. et al.

https://do1.org/10.20363/BZB-2020.69.1.011

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:237955E5-9C3A-4222-8256-EEFOF80BFOF7

Helminths associated with terrestrial slugs in some parts of Europe

Anna Filipiak’’, Solveig Haukeland”’, Kamila S. Zajac’, Dorota Lachowska-Cierlik’ & Bjorn A. Hatteland* °

‘Institute of Plant Protection — National Research Institute, Wladystawa Wegorka 20, PL-60-318 Poznan, Poland

Norwegian Institute of Bioeconomy Research (NIBIO), Postboks 115, NO-1431 As, Norway

3 Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, PL-30-387 Krakow, Poland

‘Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, PL-30-387 Krakow, Poland

5Department of Biological Sciences, University of Bergen, PO Box 7800, NO-5020 Bergen, Norway

°Norwegian Institute of Bioeconomy Research (NIBIO), Plant Health and Biotechnology, NIBIO Ullensvang, NO-5781 Lofthus,

Norway

‘icipe, International Institute of Insect Physiology and Ecology, P.O. Box 30772-00100 Nairobi, Kenya

* Corresponding author: Email: a filipiak@iorpib.poznan. pl

'urn:|sid:zoobank.org:author:CS5FE638 | -E42B-4517-A9F5-99CCBC293D78

2urn:Isid:zoobank.org: author: FBDS54FE6-8950-47 1 8-8E9A-28A 6092DF6D9

3urn:Isid:zoobank.org:author:9F 5DCOSE-80CF-4FB2-A AD2-5 1D243834D80

*urn:lsid:zoobank.org:author:A5944069-0F77-4B9F-BE12-7B302385C7E2

>urn:Isid:zoobank.org:author:01C01518-F8C6-436A-BA3E-0C73EF95C1C5

Abstract. A survey of helminths associated with terrestrial slugs focusing on the invasive Arion vulgaris and the native A.

ater was conducted on populations from France, Germany, Netherlands, Norway and Poland. In total, 648 terrestrial slugs

were collected from 18 sample sites, and identified by means of morphological examination, dissection of genitalia and

molecular analysis using mitochondrial DNA. In addition to A. vulgaris and A. ater, also A. vulgaris/A. rufus hybrids and

A. ater/A. rufus hybrids were collected. Helminth species were identified based on morphological features and sequencing

of the 18S and ITS rDNA regions. The parasites included four nematode species: Alloionema appendiculatum, Angiosto-

ma sp., Phasmarhabditis hermaphrodita, Entomelas sp., two trematode species: Brachylaima mesostoma, Eurytrema sp.,

and one cestode (tapeworm) species: Skrjabinia sp. Alloionema appendiculatum was the most common helminth in the

investigated slug populations. Furthermore, we found higher prevalence of trematodes in the invasive A. vulgaris compa-

red with the native A. ater, while differences in the prevalence for nematodes were not as clear.

Keywords. Slugs, Arionidae, helminth parasites, nematodes, trematodes, tapeworm.

INTRODUCTION

Parasitism plays an important role in the ecology and

evolution of terrestrial gastropods (slugs and snails) influ-

encing the evolution of sexual reproduction, life-history

traits as well as host resistance leading to host-parasite

co-evolution. Parasites have a direct impact on life cycles

of their hosts, and the effects of parasites can be modu-

lated by environmental factors. Several studies have been

conducted on the impact of climate change on crop pests

in relation to natural enemies such as insect predators,

parasitoids, pathogenic microorganisms, and helminth

parasites (Gerard et al. 2013; Wilson et al. 2015). The

presence of helminths in slugs can be influenced by the

size, age and the spatial isolation of the host population

and by habitat characteristics (Baur & Baur 2005; Gerard

et al. 2013; Wilson et al., 2012; Wilson et al. 2015).

Different groups of helminths can be associated with

terrestrial gastropods, but slugs as hosts have been given

most attention (Ross et al. 2010a; Ross et al. 2010b; Ross

Received: 10.10.2019

Accepted: 14.01.2020

et al. 2016). Currently more than 25,000 species of nem-

atodes have been described, of which around 3,500 are

parasitic nematodes of invertebrates (Laznik et al. 2010).

Nematodes parasitise both slugs and snails, however slugs

are parasitised more frequently and by a greater diversity

of nematodes than snails (Mengert 1953). This 1s because

slugs usually inhabit soil, thus increasing their exposure

to nematodes (Morand et al. 2004; Ross et al. 2010a).

Currently, representatives of eight nematode families are

known to be associated with terrestrial slugs: Agfidae, Al-

aninematidae, Alloionematidae, Angiostomatidae, Cos-

mocercidae, Diplogasteridae, Mermithidae, and Rhab-

ditidae (particularly the genus Phasmarhabditis) (Ross

et al. 2017). These families are known to form a number

of different relationships with slugs, including parasitic

(specialist or generalist), phoretic and necromenic asso-

ciations (Ross et al. 2010b; Ross et al. 2017). Moreover,

trematodes, mites, sporozoa, ciliates, and cestodes have

also been described to interact with slugs (Stephenson &

Knutson 1966; Baur & Baur 2005).

Corresponding editor: B. Huber

Published: 20.02.2020

12 Anna Filipiak et al.

Terrestrial gastropods are considered to be one of the

most successful and diverse animal groups in terrestrial

ecosystems (Barker 2001). Many of them have become

invasive species in the context of expanding their range

of distribution and generating economic damages (e.g.,

Lissachatina fulica Bowdich, 1822 and Deroceras retic-

ulatum Miller, 1774) (Hammond & Byers 2002; Ross

et al. 2010a). One of the 100 most invasive species in Eu-

rope is Arion vulgaris Moquin-Tandon, 1855, commonly

known as the Spanish slug. It has probably been unin-

tentionally introduced into new habitats via plant matter,

packaging, and waste materials (Kozlowski 2007; Hat-

teland et al. 2013; Zajac et al. 2017). It is a major defoli-

ator of plants and causes severe damage in orchards and

gardens as well as in crops (Gren et al. 2009). This slug

has been assumed to originate from the Iberian Peninsula

and spread into Central Europe in the 1950s (Frank et al.

2002), although recent studies suggest a more northern

origin, possibly in France (Hatteland et al. 2015; Zemano-

va et al. 2016). Monitoring the spread of A. vulgaris is

difficult because the pest 1s morphologically similar to

the other closely related, large arionids (A. ater Linnaeus,

1758; A. rufus Linnaeus, 1758; A. magnus Torres Min-

guez, 1923; A. lusitanicus Mabille, 1868; A. flagellus

Collinge, 1893) that occur in Europe. Avion ater, A. rufus

and A. vulgaris can hybridise with each other (Roth et al.

2012; Dreijers et al. 2013) and introgression has readi-

ly been shown, especially between A. ater and A. rufus

(Hatteland et al. 2015; Zemanova et al. 2017). Moreover,

A. vulgaris may outcompete native slug species because

of its large size and high population densities (Frank

2003). Native slugs like A. ater and A. rufus have been

observed to decline and/or disappear in areas colonized

by invasive slugs such as A. vulgaris in continental Eu-

rope (Falkner 1990) and Scandinavia (B. A. Hatteland

pers. obs.) and a similar pattern seems to occur where

A. flagellus has been introduced in Britain (Davies 1987).

There are numerous hypotheses regarding what makes

species invasive. Release from natural enemies is regard-

ed to be an important factor supporting invasiveness by

many organisms (Torchin et al. 2003). The enemy release

hypothesis (ERH) states that the lack of natural enemies

in an invader’s introduced range influences its abundance

or impact (e.g., estimated using individual size, popula-

tion abundance, or propensity to displace native species)

(Torchin et al. 2003; Colautti et al. 2004). Torchin et al.

(2003) studied parasite burdens in 26 species of invasive

animals and found that most of them had fewer parasites

in their introduced areas compared with their home rang-

es. Indeed, it is less likely that hosts will spread parasites

into their introduced range since introduced populations

often originate from relatively small subsets of native

populations (and sometimes from uninfected life-histo-

ry stages) (Torchin et al. 2003). However, recent studies

have shown that A. vulgaris hosts a range of parasites in

introduced areas as well as relatively high parasitic loads

Bonn zoological Bulletin 69 (1): 11-26

compared with other native slug species (Ross et al.

2010a; Ross et al. 2016).

This study describes results on the diversity and dis-

tribution of helminths associated with A. vulgaris and

A. ater in Europe, 1.e., France, Germany, Netherlands,

Norway and Poland.

MATERIAL AND METHODS

Collection and identification of slugs and helminths

Slugs were collected from 18 sites in Europe (France,

Germany, Netherlands, Norway, Poland) in 2015 and

2016 from late August to October (Table 1). Sites were

selected based on information from local growers and

gardeners as well as advisory services in the region re-

garding the presence of slugs. At each site more than 10

slugs were collected and sent to the Institute of Environ-

mental Sciences (Jagiellonian University, Krakow, Po-

land) and Norwegian Institute of Bioeconomy Research

(NIBIO, As, Norway). Slugs were identified by means

of morphological examination guided by von Proschwitz

(2009), dissection of their genitalia and molecular anal-

ysis using a fragment of mitochondrial cytochrome c

oxidase subunit I (COI, mtDNA). The main features of

the genitalia in A. vu/garis are the small atrium, almost

symmetrical, one-partite, bursa copulatrix oval and a

free oviduct with a short, thin posterior end and a thick,

rapidly expanding anterior end with a large, asymmetric

ligula inside (Wiktor 2004). The main characteristics of

A. ater are the atrium and vagina considerably narrower

than spermatheca, oviduct narrow and the spermatheca

spherical (Welter-Schultes 2012). During the dissection

of slugs, a piece of tissue was taken for DNA extraction

and preserved in 96% ethanol at -80°C.

Slugs were checked for potential helminths, which

were identified using a combination of morphological

and molecular techniques. The helminths were first clas-

sified morphologically as nematodes or trematodes un-

der a stereomicroscope Olympus SZX10. For purposes

of molecular identification, all helminth samples (..e.,

adults, juveniles and cysts) were transferred to Eppen-

dorf tubes containing 70% ethanol. Each helminth was

introduced to a separate Eppendorf tube.

DNA isolation, amplification and sequencing

DNA extraction of slugs was performed using a commer-

cial DNA extraction kit (NucleoSpin® Tissue, Mache-

rey-Nagel, Duren, Germany), which uses a proteinase

K to digest proteins within cell membranes and columns

with silica membranes and buffers for cleaning extracted

DNA. PCR reactions were performed to obtain a frag-

ment of mitochondrial DNA with LCO1490/HC02198

primers (Folmer et al. 1994). A PCR reaction was per-

©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe 13

formed in a reaction mixture of 20 ul per each sample and

consisted of 3 ul of template DNA, 0.6 ul of each primer,

2 ul of 10x buffer, 13 wl of ddH20, 0.6 ul of 20 mM

dNTP and 0.2 ul of DreamTaq™ DNA Polymerase

(Thermo Fisher Scientific Inc., MA, USA). PCR condi-

tions included 5 min initial denaturation at 94°C and then

1 min denaturation at 94°C, 1 min 30 s annealing at 45°C

and 1 min 30 s elongation at 72°C for 5 cycles and then

1 min denaturation at 94°C, 1 min 30 s annealing at 50°C

and 1 min elongation at 72°C for 35 cycles followed by

a final elongation step for 5 min at 72°C. A volume of 5

ul sample of PCR product was run ona 1.0% agarose gel

for 30 min at 100 V to check DNA quality. PCR products

were cleaned up by commercial kit (NucleoSpin® Gel

and PCR Clean-up, Macherey-Nagel, Duiren, Germany).

The sequencing reaction was performed in a reaction

mixture of 10 pl per each sample and consisted of 2 ul of

template DNA, 5.85 ul of ddH20, 0.15 ul of primer, | ul

of 5x buffer and 1 ul of Terminator (BrightDye® Termi-

nator Cycle Sequencing Kit, MCLAB, South San Fran-

cisco, USA). Sequencing products were cleaned by using

a kit to remove terminators after sequencing reactions

(ExTerminator, A&A Biotechnology, Gdynia, Poland).

The sequencing reactions were performed in Molecular

Ecology Lab, Institute of Environmental Sciences (Jagi-

ellonian University, Krakow, Poland).

The genomic DNA of helminths was isolated with a

QIAamp DNA Micro Kit (Qiagen, Hilden, Germany)

according to the protocol provided by the manufactur-

er. DNA concentration and its purity were measured

using a NanoDrop spectrophotometer (Thermo Scien-

tific, Waltham, MA, USA). Polymerase chain reactions

(PCR) were performed on the partial 18S and ITS rDNA

regions. For nematodes, the ITS region was amplified us-

ing two sets of primers, i.e. 18S/26S (Vrain et al., 1992),

and N93/N94 (Nadler et al. 2005). Amplification of the

18S region was done with 24F/18P primers (Blaxter

et al. 1998). DNA of trematodes and cestodes was am-

plified using 3S/A28 primers for ITS2 region (Bowles

et al. 1995). PCR were performed in a reaction mixture

of 20 ul per each sample and consisted of 1 ul of template

DNA (100 ng of template DNA in 1 ul volume), | ul of

each forward and reverse primer (0.5 uM), 10 ul of 2x

DreamTaq™ Master Mix (Thermo Fisher Scientific Inc.,

MA, USA) and 7 ul of sterile distilled water. The PCR

amplifications were performed as described in Nermut’

et al. (2015) for the 18S/26S primers, Nadler et al. (2005)

for N93/N94 primers, Ross et al. (2010b) for 24F/18P,

and Prasad et al. (2007) for 3S/A28. A volume of 5 ul

sample of PCR product was run ona 1.5% agarose gel for

30 min at 100 V to check DNA quality. For rDNA partial

sequences, PCR products were sequenced with primers

used for PCR reactions. Sequencing was performed by

Genomed (Warsaw, Poland). Contigs assembled were de-

termined using BioEdit version 7.1.3.0 (Hall 1999).

Bonn zoological Bulletin 69 (1): 11-26

Phylogenetic analysis

The molecular phylogenetic status of helminths was

determined using BioEdit version 7.1.3.0 for multiple

sequence alignments (Hall, 1999). Multiple nucleotide

sequence alignments were generated using also other se-

quences deposited in GenBank showing the highest sim-

ilarity to the sequence of examined helminths (Appendix

I). The species names and GenBank accession numbers

of the sequences compared to the analyzed helminths are

shown in the phylograms. Phylogenetic trees were gen-

erated using MEGA X (Kumar et al. 2018) by maximum

likelihood (ML) and neighbour-joining (NJ) algorithms.

The base substitution model was determined for the 18S

and ITS using MEGA X under the Bayesian Information

Criterion. The percentage of replicate trees in which the

associated taxa clustered together in the bootstrap test

(1000 replicates) are shown next to the branches. Boot-

strap values above 60% were considered. Branch lengths

indicate evolutionary rates expressed as the number of

base differences per site.

Statistical analyses of prevalence

A comparison of parasite prevalence was carried out

between the invasive A. vulgaris and the native A. ater.

Hybrid slugs were not included since the number of spec-

imens was low. Generalized linear models (GLMs) with

binomial distribution were used to test possible differ-

ences in presence/absence of nematodes and trematodes,

respectively. All specimens from all investigated popu-

lations were included in the data set. Locality was used

as an explanatory factor in addition to slug species to

test the prevalence of the two different parasite groups.

Statistical analyses were performed in the software R (R

Core Team 2017).

RESULTS

Slug identification

All collected slugs were identified based on morphology

and genital morphology and sequences of cytochrome c

oxidase subunit I (COI) based on BLAST search results.

In total, 20 European populations were investigated,

which included 13 populations of A. vulgaris (Norway

— 9, Poland — 2, France — 1, Germany — 1), and five popu-

lations of A. ater (all in Norway). Additionally, two pop-

ulations of hybrids were collected, one population of A.

ater/A. rufus (Klepp, Norway) and one population of A.

vulgaris/A. rufus (Zoetermeer, Netherlands). From these

sites a total of 648 slugs of the genus Arion were col-

lected comprising 490 A. vulgaris, 92 A. ater, 44 A. vul-

garis/A. rufus hybrids and 22 A. ater/A. rufus hybrids

(Table 1).

©ZFMK

14 Anna Filipiak et al.

Helminth identification and prevalence

Helminths were found associated with slugs at 17 of the

18 sample sites in Europe (94.4%). A total of 501 (77.3%)

of 648 examined slugs were infected with helminths. All

slug taxa were infected with nematodes. Trematodes

were found in A. vulgaris and A. ater, and cestodes in

A. vulgaris and A. ater/A. rufus hybrids. In A. vulgaris,

359 specimens were infected with helminths, 1.e., 148

with nematodes (A/loionema appendiculatum Schneider,

1859; Angiostoma sp.; Phasmarhabditis hermaphrodita

Schneider, 1859), 198 with trematodes (Brachylaiama

mesostoma Rudolphi, 1803) and 13 with cestodes (Sk7j-

abinia sp.). In A. ater, 74 of the 92 dissected specimens

were infected with helminths, 1.e., 57 with nematodes

(A. appendiculatum, P. hermaphrodita, Angiostoma sp.

and Entomelas sp.), and 17 with trematodes (B. mesosto-

ma, Eurytrema sp.). In A. vulgaris/A. rufus, 43 of the 44

dissected slugs were infected with nematodes (A. ap-

pendiculatum). In the 22 dissected A. ater/A. rufus, 25

helminths were found, 1.e., 23 nematodes (A. appendicu-

latum, P. hermaphrodita), and 2 cestodes (Skrjabinia sp.)

(Table 1).

Nematodes were found in slugs at 14 of the 18 visited

sites (Norway — 11, France — 1, Netherlands — 1, Poland

— 1; 77.8% of all sample sites), trematodes at 12 of the

18 sites (Norway — 11, France — 1; 66.7% of all sample

sites), and cestodes at five of the 18 sites (Norway — 4,

Germany — 1; 27.8% of all sample sites). A total of four

nematode species (A. appendiculatum, Angiostoma sp.,

P. hermaphrodita, Entomelas sp.), two trematode species

(B. mesostoma, Eurytrema sp.) and one cestode (Skrja-

binia sp.) species were identified based on morpholog-

ical and molecular identification (Table 1; explanation

regarding the three species Entomelas sp., Eurytrema sp.,

and Skrjabinia sp. being listed as “genus sp.” is provided

in the paragraph “Phylogenetic analysis” below).

From sites positive for nematodes, A. appendiculatum

was recorded in 11 sites, P. hermaphrodita in eight sites,

Angiostoma sp. in five sites, and Entomelas sp. in only

one site. For sites positive for trematodes, B. mesostoma

was found 1n 11 sites, and Eurytrema sp. in only one site.

All cestodes were identified as Skrjabinia sp. (Table 1).

Phylogenetic analysis

In total, 501 sequences of the 18S and ITS rDNA regions

were generated (Table 1). These sequences represented

seven species of helminths from seven families. Sequenc-

es of the same species were identical across the 18S and

ITS rDNA regions, so only one representative sequence

was submitted for each taxon. Obtained sequences of hel-

minth species have been deposited in GenBank with the

following accession numbers: KY355082—K Y355088

(Table 2).

Bonn zoological Bulletin 69 (1): 11-26

BLAST search for three species sequences did not

show exact matches with other sequences deposited in

GenBank. The sequence of KY355086 revealed 92.98%

identity with Entomelas dujardini Maupas, 1916 (ac-

cession number: KF999591), sequence of KY355087

revealed 90.46% identity with Eurytrema pancreaticum

Janson, 1889 (accession number: KY490000), and se-

quence of KY355088 revealed 83.63% identity with

Skrjabinia cesticillus Molin, 1858 (accession number:

AY382321). Other sequences were characterised by

very low query coverage, resulting in low total scores

of BLAST searches. None of the sequences available

in GenBank were significantly similar to sequences ob-

tained in this study for these three species. Therefore,

these three detected helminths (1.e., Entomelas sp., Eu-

rytrema sp., and Skrjabinia sp.) are listed in the study as

“genus sp.”

Trees that were inferred from maximum-likelihood

(ML) and neighbor joining (NJ) revealed identical to-

pologies. Thus only maximum-likelihood results are pre-

sented along with bootstrap support from each method

of analysis (Figs 1-6). The molecular phylogenetic trees,

generated from partial 18S and ITS of rDNA regions with

ML and NJ algorithms, showed that the detected nema-

todes belonged to the species A. appendiculatum (Fig. 1)

and P. hermaphrodita (Fig. 2), and to the genus Angiosto-

ma sp., and Entomelas sp. The molecular phylogenetic

analysis revealed that these two nematodes are closely

related to Angiostoma margaretae and A. norvegicum

(Fig. 3), and Entomelas dujardini (Fig. 4). BLAST

search for Angiostoma sequences revealed 100% iden-

tity with Angiostoma margaretae Ross, Malan, Ivanova,

2011 (accession number: HQ115062) and Angiostoma

norvegicum Ross, Haukeland, Hatteland, Ivanova, 2017

(accession number: KU712560). Due to the fact that not

enough material was available for molecular work, the

28S and COI could not be used for the identification of

these nematodes. Therefore, the nematodes were listed as

Angiostoma sp. In the study of Singh et al. (2019), partial

18S and D2D3 sequences from the same DNA material

were also found to be almost 100% similar to sequences

from two different species. The evolutionary history of

A. appendiculatum was inferred by using the ML meth-

od based on the General Time Reversible (GTR) model,

and P. hermaphrodita, Angiostoma sp. and Entomelas sp.

based on the Tamura 3-parameter model.

The molecular phylogenetic trees, generated from par-

tial ITS of rDNA regions with ML and NJ algorithms,

showed that the detected trematodes belong to the spe-

cies B. mesostoma and to the genus Eurytrema sp.

(Fig. 5). The molecular phylogenetic analysis revealed

that this trematode is closely related to E. pancreaticum.

The ML method based on the GTR model indicate the

evolutionary history of B. mesostoma and Eurytrema sp.

The molecular phylogenetic trees, generated from par-

tial ITS of rDNA regions with ML and NJ algorithms,

©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe

Table 1. The prevalence (%) of infection of terrestrial slugs with parasite species collected in Europe

(N = number of slugs examined).

Locality

France:

Metz

Germany:

Gauting

Netherlands:

Zoetermeer

Norway:

Balestrand

Hana, Sandnes

Horten

Jensvoll, Bodo

Kjenneveien,

Fredrikstad

Kristiansand

Oslo

Lindhjem, Larvik

Manstad, Fredrikstad

Klepp

Vesteroya, Sandefjord

Bergen

Time, Bryne

Poland:

Igotomia

Rzeszow

GPS coordinates

49°71" N

6°10'59" BR

48°4"1"N

Mee

52°03’54’"N

4°30°31”E

61°10’39"N

6°24°14”"E

69°3171”"N

2022" E

59°25" N

LOE235 39 "E

67°16’5”N

14°24’°0”E

59°14’59""N

LOPS 30FE

58°10°1”N

8°00" E

59°57°41°N

10337 13°F

59°0’42”N

9°58°34”"E

59°16’°9”"N

10°46’°7” E

58°46’59""N

3°35°60”E.

59°6’14”"N

10°14°34”E

60°23°37°N

52238 EB.

58°43’59""N

5 BF 0" E

S0°5 200M

20°14’20”E

50°1’59”N

22 ON SE

Bonn zoological Bulletin 69 (1): 11-26

Slug species

Arion vulgaris

Arion vulgaris/

A. rufus

Arion ater

Arion vulgaris

Arion ater

Arion vulgaris

Arion ater/A. rufus

Arion ater

Arion vulgaris

112

100

Parasite species

Alloionema appendiculatum

Brachylaima mesostoma

Skrjabinia sp.

Alloionema appendiculatum

Brachylaima mesostoma

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Eurytrema sp.

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Brachylaima mesostoma

Phasmarhabditis hermaphrodita

Skrjabinia sp.

Brachylaima mesostoma

Angiostoma sp.

Brachylaima mesostoma

Entomelas sp.

Alloionema appendiculatum

Brachylaima mesostoma

Angiostoma sp.

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Angiostoma sp.

Brachylaima mesostoma

Skrjabinia sp.

Brachylaima mesostoma

Skrjabinia sp.

Alloionema appendiculatum

Brachylaima mesostoma

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Phasmarhabditis hermaphrodita

Skrjabinia sp.

Angiostoma sp.

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Angiostoma sp.

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Angiostoma sp.

Brachylaima mesostoma

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

Brachylaima mesostoma

Phasmarhabditis hermaphrodita

Alloionema appendiculatum

©ZFMK

Anna Filipiak et al.

Alloionema appendiculatum KJ&851561

wee Alloionema appendiculatum KY355082

100/100

97/a3

B17

100/100

67/61

100/100

Neoalloionema tricaudatum KR817921

Alloionema sp. KP204849

Neoalloionema sp. KX017496

Strongyloides procyonis AB205054

Strongyloides fuelleborni AB272235

Strongyloides callosciureus AB272229

Strongyloides robustus AB2/2232

Rhabditophanes sp. KP204851

0.10

Steinernema feltiae AB243439

Fig. 1. Unrooted maximum likelihood phylogeny of ITS rDNA regions for A//oionema appendiculatum. The scale bar represents

0.10 substitutions per nucleotide position. Only bootstrap values above 60% are shown.

0.10

Angiostoma margaretae MF 192968

—— Angiostoma norvegicum MK214816

Angiostoma gandavensis MK214815

Angiostoma dentiferum MK214814

Phasmarhabditis neopapillosa FJ516760

Phasmarhabditis hermaphrodita FJ516761

Phasmarhabditis hermaphrodita KM510202

Phasmarhabditis hermaphrodita KY355083

Agfa flexilis MK214813

Caenorhabditis elegans FJ589007

Fig. 2. Unrooted maximum likelihood phylogeny of ITS rDNA regions for Phasmarhabditis hermaphrodita. The scale bar rep-

resents 0.10 substitutions per nucleotide position. Only bootstrap values above 60% are shown.

showed that the detected cestodes belong to the genus

Skrjabinia sp. (Fig. 6). The molecular phylogenetic anal-

ysis (ML method based on the Hasegawa-Kishino- Yano

model) revealed that this cestode is most closely related

to S. cesticillus and Raillietina echinobothrida.

Bonn zoological Bulletin 69 (1): 11-26

Statistical analyses of prevalence

A tendency of higher prevalence of trematodes was found

in A. vulgaris populations compared with A. ater popu-

lations (Fig. 7; GLM, p=0.0618). On the other hand, a

©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe 17

Table 2. The accession numbers of examined slug-parasites with NCBI matches.

Parasite GenBank no. NCBI match Query | Percentage Source

family/species coverage | identity

Family:

Alloionematidae

Alloionema KY355082 Alloionema appendiculatum; 100 98.95 Nermut’ et al. (2015)

appendiculatum KJ851581

Family:

Rhabditidae

Phasmarhabditis KY355083 Phasmarhabditis hermaphrodita, | 100 100 =

hermaphrodita FJ516761

Family:

Angiostomatidae

Angiostoma sp. KY355084 Angiostoma margaretae;, 100 100 Ross et al. (2011)

HQ115062

Angiostoma norvegicum; 100 100 Ross et al. (2017)

KU712560

Family:

Rhabdiasidae

Entomelas sp

KY355086 Entomelas dujardini; 100 92.98 Tkach et al. (2014)

KF999591

Family:

Brachylaimidae

Brachylaima mesostoma

KY355085 Brachylaima mesostoma; 100 100 Heneberg ef al. (2016)

KT074964

Family:

Dicrocoeliidae

Eurytrema sp. KY355087 Eurytrema pancreaticum; 99 90.46 Su et al. (2018)

KY490000

Family:

Davaineidae

Skrjabinia sp. KY355088 Skrjabinia cesticillus;

AY382321 81 83.63 —

somewhat lower prevalence of nematodes in A. vulgaris

than in A. ater (Fig. 8) was revealed, although this differ-

ence was not significant (GLM, p=0.1569).

DISCUSSION

This study presents the occurrence of helminths associ-

ated with two slug species: A. vulgaris and A. ater, as

well as A. vulgaris/A. rufus hybrids, and A. ater/A. rufus

hybrids in some parts of Europe, 1.e., France, Germany,

Netherlands, Norway and Poland. Previous studies on the

diversity and distribution of slug parasites have focused

on the presence of nematodes in slugs (Mengert 1953;

Gleich et al. 1977; Charwat & Davies 1999; Laznik et al.

2009; Ross et al. 2010b; Ross et al. 2011; Ivanova et al.

2013; Ross et al. 2016; Singh et al. 2019). In our study, a

total of seven species of helminths were found to be asso-

ciated with these slugs including nematodes, trematodes

Bonn zoological Bulletin 69 (1): 11-26

and one cestode species. The nematodes were identified

to Alloionema appendiculatum, Angiostoma sp., Phas-

marhabditis hermaphrodita, Entomelas sp., trematodes

were identified as Brachylaima mesostoma, Eurytrema

sp., and the cestode species was identified as Skrjabinia

sp. We found a tendency for higher prevalence of trem-

atodes in A. vulgaris compared with the native A. ater.

However, we did not find the same pattern in terms of

prevalence for nematodes.

Slug-parasitic nematodes were found in all organs of

the body cavity and also on foot muscles, typical of A. ap-

pendiculatum. The most intensively studied species of

slug-parasitic nematode of agricultural and horticultural

crops is P. hermaphrodita. In our survey, P. hermaphro-

dita was found in eight of the 18 sample sites examined,

and was found to parasitize both A. ater, A. vulgaris, as

well as A. ater /A. rufus hybrids. Only juveniles of P. her-

maphrodita were detected in our study. Within the Rhab-

ditidae family, Phasmarhabditis is the only genus that

©ZFMK

18 Anna Filipiak et al.

Angiostoma margaretae HQ115062

Angiostoma dentiferum MK214806

Phasmarhabditis hermaphrodita FJ516755

8v@8L_ Phasmarhabditis neopapillosa FJ516754

Phasmarhabditis californica KM510210

sasa| Angiostoma dentifera FJ516752

Phasmarhabditis papillosa KM510211

Oscheius chongmingensis EU273597

Oscheius insectivora AF083019

Pellioditis marina AF08&3021

Angiostrongylus vasorum AJ920365

Heterorhabditis indica LN611143

Steinernema feltiae FJ381667

——___—1

0.020

Fig. 3. Unrooted maximum likelihood phylogeny of 18S rDNA regions for Angiostoma sp. The scale bar represents 0.020 substi-

tutions per nucleotide position. Only bootstrap values above 60% are shown.

Rhabdias bufonis KF999593

Rhabdias engelbrechti MG428406

Rhabdias bulbicauda KF999600

Rhabdias bermani KF999610

Rhabdias elegans KF999604

Rhabdias pseudosphaerocephala EU836873

L Rhabdias bakeri EU360831

Rhabdias tarichae MH023523

Rhabdias picardiae MG195567

Rhabdias sylvestris KJO18/77

Pneumonema sp. KF999603

Pneumonema tiliquae KF999611

Entomelas entomelas KF999592

Entomelas sp. KF999601

- Entomelas dujardini KF999591

Entomelas sp. KY355086.

99!

Sfeinernema feltiae AB243439

I j

0.10

Fig. 4. Unrooted maximum likelihood phylogeny of ITS rDNA regions for Entomelas sp. The scale bar represents 0.10 substitu-

tions per nucleotide position. Only bootstrap values above 60% are shown.

Bonn zoological Bulletin 69 (1): 11-26 ©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe 19

Leucochloridium paradoxum KP903688

' Leucochloridium sp. AY258145

Leucochloridium vogtianum KP903700

Leucochloridium perturbatum KP903707

Brachylaima sp. JX010634

Brachylaima mesostoma KT074964

Brachylaima mesostoma KY355085

Clinostomum album KU708008

Clinostomum marginatum KU708007

greet Macroderoides sp. HQ680850

__ 9498] Macroderoides texanus EU&50398

Macroderoides flavus HQ680851

Dicrocoelium hospes EF 102026

Lutztrema attenuatum KU563718

Eurytrema sp. KY355087

Concinnum ten AB521802

Eurytrema pancreaticum KY490000

Opisthorchis viverrini MG797539

0.10

Fig. 5. Unrooted maximum likelihood phylogeny of ITS rDNA regions for Brachylaima mesostoma and Eurytrema sp. The scale

bar represents 0.10 substitutions per nucleotide position. Only bootstrap values above 60% are shown.

Railletina echinobothrida MH122787

_ 84/96 Skrabinia cesticillus AY382321

S08 Skrabinia sp. KY355088

Parorchites zederi KP893424

Hymenolepis nana LC389873

Mesocestoides litteratus MH936660

— Mesocestoides sp. MH936661

Proteocephalus torulosus AY375549

Raillietina sp. MK201802

Raillietina beveridgei AY382318

a7199 Raillietina dromaius AY382320

88/97| Raillietina australis AY382317

“°L__ Raillietina chiltoni AY382319

Hymenolepis diminuta MF 143799

TOO/TOO]

0.20

Fig. 6. Unrooted maximum likelihood phylogeny of ITS rDNA regions for Skrjabinia sp. The scale bar represents 0.20 substitutions

per nucleotide position. Only bootstrap values above 60% are shown.

Bonn zoological Bulletin 69 (1): 11-26 ©ZFMK

20 Anna Filipiak et al.

0.6

Trematode prevalence

0.0

Arion ater

Anon vulgans

Fig. 7. Boxplot of trematode prevalence (proportionally) in

populations of Arion vulgaris and A. ater.

is considered to be truly parasitic towards slugs. P. her-

maphrodita is known to be capable of killing many spe-

cies of slugs from several families (Morand et al. 2004;

Wilson et al. 2012). The nematode has been formulated

into an effective biological control agent (Tan & Grewal

2001; Wilson et al. 2015). Infective dauer juveniles (a

non-feeding survival stage) of P. hermaphrodita seek out

the host through a combination of both chemotactic and

chemokinetic responses towards chemical attractants in

slug feces and mucus from the foot and mantle (Rae et al.

2006; Hapca et al. 2007).

Another nematode known to be associated with ter-

restrial gastropods is Alloionema appendiculatum. This

nematode has a broad geographical distribution and has

been found in areas including Europe, Australia and

North America (Morand et al. 2004; Laznik et al. 2009;

Nermut’ et al. 2015). In our study, A. appendiculatum

was found in 11 of the 18 sample sites examined. The

nematode was found to parasitize A. ater, A. vulgaris,

and A. ater /A. rufus and A. vulgaris/A. rufus hybrids. A.

appendiculatum is a common juvenile parasite of many

terrestrial gastropods. This nematode has both parasitic

and free-living life stages. During the parasitic cycle,

third-stage juveniles (J3) enter the slug’s body through its

foot, where the nematodes moult to the fourth-stage juve-

nile (J4) which become encapsulated in the pedal muscu-

lature. These juveniles then exit the slug and moult into

free-living immature adults (Cabaret & Morand 1990;

Laznik et al. 2009). In our study we also identified An-

giostoma sp., present in five of the 18 sample sites exam-

ined. The nematode was found to parasitize both A. ater

and A. vulgaris. With the recent discovery of A. gandav-

ensis, the total number of described species of the genus

Bonn zoological Bulletin 69 (1): 11-26

0.6 0.8 1.0

Nematode prevalence

0.4

0.2

0.0

Arnon ater

Arion vulgaris

Fig. 8. Boxplot of nematode prevalence (proportionally) in

populations of Arion vulgaris and A. ater.

Angiostoma is now 19, of which 15 are described from

molluscan hosts (Singh et al. 2019). International surveys

reveal that molluscan angiostomatids are present in Eu-

rope, North America, Africa, South-East Asia and New

Zealand (Ivanova & Wilson 2009; Ivanova & Spiridonov

2010; Ross et al. 2010a, b; Ross et al. 2011; Ross et al.

2017).

The other nematode identified in our study was En-

tomelas sp. The nematode was only found in one of the

18 sample sites examined, and only in the native A. ater.

Entomelas sp. is classified in the family Rhabdiasidae,

which includes up to 100 known nematode species par-

asitic in amphibians and reptiles. All share some mor-

phological characters but the most remarkable feature

of rhabdiasids is the regular alternation of parasitic and

free-living generations (heterogony) in their life cycles

(Tkach et al. 2014). Entomelas dujardini and E. entome-

las are commonly associated with Anguis fragilis. Ex-

perimental infection of the slugs Deroceras reticulatum

(Agriolimacidae) and Arion subfuscus (Arionidae) with

infective larvae of E. entomelas and E. dujardini has re-

vealed that both slug species are classed as paratenic (eu-

paratenic) hosts for these nematode species (Kuzmin &

Sharpilo 2000).

Among the detected parasites were also trematodes,

1.e., B. mesostoma and Eurytrema sp. We found B. me-

sostoma in 11 of the 18 sample sites examined and it

was found in both A. ater and A. vulgaris. The genus

Brachylaima contains 72 species that parasitize mam-

mals and birds as definitive hosts around the world, ex-

cept Antarctica. Terrestrial gastropods are involved as

first and second intermediate hosts. They are important

from a public health point of view, as they cause diseases

©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe 2

in humans like hemorrhagic enteritis, diarrhea, inflam-

mation of the bile ducts, and anemia (Sirgel et al. 2012;

Suleman & Khan 2016; Valente et al. 2016).

The trematode Eurytrema sp. was found in one of the

18 sample sites, in A. ater only. Species of Eurytrema are

natural parasites of domestic animals (e.g., cattle, goats,

sheep, pigs, dogs) and wild ruminants (such as buffalos,

camels, deer) as well as monkeys and humans parasit-

izing pancreatic ducts and bile ducts. Rarely, terrestrial

snails of various species (e.g., Bradybaena similaris) are

intermediate hosts for these parasites (Pinheiro & Am-

ato 1994). These parasites often cause epithelial hyper-

plasia, hypertrophy of pancreatic ducts, and periductal

fibrosis that lead to eurytrematosis (Cai et al. 2012; Man-

ga-Gonzalez & Ferreras 2014).

Terrestrial slugs can also be associated with tape-

worms. One of the most common tapeworm affecting

poultry systems is Davainea proglottina and the inter-

mediate hosts are gastropods. Tapeworm segments that

pass through poultry feces are ingested by snails and

slugs (of the genera Agriolimax, Arion, Cepaea and Li-

max) and within three weeks a cysticercoid is produced.

Adult tapeworms are produced in the infected host 8-15

days after ingestion of an infected snail or slug (Jordan &

Pattison 1996).

In our study, the tapeworm Skrjabinia sp. was found in

five of the 18 sample sites examined. The tapeworm was

found in A. vulgaris and A. ater/A. rufus hybrids. Skrj-

abinia is a genus of tapeworms that includes helminth

parasites of vertebrates, mostly of birds. One of the most

common parasitic platyhelminths in modern poultry fa-

cilities throughout the world is S. cesticillus. It is a rela-

tively harmless species among intestinal cestodes in spite

of a high prevalence. Sometimes called “broad-headed

tapeworm”, it infects the small intestine of chicken and

occasionally other birds, such as guinea fowl and tur-

key, which are generally in close proximity to backyard

poultry (Kaufmann 1996; Morishita & Schaul 2007).

Our study showed that, in some cases, a single slug was

infected with up to two different species of parasites

(i.e., by two species of nematodes or by one species of

nematode and one species of trematode). Two different

parasites detected from one host was also sometimes

observed in a study by Singh et al. (2019). Moreover,

our study confirmed that endoparasitic helminths appear

to have a broad host range of slug species (Ross et al.

2010b; Singh et al. 2019). Alloionema appendiculatum

was reported from all four different slug species, P. her-

maphrodita from three, Angiostoma sp. from two, B. me-

sostoma from two, and Skrjabinia sp. also from two.

The enemy release hypothesis suggests that species

become invasive due to a lack of enemies in their in-

troduced areas (Mitchell & Power 2003; Torchin et al.

2003). However, Colautti et al. (2004) suggested that

there are strong, enemy-specific effects on host survival

and that hosts have developed tailored defenses. Thus,

Bonn zoological Bulletin 69 (1): 11-26

one may expect that it is the release from specific ene-

mies that causes direct changes to survivorship, fecundi-

ty, biomass, or demographic variables that really matters.

Alternatively, the loss of enemies against which a host

is well defended would be of little consequence for the

host populations (Colautti et al. 2004). We found a con-

trasting pattern in our study, suggesting that the preva-

lence of trematodes in invasive slugs is higher than in

native species. The role of trematodes in slugs should be

further investigated including comparative studies with

nematodes.

The anthropogenic spread of slugs may potentially

lead to a higher degree of mixing of slug populations

than would occur when spread naturally. This may also

include the spread of parasites along with their slug

hosts, which may have implications for the prevalence

of trematodes and cestodes that use slugs as intermediate

hosts and thus may become more common in domestic

mammals such as cattle and sheep.

Acknowledgements. The authors would like to thank Kar-

in Westrum, Henrik Anztée-Hyllseth, Elisa Baluya Gauslaa

(NIBIO, Norway) and Daniel Kubler (Jagiellonian University,

Poland) for help in dissections of slugs. The authors would fi-

nally like to thank two anonymous reviewers for valuable com-

ments and Bernhard A. Huber (Bonn zoological Bulletin) for

useful suggestions during the peer review.

Financial support. This work was supported by the Pol-

ish-Norwegian Research Programme (Pol- Nor/201888/77).

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©ZFMK

APPENDIX

Anna Filipiak et al.

Species name of helminths, GenBank accession numbers and region of sequences used for phylogenetic analyses.

Fig. number

Species name

Alloionema appendiculatum

Neoalloionema tricaudatum

Alloionema sp.

Neoalloionema sp.

Strongyloides procyonis

Strongyloides fuelleborni

Strongyloides callosciureus

Strongyloides robustus

Rhabditophanes sp.

Steinernema feltiae

Angiostoma margaretae

Angiostoma norvegicum

Angiostoma gandavensis

Angiostoma dentiferum

Phasmarhabditis neopapillosa

Phasmarhabditis hermaphrodita

Agfa flexilis

Caenorhabditis elegans

Angiostoma margaretae

Angiostoma sp.

Angiostoma norvegicum

Angiostoma dentiferum

Phasmarhabditis hermaphrodita

Phasmarhabditis neopapillosa

Phasmarhabditis californica

Angiostoma dentifera

Phasmarhabditis papillosa

Oscheius chongmingensis

Oscheius insectivora

Pellioditis marina

Angiostrongylus vasorum

Heterorhabditis indica

Steinernema feltiae

Rhabdias bufonis

Rhabdias engelbrechti

Bonn zoological Bulletin 69 (1): 11-26

GenBank

accession n°

KJ851581

KY355082

KR817921

KP204849

KX017496

AB205054

AB272235

AB272229

AB272232

KP204851

AB243439

MF192968

MK214816

MK214815

MK214814

FJ516760

FJ516761

KM510202

KY355083

MK214813

FJ589007

HQ115062

KY355084

KU712560

MK214806

FJ516755

FJ516754

KM510210

FJ516752

KMS510211

EU273597

AF083019

AF083021

AJ920365

LN611143

FJ381667

KF999593

MG428406

Region

18S-ITS1-5.8S-ITS2-28S8

18S-ITS1-5.8S-ITS2-28S

18S-ITS1-5.8S-ITS2-28S8

18S-ITS1-5.8S-ITS2-288

18S-ITS1-5.8S-ITS2-28S8

18S-ITS1-5.8S-ITS2

ITS1-5.8S-ITS2

18S-ITS1-5.8S-ITS2

18S-ITS1-5.8S-ITS2-28S8

18S

ITS1-5.8S-ITS2-28S

18S-ITS1-5.8S-ITS2-28S8

Source

Nermut’ et al. (2015)

This study

Ivanowa et al. (2016)

Nermut’ et al. (2015)

Unpublished

Sato et al. (2006)

Sato et al. (2007)

Nermut’ et al. (2015)

Kuwata et al. (2006)

Unpublished

Singh et al. (2019)

Unpublished

Tandigan et al. (2014)

This study

Singh et al. (2019)

Imai et al. (2009)

Ross et al. (2011)

This study

Ross et al. (2017)

Singh et al. (2019)

Ross et al. (2010b)

Tandigan ef al. (2014)

Ross et al. (2010b)

Tandigan ef al. (2014)

Liu et al. (2012)

Unpublished (2002)

Unpublished

Chilton et al. (2006)

Unpublished

Tkach et al. (2014)

Kuzmin et al. (2017)

©ZFMK

Helminths associated with terrestrial slugs in some parts of Europe 25

Fig. number | Species name yeas n° Region Source

Rhabdias bulbicauda KF999600 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Rhabdias bermani KF999610 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Rhabdias elegans KF999604 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Rhabdias pseudosphaerocephala | EU836873 ITS1-5.8S-ITS2-28S Dubey &Shine (2008)

Rhabdias bakeri EU360831 18S-ITS1-5.8S-ITS2-288 | Dare et al. (2008)

Rhabdias tarichae MH023523 18S-ITS1-5.8S-ITS2-288S | Johnson er al. (2018)

Rhabdias picardiae MG195567 18S-ITS1-5.8S-ITS2-28S | Svitin et al. (2018)

Rhabdias sylvestris KJ018777 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Pneumonema sp. KF999603 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Pneumonema tiliquae KF999611 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Entomelas entomelas KF999592 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Entomelas sp. KF999601 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Entomelas dujardini KF999591 ITS1-5.8S-ITS2-28S Tkach et al. (2014)

Entomelas sp. KY355086 ITS1-5.8S-ITS2-28S This study

Steinernema feltiae AB243439 18S-ITS1-5.8S-ITS2-28S | Kuwata et al. (2006)

5 Leucochloridium paradoxum KP903688 ITS1-5.8S-ITS2-28S Heneberg et al. (2016)

Leucochloridium sp. AY258145 ITS1-5.8S-ITS2-28S Casey et al. (2003)

Leucochloridium vogtianum KP903700 ITS1-5.8S-ITS2-28S Heneberg et al. (2016)

Leucochloridium perturbatum KP903707 5.8S-ITS2-28S Heneberg et al. (2016)

Brachylaima sp. JX010634 5.8S-ITS2-28S Unpublished

Brachylaima mesostoma KT074964 5.8S-ITS2-28S Heneberg et al. (2016)

Brachylaima mesostoma KY355085 5.8S-ITS2-28S8 This study

Clinostomum album KU708008 18S-ITS1-5.8S-ITS2-28S | Rosser et al. (2017)

Clinostomum marginatum KU708007 18S-ITS1-5.8S-ITS2-28S | Rosser et al. (2017)

Macroderoides sp. HQ680850 18S-ITS1-5.8S-ITS2-28S | Tkach & Kinsella (2011)

Macroderoides texanus EU850398 18S-ITS1-5.8S-ITS2-28S | Tkach et al. (2008)

Macroderoides flavus HQ680851 18S-ITS1-5.8S-ITS2-28S | Tkach & Kinsella (2011)

Dicrocoelium hospes EF102026 5.8S-ITS2-28S Maurelli et al. (2007)

Lutztrema attenuatum KU563718 5.8S-ITS2-28S8 Unpublished

Eurytrema sp. KY355087 5.8S-ITS2-28S8 This study

Concinnum ten ABS521802 5.8S-ITS2-28S Sato et al. (2010)

Eurytrema pancreaticum K Y490000 18S-ITS1-5.8S-ITS2-288S | Su et al. (2018)

Opisthorchis viverrini MG797539 5.8S-ITS2-28S Sanpool et al. (2018)

6 Raillietina echinobothrida MH122787 5.8S-ITS2-28S8 Unpublished

Skrjabinia cesticillus AY382321 5.8S-ITS2-28S8 Unpublished

Skrjabinia sp. KY355088 5.8S-ITS2-28S This study

Parorchites zederi KP893424 18S-ITS1-5.8S-ITS2-28S | Kleinertz et al. (2014)

FHymenolepis nana LC389873 ITS2 Banzai et al. (2018)

Mesocestoides litteratus MH936660 ITS1-5.8S-ITS2-28S Unpublished

Mesocestoides sp. MH936661 ITS1-5.8S-ITS2-28S Unpublished

Proteocephalus torulosus AY375549 5.8S-ITS2-28S Scholz et al. (2003)

Bonn zoological Bulletin 69 (1): 11-26 ©ZFMK

Anna Filipiak et al.

GenBank

Fig. number | Species name necestiin na? Region Source

Raillietina sp. MK201802 5.8S-ITS2 Unpublished

Raillietina beveridgei AY382318 5.8S-ITS2-28S8 Unpublished

Raillietina dromaius AY382320 5.8S-ITS2-28S Unpublished

Raillietina australis AY382317 5.8S-ITS2-28S Unpublished

Raillietina chiltoni AY382319 5.8S-ITS2-28S Unpublished

Hymenolepis diminuta MF 143799 ITS1-5.8S-ITS2 Unpublished

Bonn zoological Bulletin 69 (1): 11-26

©ZFMK

Bonn zoological Bulletin 69 (1): 27-44

2020 - Das P. et al.

https://do1.org/10.20363/BZB-2020.69. 1.027

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:C5E25AC5-EF44-43 F6-A4DC-69858D3C8EC8

The Ladybird Beetles (Coleoptera: Coccinellidae) of Arunachal Pradesh, East Himalaya, India

with new combinations and new country records

Priyanka Das', Kailash Chandra” & Devanshu Gupta*"

2.3 Zoological Survey of India, M Block, New Alipore, Kolkata-700,053

* Corresponding author: Email: devanshuguptagb4102@gmail.com

'urn:|sid:zoobank.org:author:DCB2893D-CFF9-43A4-9508-0C47389F43E9

2urn:Isid:zoobank.org:author: D26C02D0-9F20-44A E-A 19C-B7AC83B3F67A

3urn:Isid:zoobank.org:author:529E2996-6242-487E-89FD-66DSAEC2486F

Abstract. The present communication on ladybird beetles (Coccinellidae) of Arunachal Pradesh (AP), India, a part of

Eastern Himalayan biodiversity hotspot, reports a total of 44 species belonging to 22 genera and 6 tribes. Thirty-eight

species were examined and illustrated, including three new species records from India: ///eis shensiensis Timberlake,

1943, Afissa rana (Kapur, 1958), and Henosepilachna vigintioctomaculata (Motschulsky, 1857) (first confirmed record

from India), and 26 species as new to Arunachal Pradesh. Epilachna gibbera Crotch, 1874, E. mystica Mulsant, 1850, and

E. undecimspilota Hope, 1831 are transferred to the genus Afissa.

Key words. Checklist, new distributional records, taxonomy, Himalaya.

INTRODUCTION

The family Coccinellidae include around 6,000 described

species belonging to 360 genera and 25 tribes under su-

perfamily Coccinelloidea globally (Seago et al. 2011;

Robertson et al. 2015), of which approximately 430 spe-

cies are known from India (Jadwiszczak & Wegrzyno-

wicz 2003; Poorani 2002b, 2004). The coccinellid fauna

of Indian part of Himalaya is represented by more than

203 species with most of them recorded from North-west

(68 species), Western (107 species), and Central Hima-

laya (133 species), and the eastern Himalaya in the state

of Arunachal Pradesh (AP) remains largely unexplored

(Gupta et al. 2018). The recent contributions on ladybird

beetle fauna of AP have been made by Poorani & Booth

(2016), Poorani & Sambath (2017), Poorani & Thangjam

(2019), and Poorani (2019). Therefore, the present study

is intended to fill this gap in the distribution and report the

previously unrecorded species from the state, along with

the new additions to the ladybird beetle fauna of India.

The present study, collectively with the previously

published data (6 species), reports a total of 44 species

of ladybird beetles belonging to 22 genera and 6 tribes

of family Coccinellidae from the state. Among them,

38 species were examined and illustrated (Figs 1-53).

Whereas, Renius cornutus Li & Wang, 2017, Halyzia

nepalensis Canepari, 2003, Halyzia sanscrita Mulsant,

1853, Harmonia manillana (Mulsant, 1866), Micraspis

unicus Poorani, 2019, and Oenopia chinensis (Weise,

1912) were included from literature. All the species are

Received: 29.05.2019

Accepted: 15.01.2020

listed with their valid names along with their major cita-

tions and their distribution in AP (in districts), India (in

states) and outside India. ///eis shensiensis Timberlake,

1943 and Afissa rana (Kapur, 1958) are recorded for the

first time from India along with the first verified record

of Henosepilachna vigintioctomaculata (Motschulsky,

1857) from India, which was listed from India by Poorani

(2004) in her updated checklist, but without any specific

locality data. Twenty-six species have been reported for

the first time from the state. New combinations are pro-

posed here for three species of Epilachini: Afissa gibbera

(Crotch, 1874), comb. nov., Afissa mystica (Mulsant,

1850), comb. nov., and Afissa undecimspilota (Hope,

1831), comb. nov., based on the phylogenetic classifica-

tion and revision of the world genera of tribe Epilachni-

ni by Tomaszewska & Szawaryn (2016). These species

were previously included in the genus Epilachna.

MATERIALS AND METHODS

The materials for the present study collected during re-

cent faunistic surveys to Dihang-Dibang Biosphere Re-

serve, Namdapha National Park, and Tawang districts

of AP along with the specimens, deposited at the Cole-

optera Section of Zoological Survey of India, Kolkata.

The specimens were identified with the help of follow-

ing publications: Dieke (1947), Kapur (1946, 1948),

Bielawski (1961), Iablokoff-Khnzorian (1982), Booth

(1997), Poorani & Booth (2006), Poorani et al. (2008),

Corresponding editor: D. Ahrens

Published: 20.02.2020

28 Priyanka Das et al.

Ren et al. (2009), and Tomaszewska & Szawaryn (2016).

The specimen identifications were verified also with Dr

A.P. Kapur’s Coccinellidae collection present at the Co-

leoptera Section, ZSI. Wherever required, the male gen-

italia was also dissected, cleaned in 10% KOH solution,

and studied for confirming the identity of the species.

The specimens were examined using a Nikon SMZ25

stereo zoom-microscope, and the photographs were tak-

en using DS-R12 camera with NIS Elements BR 5.10.00

imaging software. Images were also slightly modified

using Adobe Photoshop CS3. Scanning electron micros-

copy technique was also used and the images were tak-

en using Carl Zeiss EVO18. The species with a single

asterisk mark (*) are newly recorded from AP whereas

with two asterisks marks (**) are recorded for the first

time from India. The material examined in each species

broadly includes the district in AP, micro locality, date of

collection, number of examples, and collector name. The

specimens are deposited in the National Zoological Col-

lection of Zoological Survey of India, Kolkata (NZSI).

Institutional abbreviations

NZSI = Zoological Survey of India, M Block, New

Alipore, Kolkata, 700053, India;

ZSI-CZRC = Zoological Survey of India, Central

Zone Regional Centre, Vijay Nagar, Jabalpur,

482002, Madhya Pradesh;

NBAIR = National Bureau of Agricultural Insect

Resources, Bellary Road, Bengaluru, 560024,

Karnataka, India;

SCAU = South China Agriculture University,

Guangzhou, 510640, China.

RESULTS

Taxonomic Account

Family Coccinellidae Latreille, 1807

Subfamily Coccinellinae Latreille, 1807

Tribe Aspidimerini Mulsant, 1850

Genus Cryptogonus Mulsant, 1850

1. Cryptogonus bimaculatus Kapur, 1948 (Fig. 1)

Cryptogonus bimaculatus Kapur, 1948: 100, fig. 8D.

Material examined. Papum Pare: Banderdewa,

11.iv.2001 (1 @), leg. Sheela.

Distribution. India: Arunachal Pradesh (Papum Pare),

Assam, Nagaland, and Tamil Nadu. Elsewhere: Bhutan,

China, Myanmar, Nepal, and Thailand (Kapur 1948;

Canepari 1997; Poorani 2002b, 2004; Kovar 2007; Ren

et al. 2009).

Bonn zoological Bulletin 69 (1): 27-44

2. Cryptogonus quadriguttatus (Weise, 1895) (Fig. 2)*

Aspidiphorus quadriguttatus Weise, 1895: 326.

Cryptogonus quadriguttatus: Weise, 1900: 428; Kapur,

1948: 97, fig. 7A-I.

Cryptogonus quadriguttatus var. conjluens Kapur, 1948:

99.

Cryptogonus quadriguttatus var. nigriscens Kapur, 1948:

Oe.

Material examined. Papum Pare: Banderdewa,

11.iv.2001 (1 9) (25402/H4A), leg. Sheela.

Distribution. India: Arunachal Pradesh (Papum Pare),

Assam, Goa, Nagaland, Uttar Pradesh, Uttarakhand, Sik-

kim, Tripura, and West Bengal. Elsewhere: Bhutan, and

China (Kapur 1948, 1963; Poorani 2002b, 2004).

Tribe Chilocorini Mulsant, 1846

Genus Renius Li & Wang, 2017

3. Renius cornutus Li & Wang, 2017

Renius cornutus Li & Wang, 2017 in Li et al. 2017: 122,

124.

Distribution. India: Arunachal Pradesh (Tiwarigaow).

Elsewhere: China (Poorani & Thangjam, 2019).

Remarks. R. cornutus was described by Li & Wang

(2017) from China (Tibet), the type material of which

is deposited at SCAU. Recently, Poorani & Thang-

jam (2019) identified and reported this species from

Arunachal Pradesh, based on a female specimen, depos-

ited at NBAIR. We lack this species in our collection,

therefore could not examine the material of the species.

Genus Priscibrumus Kovar, 1997

4. Priscibrumus uropygialis Mulsant, 1853 (Fig. 3)*

Exochomus uropygialis Mulsant, 1853: 196.

Brumus uropygialis. Crotch, 1874: 196.

Exochomus (Exochomus) uropygialis: Barovsky, 1922:

297; Miyatake, 1985: 11-12, figs 19-22.

Priscibrumus uropygialis. Kovart, 1997: 117.

Material examined. Changlang: Namdapha National

Park, 24.vi.2017 (1ex.) (24904/H4A), 361m, leg. J. Saini.

Distribution. India: Arunachal Pradesh (Changlang),

Himachal Pradesh, and Jammu & Kashmir. Elsewhere:

Bhutan, Nepal, and Pakistan (Bielawski 1979; Canepari

1997; Poorani 2002b, 2004).

Tribe Coccinellini Latreille, 1807

Genus Alloneda lablokoff-Khnzorian, 1979

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The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 29

Figs 1-9. Habitus of (1) Cryptogonus bimaculatus Kapur, 1948; (2) Cryptogonus quadriguttatus (Weise, 1895); (3) Priscibrumus

uropygialis Mulsant, 1853; (4) Alloneda dodecaspilota (Hope, 1831); (5) Calvia albida Bielawski, 1972; (6) Calvia sykesii (Crotch,

1874); (7) Coccinella luteopicta (Mulsant, 1866); (8) Coccinella septempunctata Linnaeus, 1758; (9) Coccinella transversalis

Fabricius, 1781.

Bonn zoological Bulletin 69 (1): 27-44 ©ZFMK

30 Priyanka Das et al.

5. Alloneda dodecaspilota (Hope, 1831) (Fig. 4)*

Coccinella 12-spilota Hope, 1831: 31.

Caria duodecimspilota: Mulsant, 1850: 236.

Aiolocaria dodecaspilota: Crotch, 1874: 178; Kapur,

1963, 26, fig. 9A.

Palaeoneda dodecaspilota: Mader, 1934: 302.

Alloneda dodecaspilota: \ablokoff-Khnzorian,

277, fig. 45b; Miyatake, 1985: 20, figs 38-42.

1932.

Material examined. West Kameng: Bokhar, 27.v.1961

(2 exs) (25302/H4A), 2800m, leg. K.C. Jayram.

Distribution. India: Arunachal Pradesh (West Kameng),

Himachal Pradesh, Sikkim, and West Bengal. Elsewhere:

Bhutan, China, Myanmar, Nepal, Thailand, and Vietnam

(Miyatake 1985; Canepari 1997; Poorani 2002b, 2004).

Genus Calvia Mulsant, 1846

6. Calvia albida Bielawski, 1972 (Fig. 5)*

Calvia albida Bielawski, 1972: 308, figs 131, 132-139;

Booth, 1997: 931, fig. 28, 41; Poorani, 2014: 4, figs 1d, 3.

Material examined. Tawang: Jang, 25.1x.2013 (2 exs)

(25398/H4A), leg. P.P.B.

Distribution. India: Arunachal Pradesh (Tawang), Mani-

pur, Sikkim, Uttar Pradesh, and West Bengal. Elsewhere:

Nepal (Poorani 2002b, 2004; Poorani & Sambath, 2017).

7. Calvia sykesii (Crotch, 1874) (Fig. 6)*

Anisocalvia sykesii Crotch, 1874: 146.

Calvia sykesii: Korschefsky, 1932: 529; Booth, 1997:

930, fig. 27.

Material examined. Changlang: Namdapha National

Park, Deban, 361m, 24.vi.2017 (4 exs) (24906/H4A),

leg. J. Saini.

Distribution. India: Arunachal Pradesh (Changlang), As-

sam, Meghalaya, Sikkim, Tamil Nadu, and West Bengal.

Elsewhere: Nepal (Booth 1997; Poorani 2002b, 2004).

Genus Coccinella Linnaeus, 1758

8. Coccinella luteopicta (Mulsant, 1866) (Fig. 7)*

Adalia luteopicta Mulsant, 1866: 45.

Lioadalia luteopicta. Crotch, 1874: 104; Bielawsk1,

1971: 7-8, figs 27-35.

Coccinella luteopicta: lablokoff-Khnzorian, 1982: 395;

Canepari, 1997: 52.

Material examined. East Kameng: Seppo, 3500m,

11.x.1996, (1 ex.) (25303/H4A), leg. S.K. Mondal.

Tawang: 24.1x.2013, (1 ex.) (25304/H4A), leg. P.P.B;

Jang: 26.1x.2013 (1 ex.) (25305/H4A), leg. J. Majumder.

Bonn zoological Bulletin 69 (1): 27-44

Distribution. India: Arunachal Pradesh (East Kameng,

Tawang), Himachal Pradesh, Sikkim, Uttar Pradesh,

and West Bengal. Elsewhere: Bhutan, China, and Nepal

(Poorani 2002b, 2004; Kovar 2007).

9. Coccinella septempunctata Linnaeus, 1758 (Fig. 8)

Coccinella 7-punctata Linnaeus, 1758: 365.

Coccinella septempunctata: Korschefsky, 1932: 486.

Coccinella divaricata Olivier, 1808: 1001.

Coccinella confusa Wiedemann, 1823:72.

Coccinella bruckii Mulsant, 1866: 90; Crotch, 1874: 46.

Coccinella septempunctata brucki: Korschefsky, 1932:

49].

Material examined. West Kameng: Kalaktang, Stn. 17,

17.11.1961, (1 ex.), Rahang, Stn. 34, 17.1v.1961, (1 ex.),

Bomdila Pass, Stn. 33, 17.1v.1961, (1 ex.), Shergaon, Stn.

51, 05.v.1961, (1 ex.), Shergaon, Stn. 25, 08.v.1961, (2

exs), Moshing, Stn. 22, 11.v.1961, (2 exs), But Vill. Stn.

61, 24.vi.1961, (1 ex.), leg. K.C. Jayram. Gandhigram:

22.11.1988 (1 ex.), 26.11.1988 (1 ex.). Papum Pare: Kok-

ila North of Chessa, 21.x.1996 (lex.) (24302/H4A), leg.

A.M. Biswas. Roing: Debang Valley, 25.1.2000 (1 ex.)

(24303/H4A), Deopani, 250m, 29.1.2000 (2 exs) (25306/

H4A), leg. S.K. Mondal. Ziro: Joram, 2.vi.2000 (3 exs)

(24304/H4A), leg. B. Mitra. West Kameng: Tenga,

24.iv.2001 (1 ex.) (25307/H4A), leg. S. Sheela. Chang-

lang: Namdapha National Park, Lankhal Nala, 6.111.2017

(1 ex.) (25308/H4A), Deban River Bed, 345m, 12.11.2017

(2 exs) (24309/H4A), Anamika Fall, 413m, 13.111.2017

(1 ex.) (25310/H4A), leg. J. Saini. Tawang: Zemithang,

24.vi.2017 (3 exs) (24911/H4A), Lumla, 24.vi.2017 (1

ex.) (25311/H4A), 11.iv.2018 (1 ex.) (24912/H4A),

Namtsering, 15.iv.2018 (1 ex.) (24913/H4A)/16.iv.2018

(1 ex.) (24914/H4A), 17.1v.2018 (7 exs) (24915/H4A),

leg. J. Saini. Dihang Dibang Biosphere Reserve, Maliny,

25.x.2017 (5 exs) (24437/H4A), leg. D. Gupta.

Distribution. Widely distributed throughout India in-

cluding Arunachal Pradesh (Gandhigram, Papum Pare,

Roing, Ziro, West Kameng, Changlang, Tawang, Dihang

Dibang Biosphere Reserve). Elsewhere: China, Afro-

tropical Region, North America, Pakistan, and Sri Lanka

(Poorani 2002b, 2004; Kovar 2007; Poorani & Sambath

2017).

10. Coccinella transversalis Fabricius, 1781 (Fig. 9)*

Coccinella transversalis Fabricius, 1781: 97;

Iablokoff-Khnzorian, 1979: 68.

Coccinella repanda Thunberg, 1781: 18.

Material examined. Papum Pare: Kokila North of Ches-

sa, 21.x.1996 (lex.) (24299/H4A), leg. A.M. Biswas;

Balijan, 23.x.1996 (lex.) (24300/H4A), leg. S.K. Mon-

dal; Baderdewa: 11.1v.2001 (2 exs) (24301/H4A), leg.

Sheela. East Siang: Boleng, 18.1.2000 (1 ex.) (25312/

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The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 31

H4A), leg. S.K. Mondal. Dihang Dibang Biosphere Re-

serve, Maliny, 25.x.2017 (4 exs) (24436/H4A), leg. D.

Gupta.

Distribution. Widely distributed in throughout India

including Arunachal Pradesh (Papum Pare, Baderdewa,

East Siang, Dihang Dibang Biosphere Reserve). Else-

where: Australia, Bangladesh, Indochina, Indonesia,

Japan, Nepal, New Zealand, and Sri Lanka (Poorani

2002b, 2004).

Remarks. It is commonly distributed species in India

but was not earlier reported from the state of Arunachal

Pradesh.

Genus Coelophora Mulsant, 1850

11. Coelophora bissellata Mulsant, 1850 (Fig. 10)*

Coelophora bissellata Mulsant, 1850: 400.

Spilocaria bissellata: Timberlake, 1943: 58.

Lemnia (Spilocaria) bissellata: \ablokoff-Khnzorian,

1979: 62.

Lemnia bissellata: Hoang , 1983: 74; lablokoff-Khnzo-

rian, 1982: 218.

Caria gracilicornis Weise, 1902: 505.

Material examined. Siang, NEFA: 10.xi.1971 (1 ex.

on leaves,) (25318/H4A), leg. S. Ghose. Papum Pare:

Kokila, North of Chessa, 21.x.1996 (1 ex.) (25315/

H4A), leg. A.M. Biswas; Banderdewa, 11.iv.2001 (1 ex.)

(25320/H4A), leg. Sheela. Debang Valley: Kannu North,

1.11.2000 (1 ex.) (25322/H4A), leg. S.K. Mondal. Roing :

Diban Valley, 29.1x.2000 (1 ex.) (25319/H4A), leg. R.S.

Mridha. Itanagar: Ganga Lake, 28.v.2000 (4 exs) (25314/

H4A), leg. T.K.Mondal; Naharlagun, 530m, 29.v.2000

(1 ex.) (25321/H4A), leg. K. Bhattacharya. West Siang:

Aalo (formerly Along), Hissan Colony, 11.vi.2000 (2

exs) (25317/H4A), leg. R.S. Mridha. East Kameng:

Rang, Gthili, 17.1x.2000 (5 exs) (25313/H4A), leg. A.R.

Lahiri. Changlang, Deban Rest House, 4.111.2017 (1 ex.)

(25316/H4A), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Siang, Papum

Pare, Roing, Debang Valley, West Siang, East Kameng,

Changlang), Assam, Himachal Pradesh, Karnataka, Ker-

ala, Manipur, Meghalaya, Sikkim, Tamil Nadu, Uttar

Pradesh, and West Bengal. Elsewhere: Bhutan, Bangla-

desh, China, Indonesia, Nepal, New Guinea, Philippines,

Thailand, and Vietnam (Poorani 2002b, 2004; Kovar

2007).

Genus Halyzia Mulsant, 1846

12. Halyzia dejavu Poorani & Booth, 2006 (Fig. 11)

Halyzia dejavu Poorani & Booth, 2006: 66, pl. 1B, figs

10-17.

Bonn zoological Bulletin 69 (1): 27-44

Material examined. Changlang: Deban, 24.xii.2017

(lex.) (24905/H4A), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Changlang,

Tawang), Sikkim; Nepal (Poorani & Booth 2006; Poora-

ni & Sambath 2017).

13. Halyzia nepalensis Canepari, 2003

Halyzia nepalensis Canepari 2003: 261, figs 1-2.

Distribution. India: Arunachal Pradesh. Elsewhere:

Myanmar, and Nepal (Poorani & Thangjam 2019).

Remarks. Poorani & Thangjam (2019) reported this

species from Arunachal Pradesh, based on photographic

records, which they found identical with the specimens

from Myanmar, deposited at NZSI. The specimens of this

species from Arunachal Pradesh were unavailable with

us for examination.

14. Halyzia sanscrita Mulsant, 1853

Halyzia sanscrita Mulsant, 1853: 152.

Distribution. India: Arunachal Pradesh (Tawang), Hi-

machal Pradesh, Sikkim, and Uttarakhand. Elsewhere:

Bhutan, China, and Nepal (Poorani 2002b, 2004; Kovar

2007; Poorani & Sambath 2017).

Remarks. Poorani & Sambath (2017) recorded this spe-

cies from Tawang, Arunachal Pradesh, based on the spec-

imens, deposited at ZSI-CZRC, which were examined by

the authors.

Genus Harmonia Mulsant, 1846

15. Harmonia dimidiata (Fabricius, 1781) (Fig. 12)

Coccinella dimidiata Fabricius, 1781: 94.

Coccinella dimidia Hope, 1831: 30.

Leis dimidiata. Mulsant, 1850: 242.

Coccinella quindecimmaculata Hope, 1831: 30.

Coccinella bicolor Hope, 1831: 31.

Harmonia dimidiata: Miyatake, 1965: 62.

Material examined. West Kameng: Salari, Stn. 60,

22.v1.1961, (2 exs), But village, Stn. 61, 24.vi.1961,

(lex). Denezi “Sti: ol6. 25 vi 196) s6l.ex))- dee. kK: C2

Jayram.

Distribution. India: Arunachal Pradesh (West Kameng,

Tawang), Assam, Himachal Pradesh, Jammu & Kashmir,

Manipur, Punjab, Rajasthan, Sikkim, and West Bengal.

Elsewhere: Bhutan, China, Japan, Nepal, and Pakistan

(Poorani 2002b, 2004; Kovar 2007; Poorani & Sambath

2017).

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32 Priyanka Das et al.

16 17 18

Figs 10—18. Habitus of (10) Coelophora bissellata Mulsant, 1850; (11) Halyzia dejavu Poorani & Booth, 2006; (12) Harmonia

dimidiata (Fabricius, 1781); (13) Harmonia eucharis (Mulsant, 1853); (14) Harmonia sedecimnotata (Fabricius, 1801); (15)

Hippodamia variegata (Goeze, 1777); (16) lleis confusa Timberlake, 1943; (17) I/leis indica Timberlake, 1943; (18) Macroilleis

hauseri (Mader, 1930).

Bonn zoological Bulletin 69 (1): 27-44 ©ZFMK

The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 33

16. Harmonia eucharis (Mulsant, 1853) (Fig. 13)

Ballia eucharis Mulsant, 1853: 167.

Material examined. West Kameng: Rahung, Stn. 34,

7.1v.1961, (1 ex.), Rahung, Stn. 35, (1 ex.) 24.iv.1961,

leg. K.C. Jayram. Tawang: Zemithang, 24.vi.2017, (1 ),

leg. J. Saini. Dibang Valley, Dihang Dibang Biosphere

Reserve, Mipi, 01.x1.2017 (1 ex), leg. D. Gupta.

Distribution. India: Arunachal Pradesh (Tawang, West

Kameng, Dihang Dibang Biosphere Reserve), Jammu

and Kashmir, Himachal Pradesh, Manipur, Sikkim, Ut-

tarakhand, and Uttar Pradesh. Elsewhere: China, Myan-

mar, Nepal, and Pakistan (Poorani 2002b, 2004; Kovar

2007; Poorani & Sambath, 2017).

Remarks. See Kovar (2007) for synonyms.

17. Harmonia manillana (Mulsant, 1866)

Caria manillana Mulsant, 1866: 170.

Leis atrocincta Mulsant, 1866: 175.

Neda paulinae Mulsant, 1866: 203.

Leis dunlopi Crotch, 1874: 121.

Leis cerasicolor Crotch, 1874: 121.

Leis aterrima Crotch, 1874: 121.

Leis papuensis Crotch, 1874: 121.

Leis papuensis var. suffusa Crotch, 1874: 121.

Distribution. India: Arunachal Pradesh (Pasighat).

Elsewhere: Philippines, Malaysia, and Indonesia

(lablokoff-Khnzorian 1982; Poorani & Booth 2016).

Remarks. Poorani & Booth (2016) first time record-

ed this species from the Palearctic region of Arunachal

Pradesh, and also mentioned to be very rare in mainland

India. Earlier, the species was known from the oriental

region of Indonesia, Malaysia, and the Philippines. We

could not find specimen of this species from the study

area in our collection.

18. Harmonia sedecimnotata (Fabricius,

(Fig. 14)*

Coccinella sedecimnotata Fabricius, 1801: 370.

Daulis 16-notata: Mulsant, 1850: 296.

Callineda sedecimnotata: Crotch, 1874: 161.

Harmonia sedecimnotata: Timberlake, 1943: 18.

1801)

Material examined. Changlang: Namdapha National

Park, Deban, 24.vi.2017 (3 exs) (24918/H4A), leg. J.

Saini.

Distribution. India: Arunachal Pradesh (Changlang),

Sikkim, and West Bengal. Elsewhere: China, Nepal, and

Southeast Asia (Poorani 2002b, 2004; Kovar 2007).

Bonn zoological Bulletin 69 (1): 27-44

Genus Hippodamia Chevrolat, 1836

19. Hippodamia variegata (Goeze, 1777) (Fig. 15)*

Coccinella variegata Goeze, 1777: 246.

Adonia variegata: Mulsant, 1846: 39.

Hippodamia variegata: Belicek, 1976: 338.

Hippodamia (Adonia) variegata: \ablokoff-Khnzorian,

1982: 326.

Material examined. West Kameng: Dengzi, Stn. 16,

25.v.1961 (2 exs); Salari, Stn. 60, 22.v1.1961 (2 exs), leg.

K.C. Jayram.

Distribution. India: Arunachal Pradesh, Himachal

Pradesh, Jammu & Kashmir, Maharashtra, and Uttar

Pradesh. Elsewhere: widely distributed in Afrotropical,

Nearctic, Oriental regions; Afghanistan, China, Nepal,

and Pakistan (Poorani 2002b, 2004; Kovar 2007).

Genus //leis Mulsant, 1850

20. Illeis confusa Timberlake, 1943 (Fig. 16)*

Illeis confusa Timberlake, 1943: 61.

Material examined. Tawang: Zemithang, 24.vi.2017

(13) (24909/H4A), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Tawang), As-

sam, and West Bengal. Elsewhere: China, Nepal, and

Thailand (Poorani 2002b, 2004; Poorani & Lalitha 2018;

Kovar 2007).

21. Illeis indica Timberlake, 1943 (Fig. 17)*

Illeis indica Timberlake, 1943: 61.

Material examined. Tawang: Zemithang, 24.vi.2017 (1

ex.), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Tawang), Jam-

mu & Kashmir, Himachal Pradesh, and Uttar Pradesh.

Elsewhere: Pakistan, and Thailand (Poorani 2002b,

2004; Kovar 2007).

22. Illeis shensiensis Timberlake, 1943 (Figs 19—23)**

Illeis shensiensis Timberlake, 1943: 61; Bielawski, 1961:

358, figs 5—6, 14; Ren et al., 2009: 243.

Material examined. Changlang: Deban,

24.xii.2017 (2 64) (25409/H4A), leg. J. Saini.

355- im,

Distribution. India: Arunachal Pradesh (Changlang).

Elsewhere: China (Shensi), and Pakistan (Kovar 2007;

Hayat et al. 2017).

Remarks: J. shensiensis can be distinguished from

closely related species by the following characters: pro-

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34 Priyanka Das et al.

Figs 19-23. //leis shensiensis Timberlake, 1943. (19) Habitus; (20) Sipho; (21) Phallobase in dorsal view; (22) Phallobase in

lateral; (23) Apical portion of Sipho.

notum with two small black marks (Fig 19), sipho not

bifid at apex (Fig 23), median lobe of tegmen having

apex strongly curved upward and more or less depressed

(Figs 21, 22), parameres shorter and stouter and some-

what strongly curved at base, otherwise straight (Fig 21).

The male genitalia of our specimen is identical with that

of /. shensiensis as illustrated in Bielawski (1961: 358,

Figs 5—6, 14) and Ren et al. (2009: 243, Fig 325).

Bonn zoological Bulletin 69 (1): 27-44

Genus Macroilleis Miyatake, 1965

23. Macroilleis hauseri (Mader, 1930) (Fig. 18)

Halyzia hauseri Mader, 1930: 162.

Macroilleis hauseri: Miyatake 1965: 71-73.

Material examined. Tawang: Zemithang, 24.vi.2017 (1

3) (25399/H4A), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Tawang), and

West Bengal. Elsewhere: Bhutan, China, Vietnam, and

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The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 35

Pakistan (Poorani 2002b; 2004; Kovar 2007; Poorani &

Sambath 2017).

Genus Menocheilus Timberlake, 1943

24. Menocheilus sexmaculata (Fabricius, 1781)

(Fig. 24)

Coccinella sexmaculata Fabricius, 1781: 96.

Material examined. Papum Pare: Bandardewa,

11.iv.2001 (2exs) (24307/H4A), leg. Sheela. Dihang

Dibang Biosphere Reserve, Maliny, 25.x.2017 (2 exs)

(24438/H4A), leg. D. Gupta.

Distribution. Widely distributed in India including

Arunachal Pradesh (Papum Pare; Dihang Dibang Bio-

sphere Reserve). Elsewhere: Australian region, Arab

Emirates, Afghanistan, Bangladesh, Bhutan, China, In-

donesia, Iran, Japan, Malaysia, Myanmar, Nepal, Oman,

Pakistan, Sri Lanka, Philippines, and Vietnam (Poorani

2002b, 2004; Kovar 2007).

Remarks. See Kovafy (2007: 619) for synonymy.

Genus Micraspis Chevrolat, in Dejean, 1836

25. Micraspis univittata (Hope, 1831) (Fig. 25)*

Coccinella univittata Hope, 1831: 31.

Alesia univittata. Mulsant, 1850: 357.

Tytthaspis univittata. Korschefsky, 1932: 384.

Micraspis univittata: lablokoff-Khnzorian, 1982: 511.

Material examined. Along: Hissan Colony, 11.vi.2000

(1 ex.) (25408/H4A), leg. R.S. Mridha.

Distribution. India: Arunachal Pradesh (Along), Andhra

Pradesh, Bihar, Karnataka, Odisha, Tamil Nadu, Tripura,

and Uttarakhand. Elsewhere: China, and Nepal (Poorani

2002b; 2004; Kovar 2007).

26. Micraspis unicus Poorani, 2019

Micraspis unicus Poorani, 2019: 190, fig. 1.

Distribution. India: Arunachal Pradesh (Mayodia).

Remarks. This species was described recently by Poora-

ni (2019) from Arunachal Pradesh, based on male, holo-

type and female paratype, deposited at NBAIR. We could

not find any specimen of this species in our collection.

Genus Oenopia Mulsant, 1850

27. Oenopia chinensis (Weise, 1912)

Coelophora chinensis Weise, 1912: 113.

Gyrocaria chinensis. Miyatake, 1965: 65.

Oenopia chinensis: Hoang, 1983: 91.

Bonn zoological Bulletin 69 (1): 27-44

Distribution. India: Arunachal Pradesh (Pasighat), and

Meghalaya. Elsewhere: China (Poorani 2002a, 2002b;

2004; Kovar 2007; Poorani & Thangjam 2019).

Remarks. Earlier known from China, this species was

reported from India by Poorani & Thangjam (2019),

based on a female specimen from Meghalaya and larvae

from Arunachal Pradesh, materials of which are deposit-

ed at NBAIR. We could not find any adult specimen of

this species from the study area in our collection.

28. Oenopia kirbyi Mulsant, 1850 (Fig. 26)*

Oenopia kirbyi Mulsant, 1850: 425; Poorani, 2002a: 102,

figs 4, 16, 23, 31.

Gyrocaria kirbyi: Miyatake, 1965: 66, fig. 34.

Material examined. Dihang Dibang Biosphere Re-

serve: Maliney, 27.x.2017 (lex.) (24432/H4A); Anini,

27.x.2017 (lex.) (24433/H4A), leg. D. Gupta. Siang:

NEFA, 10.x1.1971 (1 ex. on leaves) (25404/H4A), leg. S.

Ghose. Roing: Dibang Valley, 250 m, 25.1.2000 (2 exs)

(25405/H4A), 27.1.2000 (1 ex.) (25406/H4A), 29.1.2000

(5 exs) (25407/H4A), leg. S.K. Mondal.

Distribution. India: Arunachal Pradesh (Dihang-Dibang

Biosphere Reserve, Siang, Roing), Meghalaya, Mizoram,

Sikkim, and West Bengal; Bhutan. Elsewhere: China,

Myanmar, Nepal, and Thailand (Poorani 2002a, 2002b,

2004; Kovar 2007).

29. Oenopia mimica Weise, 1902 (Fig. 27)*

Oenopia mimica Weise, 1902: 505; Poorani, 2002a: 104,

figs 5, 17, 24, 32.

Gyrocaria mimica: Miyatake, 1985: 16.

Material examined. Siang: NEFA, 10.x1.1971 (1 ex. on

leaves) (25324/H4A), leg. S. Ghose. Lower Subansiri:

Bandardewa, 19.x.1996 (1 ex.) (25325/H4A), leg. S.K.

Mondal. Tawang: Jung, 23.1x.2013 (2 exs) (25323/H4A),

leg. J. Majumder. Dihang Dibang Biosphere Reserve,

Anini, 25.x.2019 (1 ex.), leg. D. Gupta.

Distribution. India: Arunachal Pradesh (Tawang, Siang,

Lower Subansir1), Himachal Pradesh, Uttar Pradesh, and

Sikkim. Elsewhere: Laos, Myanmar, and Nepal (Poorani

2002a, 2002b, 2004; Kovar 2007).

30. Oenopia quadripunctata Kapur, 1963 (Fig. 28)*

Oenopia quadripunctata Kapur, 1963: 27; Poorani,

2002a: 102, fig. 3.

Material examined. Debang Valley:

16.1x.2000 (1 ex.), leg. A.R. Lahiri.

Old Aloppa,

©ZFMK

36 Priyanka Das et al.

30 31 32

Figs 24-32. Habitus of (24) Menocheilus sexmaculata (Fabricius, 1781); (25) Micraspis univittata (Hope, 1831); (26) Oenopia

kirbyi Mulsant, 1850; (27) Oenopia mimica Weise, 1902; (28) Oenopia quadripunctata Kapur, 1963; (29) Oenopia sauzeti Mulsant,

1866; (30) Oenopia sexareata (Mulsant, 1853); (31) Propylea luteopustulata (Mulsant, 1850); (32) Synona melanopepla (Mulsant,

1850).

Bonn zoological Bulletin 69 (1): 27-44 ©ZFMK

The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 37

Distribution. India: Arunachal Pradesh (Debang Val-

ley), Meghalaya, Mizoram, Nagaland, Sikkim, and West

Bengal. Elsewhere: Bhutan, China, Myanmar, and Nepal

(Poorani 2002a, 2002b, 2004; Kovar 2007).

31. Oenopia sauzeti Mulsant, 1866 (Fig. 29)

Oenopia sauzeti Mulsant, 1866: 281; Poorani, 2002a:

103, figs 6, 18, 25, 33.

Gyrocaria sauzeti: Miyatake, 1967: 76; 1985: 15, figs

30-33.

Material examined. Lower Subansiri: Bandardewa,

25.1.2000 (1 ex.) (24295/H4A), leg. S.K. Mondal. West

Kameng, Kalaktang, Stn.17, 17.11.1961 (1 ex.), Dukong-

ko River, 02.v.1961 (1 ex.); Rupa, Stn. 29, 03.v.1961 (1

ex.); Shergaon, Stn. 51, 5.v.1961 (1 ex.)/Stn. 25, 8.v.1961

(2 exs); Domko, Stn. 52, 10.v.1961 (1 ex.); Moshing, Stn.

22, 11.v.1961 (1 ex.); Dengzi, Stn. 16, 25.v.1961 (3 exs);

Ankaling, Stn. 12, 25.v.1961 (1 ex.), leg. K.C. Jayram.

Changlang: Namdapha National Park, 361m, 24.vi.2017

(1 ex.) (24855/H4A), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Changlang:

Namdapha National Park, West Kameng, Lower Suban-

siri), Assam, Himachal Pradesh, Jammu & Kashmir, Me-

ghalaya, Sikkim, Uttar Pradesh, and West Bengal. Else-

where: Bhutan, China, Pakistan, Laos, Myanmar, Nepal,

Thailand, and Vietnam (Poorani 2002a, 2002b, 2004:

Kovar 2007; Poorani & Sambath 2017).

32. Oenopia sexareata (Mulsant, 1853) (Fig. 30)

Coelophora sexareata Mulsant, 1853: 181; Poorani,

2002a: 101, figs 2, 15, 22, 30.

Coelophora sexareata vat. lacerata Sicard, 1913: 500.

Gyrocaria sexareata: Miyatake, 1967: 76.

Oenopia sexareata: Hoang , 1983: 62, 92.

Material examined. West Kameng: Rahung, Stn.35,

24.iv.1961, (1 ex.), Siggun, Stn.50, 4.v.1961, (3 exs),

Denzi, Stn.16, 25.v.1961, (1 ex.) leg. K.C. Jayram, Low-

er Subansiri: Banderdewa, 19.x.1996 (1 ex.) (25327/

H4A), leg. A.M. Biswas. Roing: Dibang Valley, 250m,

25.1.2000 (1 ex.) (25328/H4A), 29.1.2000 (3 exs) leg.

S.K. Mondal. Papum Pare: Bandardewa, 11.iv.2001 (2

exs) (25329/H4A) leg. Sheela. Dihang Dibang Biosphere

Reserve: Maliney, 27.x.2017 (lex.) (24434/H4A) leg. D.

Gupta.

Distribution. India: Arunachal Pradesh (Lower Suban-

sirl, Roing, Papum Pare, West Kameng, Dihang Dibang

Biosphere Reserve), Assam, Bihar, Himachal Pradesh,

Meghalaya, Sikkim, Uttar Pradesh, and West Bengal.

Elsewhere: Bhutan, China, Indonesia, Japan, Myanmar,

Bonn zoological Bulletin 69 (1): 27-44

Nepal, and Vietnam (Canepari 1997; Poorani 2002a,

2002b, 2004; Kovar 2007).

Genus Propylea Mulsant, 1846

33. Propylea luteopustulata (Mulsant, 1850) (Fig. 31)

Oenopia (Pania) luteopustulata Mulsant, 1850: 421.

Propylea luteopustulata: Vandenberg & Gordon, 1991:

30.

Material examined. West Kameng: Kalaktang, Stn.17,

17.11.1961, (1 ex.); Rahung, Stn. 35, 24.1v.1961, (1 ex.);

Rahung, Stn. 34, 25.1v.1961, (1 ex.); Siggun, Stn. 50,

4.v.1961, (1 ex.); Shergaon, Stn. 25, 08.v.1961 (1 ex.);

Domko, Stn. 52, 10.v.1961, (1 ex.); Moshing, Stn. 22,

ld v. 1961 (lex); Dengzi,; Sti 16> 1S. v.196 1» (1Lex.):

Ankaling, Stn. 12, 15.v.1961 (2 exs), leg. K.C.Jayram;

Zamiri, 14.x.1997 (1 ex.), leg. S.K. Mondal. Siang:

NEFA, 10.x1.1971 (2 exs on leaves), leg. S. Ghose. Low-

er Subansiri: Bandardewa, 19.x.1996 (2 exs), leg. A.M.

Biswas. Tawang: Center Dirang, 15.x1.1997 (2 exs on fo-

liage), leg. A.K. Sanyal. Roing: Debang Valley, Rukmo,

27.1.2000 (2 exs), leg. S.K. Mondal. Changlang: Namda-

pha National Park, 361m, 24.vi.2017 (1 ex.), leg. J. Saini.

Distribution. India: Arunachal Pradesh (Siang, Lower

Subansiri, Tawang, West Kameng, Roing, Changlang),

Assam, Andaman & Nicobar Islands, Himachal Pradesh,

Meghalaya, Uttar Pradesh, Sikkim, and West Bengal.

Elsewhere: Bhutan, China, Myanmar, Nepal, Sri Lan-

ka, Thailand, and Vietnam (Poorani 2002b, 2004; Kovar

2007; Poorani & Sambath 2017).

Genus Synona Pope, 1989

34. Synona melanopepla (Mulsant, 1850) (Fig. 32)*

Synia melanopepla Mulsant, 1850: 376.

Synia melanaria ab. melanopepla: Korschefsky, 1932:

276.

Leis rougeti Mulsant, 1866: 175.

Synia melanaria ab. rougeti: Korschefsky, 1932: 276.

Synona melanopepla: Poorani et al., 2008: 583, figs 1, 2,

17—22,.52, 33.

Material examined. Roing: Dibang Valley, 19.1x.2000

(1 4) (25326/H4A), leg. R.S. Mridha.

Distribution. India: Arunachal Pradesh (Roing), Assam,

Bihar, Karnataka, Meghalaya, Odisha, Tamil Nadu, and

Uttar Pradesh. Elsewhere: Vietnam (Kovay 2007; Poora-

ni et al. 2008).

©ZFMK

38 Priyanka Das et al.

Tribe Epilachnini Mulsant, 1846

Genus A/fissa Dieke, 1947

Tomaszewska & Szawaryn (2016) in their revision of

world genera of Epilachnini, proposed Epil/achna to be

a new world genus and established Afissa as a valid ge-

nus. Here, three species Epilachna gibbera Crotch, 1874,

Epilachna mystica Mulsant, 1850, and Epilachna undec-

imspilota Hope, 1831 are combined with Afissa based

on the shared morphological characters, proposed by

Tomaszewska & Szawaryn (2016) for the genus: Lateral

margins of elytra not or hardly visible dorsally, some-

times narrowly explanate, and meta-ventral and abdomi-

nal post-coxal lines present.

35. Afissa gibbera (Crotch, 1874) comb. nov. (Fig. 33)*

Epilachna gibbera Crotch, 1874: 80.

Afissa gibbera: Kapur, 1963: 10.

Epilachna_ gibbera: Jadwiszczak & Wegrzynowicz,

2003: 69.

Material examined. Tawang: Camp, Stn.

14.xii.1985, (1 3), leg. SK.B. & ANTI.

No.,

Distribution. India: Arunachal Pradesh (Tawang), and

Sikkim. Elsewhere: Nepal (Poorani 2004).

36. Afissa mystica (Mulsant, 1850) comb. nov. (Figs 41—

50)

Epilachna mystica Mulsant, 1850: 841.

Afissa mystica: Dieke, 1947: 146, figs 100, 169.

Epilachna mystica: Li & Cook, 1961: 51.

Material examined. West Kameng: Munna, 8500 m,

10.x.1996, (4 exs), leg. S.K. Mondal; Bomdila: Sherra

Bash, 30.viii.1998, (3 exs), leg. A.R.Lahiri. East Kameng:

Seppo, 3500m, 11.x.1996, (2 exs), leg. S.K. Mondal.

Distribution. India: Arunachal Pradesh (Tawang, West

Kameng, East Kameng), Karnataka, Sikkim, Uttara-

khand, and West Bengal (North). Elsewhere: Bhutan,

China, Myanmar, and Nepal (Poorani 2004; Kovar 2007;

Poorani & Sambath 2017).

37. Afissa nielamuensis (Pang & Mao, 1977) (Fig. 34)

Epilachna nielamuensis Pang & Mao, 1977: 323, 327;

Miyatake, 1985: 30; Jadwiszczak & Wegrzynowicz,

2003: 94; Ren et al., 2009: 291.

Afissa nielamuensis. Poorani & Thangjam, 2019: 7, figs

6A-B.

Material examined. Tawang: Jang, Jangda, 2,572 m,

24.ix.2018 (1 3), leg. J. Saini.

Bonn zoological Bulletin 69 (1): 27-44

Distribution. India: Arunachal Pradesh (Tawang).

Elsewhere: China and Nepal (Poorani 2004; Poorani &

Thangjam 2019).

38. Afissa rana (Kapur, 1958) (Figs 51—53)**

Afissula rana Kapur, 1958: 320.

Afissa rana: Tomaszewska & Szawaryn, 2016: 53.

Material examined. West Kameng: Bomdila, Stn. 32,

25.v1.1961 (6 exs), 29.v1.1961 (1 ex.), Dukongko River,

Stn. 49, 02.v.1961 (2 exs), Moshing, Stn. 22, 03.v1.1961

(3 exs), leg. K.C. Jayram; Bomdila, Tinga, 29.v1.1995

(7 exs) (25652/H4A), Sherra Bash, 30.viii.1998 (2 exs)

(25653/H4A).

Type material. Paratype: B.M. Nepal Expedition, 1949

(B.M. 1949-637), Afissula rana gen.n., sp. nov., A.P. Ka-

pur Det., 1954 [ZSI Registration Number: 9983/H4].

Distribution. India: Arunachal Pradesh (West Kameng).

Elsewhere: China, and Nepal (Poorani 2004).

Remarks. A. rana can be distinguished from closely re-

lated species by the following characters: lateral margins

of elytra invisible in dorsal view, pronotum reddish-tes-

taceous except for yellowish margins (Fig 51), sipho nar-

row and lancet-shaped at apex (Fig 53), and parameres

shorter than median lobe (Fig 52). The male genitalia of

our specimen is identical with that of A. rana as illus-

trated in the original description by Kapur (1958: 320,

figs 5a, c-f). The paratype of the species NZSI was also

examined.

39. Afissa undecimspilota (Hope, 1831) comb. nov.

(Fige35)*

Coccinella I1-spilota Hope, 1831: 31.

Epilachna undecimspilota: Jadwiszczak & Wegrzyno-

wicz, 2003: 125.

Material examined. West Kameng: Dirang, Rahung,

1830m, 16.vi1.1961, (2 exs), leg. S. Biswas.

Distribution. India: Arunachal Pradesh (West Kameng),

and Northern India. Elsewhere: China, Bhutan, and Ne-

pal (Poorani 2004; Kovar 2007).

Genus Diekeana Tomaszewska & Szawaryn 2015

40. Diekeana macularis (Mulsant, 1850) (Fig. 36)*

Epilachna macularis Mulsant, 1850: 797.

Solanophila macularis ab. donckieri Weise, 1912: 112.

Afissa macularis: Dieke, 1947: 120, figs 78, 153.

Epilachna macularis. Jadwiszczak & Wegrzynowicz,

2003: 86.

Diekeana macularis. Tomaszewska & Szawaryn, 2016:

74.

©ZFMK

The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 39

39 40 41

Figs 33-41. Habitus of (33) Afissa gibbera (Crotch, 1874) comb. nov.; (34) Afissa nielamuensis (Pang & Mao, 1977); (35) Afissa

undecimspilota (Hope, 1831) comb. nov.; (36) Diekeana macularis (Mulsant, 1850); (37) Henosepilachna indica (Mulsant, 1850);

(38) Henosepilachna vigintioctomaculata (Motschulsky, 1857); (39) Rodolia fumida Mulsant, 1850; (40) Jauravia quadrinotata

Kapur, 1946; (41) Afissa mystica (Mulsant, 1850) comb. nov.

Bonn zoological Bulletin 69 (1): 27-44 ©ZFMK

40 Priyanka Das et al.

Figs 42-50. Scanning electron microscope images of Afissa mystica (Mulsant, 1850) comb. nov. (42) Habitus in ventral view; (43)

Head in ventral view; (44) Maxilla; (45) Labium; (46) Antennae; (47) Mandible; (48) Tarsal claws; (49) Labrum; (50) Meso-thorax.

Bonn zoological Bulletin 69 (1): 27-44 ©ZFMK

The Ladybird Beetles of Arunachal Pradesh, East Himalaya, India 4]

Figs 51-53. Afissa rana (Kapur, 1958). (51) Habitus; (52) Phallobase in dorsal view; (53) Sipho.

Material examined. Lohit: Dapha Bum, Kamlang River,

3020 ft, Stn. No. 23, 22.x11.1969, (4 exs), leg. J.M. Julka.

Tawang: Bomdila, 29.1x.2013 (1 ex. from Astimicia sp.)

(25410/H4A), leg. J. Majumder.

Distribution. India: Arunachal Pradesh (Lohit, Tawang),

and Meghalaya. Elsewhere: China and Nepal (Dieke

1947; Jadwiszczak & Wegrzynowicz 2003; Poorani

2004; Kovar 2007).

Genus Henosepilachna Li, 1961

41. Henosepilachna indica (Mulsant, 1850) (Fig. 37)*

Epilachna indica Mulsant, 1850: 776.

Epilachna ceylonica Weise, 1901: 418.

Epilachna indica: Kapur, 1961: 133-140.

Epilachna tertia Dieke, 1947: 66.

Henosepilachna indica: Jadwiszczak & Wegrzynowicz,

2003: 154.

Material examined. Lower Subansiri: Tamen, 457m,

Stn. No. 17, 18.v.1966 (1 ex.), leg. A.N.T. Joseph. Lo-

hit: Deopani, 350m, Stn. No. 8, 6.111.1969, (3 exs), leg.

S.K.Tandon; Kandu, 300 m, Stn. No. 9, 7.111.1969, (5

exs); Digaru Road, 150m, Stn. No. 12, 11.11.1969 (2

exs); Hayaliaung Road, 700 m, Stn. No. 13, 12.11.1969,

Bonn zoological Bulletin 69 (1): 27-44

(4 exs); Lohitpur Road, 150m, Stn. No. 14, 13.11.1969

(1 ex.); Namsai, 100 m, Stn. No. 15, 15.111.1969, (1 ex.),

leg. S.K. Tandon.

Distribution. India: Arunachal Pradesh (Lower Suban-

sirl, Lohit), Assam, and West Bengal. Elsewhere: Bhu-

tan, China, Laos, Myanmar, Nepal, and Vietnam (Dieke

1947; Poorani 2004; Kovar 2007).

42. Henosepilachna vigintioctomaculata (Motschulsky,

1857) (Fig. 38)**

Epilachna vigintioctomaculata Motschulsky, 1857: 40.

Epilachna 28-maculata a. incompleta Mader, 1930: 184.

Epilachna 28-maculata a. coalescens Mader, 1930: 184.

Henosepilachna_ vigintioctomaculata: Jadwiszczak &

Weerzynowicz, 2003: 178.

Material examined. NEFA, Abor, 29.x11.1911, (1 ex.)

leg. S.W. Kemp, New Aloppa: Rang, 17.1x.2000 (4 exs)

(25332/H4A), leg. A.R. Lahiri.

Distribution. India: Arunachal Pradesh. Elsewhere:

China, Japan, North Korea, Nepal, Russia, and Vietnam

(Katakura 1981; Poorani 2004).

©ZFMK

42 Priyanka Das et al.

Remarks. This 1s the first verified record of the species

from India, though it has been included from India by

Poorani (2004).

Tribe Noviini Mulsant, 1846

Genus Rodolia Mulsant, 1850

43. Rodolia fumida Mulsant, 1850 (Fig. 39)*

Rodolia fumida Mulsant, 1850: 904.

Rodolia roseipennis Mulsant, 1850: 904.

Rodolia chermesina Mulsant, 1850: 905.

Epilachna arethusa Mulsant, 1853: 254.

Epilachna testicolor Mulsant, 1853: 255.

Material examined. West Kameng: Ankaling, Stn.11,

17.v.1961 (1 ex.), leg. K.C. Jayram.

Distribution. India: Arunachal Pradesh (West Kameng),

Assam, Bihar, Delhi, Gujarat, Himachal Pradesh, Karna-

taka, Madhya Pradesh, Maharashtra, Manipur, Megha-

laya, Tamil Nadu, Uttarakhand, Uttar Pradesh, and West

Bengal. Elsewhere: China, Myanmar, Pakistan, and Sri

Lanka (Kapur 1949; Poorani 2004; Kovar 2007).

Tribe Sticholotidini Weise, 1901

Genus Jauravia Motschulsky, 1858

44. Jauravia quadrinotata Kapur, 1946 (Fig. 40)*

Jauravia quadrinotata Kapur, 1946: 85; Miyatake, 1985:

3, figs 1-3.

Material examined. West Kameng: 15.11.1961 (1 ex.),

leg. K.C. Jayram.

Distribution. India: Arunachal Pradesh (West Kameng),

Assam, Meghalaya, Sikkim, and West Bengal. Else-

where: Bhutan, China, and Nepal (Bielawski 1972;

Canepari 1997; Poorani 2002b, 2004; Kovar 2007).

Acknowledgements. The authors are thankful to the

Director, Zoological Survey of India, Kolkata for

providing necessary facilities. We wish to thank Dr Wang

Xingmin, South China Agriculture University, China,

for his help in providing literature. We are thankful to

Prof Basant Kumar Agarwala, Tripura University for his

beetle collections. We wish to thank Dr Dirk Ahrens and

Dr Ralph S. Peters (Zoologisches Forschungsmuseum

Alexander Koenig, Germany), and an anonymous

reviewer for critically reviewing the manuscript.

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©ZFMK

Bonn zoological Bulletin 69 (1): 45-54

2020 - Dongmo E.M. et al.

https://do1.org/10.20363/BZB-2020.69.1.045

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:Isid:zoobank.org: pub: B856B7FC2-EA09-404C-8542-3458777FE499

Diversity of bats (Mammalia: Chiroptera) along an altitudinal gradient

in the western region of Cameroon

Ervis Manfothang Dongmo’, Eric-Moise Bakwo Fils”, Aaron Manga Mongombe’ &

Fernand-Nestor Tchuenguem Fohouo*

"2.3 Department of Biological Sciences, Faculty of Sciences, University of Maroua, P.O. Box 814, Maroua, Cameroon

*Department of Biological Sciences, Faculty of Science, University of Ngaoundéré, P.O. Box 454 Ngaoundéré, Cameroon

* Corresponding author: Email: filshbkw27@gmail.com

'urn:lsid:zoobank. org:author:23 BESFBF-E2DF-4DF5-A34B-9BBC 10OAB5AAC

2urn:Isid:zoobank.org:author:A97 1C795-09AE-49DF-BB2C-51F397E1 8DOF

-urn:|sid:zoobank.org:author: 1556516C-665A-4F8C-9E0A-70C297CD3304

*urn:lsid:zoobank.org:author:77453B9B-A647-425B-BDED-E8C8CA929E72

Abstract. We investigated the patterns of bat species richness, abundance and distribution along an altitudinal gradient in

the West region of Cameroon from December 2016 to November 2018 with the use of mist nets. Captures were conducted

at 32 sites distributed over six distinct elevational ranges, comprising five sites in elevation range I (<< 750 ma.s.1.), four

sites in elevation range II (750—1,000 m a.s.1.), eight sites in elevation range IH (1,000—1,250 m a.s.1.), six sites in eleva-

tion range IV (1,250—1,500 m a.s.l.), six sites in elevation range V (1,500—1,750 m a.s.1.) and two sites in elevation range

VI (> 1,750 ma.s.l.). A total of 442 bats were captured during 95 sampling nights, comprising 25 species, 16 genera and

six families. Out of the 25 species, Mvonycteris angolensis was the most abundant species captured with 80 individuals,

followed by Micropteropus pusillus (61 individuals) and Eidolon helvum (60 individuals). Moreover, species richness

peaked at the mid-elevation range III (1,000—1,250 m a.s.l.), with 13 species, with richness decreasing both at higher and

lower elevations. Elevation range I had the second highest species richness with 12 species, while elevational range VI

had the least species riches with three species. Species abundance peaked at elevation range IV (750-1,250 m a.s.1.) and

decreases at higher elevations. The sample efficiency was estimated as 72.8% and a species accumulation curve of bats

did not reach an asymptote, indicating that our sampling was incomplete. Our data showed that species richness and ab-

undance is affected by elevation, with species richness probably depending on habitat types and availability of resources

such as food and suitable roost sites. Our data also contributes to a better description of the local fauna and fills gaps on

the species distribution for high altitude sites.

Key words. Bat, elevation range, diversity, West region, Cameroon, altitudinal gradient.

INTRODUCTION

The western region of Cameroon is characterized by a het-

erogeneous landscape, of series of high plateaus formed

by volcanic massifs, the most important of which are

the Bamboutos Mountains (2,740 m a.s.l.), interspersed

among lowland areas such as the Nkam and Noun valleys,

and the Tikar Plain (Temgoua 2011). This heterogeneous

landscape composed of montane forest remnants, grass-

land savannah and gallery forest in valleys is part of the

Mount Cameroon-Bioko ecoregion. This region harbors

some of the most threatened ecosystems in the country

(Temgoua 2011). Indeed, very little of the region’s native

biota remained, a consequence of decades of deforesta-

tion to make way for agriculture and urbanization. More-

over, the region harbors the highest population density

of the country with 13% of the national population, con-

centrated in only 3% of the territory (MINEPAT 2010).

The consequences of these strong anthropic pressures are

Received: 23.02.2019

Accepted: 20.01.2020

particularly evident on the Western High Plateau, where

poor soil and low rainfall have aggravated the effects of

deforestation, converting the area to grassland (Temgoua

2011). As pointed out by Estrada & Coates-Estrada

(2002), human-induced land use changes, due to agricul-

ture and urbanization are known to alter bat assemblages,

depending on the functional identity of bat species.

Bats are a species-rich group of mammals with about

357 species recorded in Africa (ACR 2018). They are

found in every biome throughout the African continent

with the exception of some extremely hot regions, and

the tops of high mountains (Happold & Happold 2013).

Several authors suggest that species richness and distri-

bution of bats is influenced by the availability of resourc-

es such as drinking sites, food and suitable roost (Curran

et al. 2012; Happold & Happold 2013). The potential

distribution of each bat species can be affected by these

ecological variables. In the tropics, vegetation types cor-

related with altitude are the principal factors that deter-

Corresponding editor: J. Decher

Published: 20.02.2020

46 Ervis Manfothang Dongmo et al.

mine bat species distribution (Kanuch & Kristin 2006;

Weier et al. 2016). Mammalian species show varied

responses to altitudinal gradient, among which two pat-

terns standout for bats: a clinal pattern in which species

richness is higher in lower elevations and decreases with

altitude (Graham 1983, 1990; Patterson et al. 1996; Pin-

ares 2006; Flores-Saldana 2008; Peters et al. 2016; Peters

et al. 2019), or modal pattern with a peak in richness at

mid-altitudes (Sanchez-Cordero 2001; McCain 2005). In

addition, Curran et al. (2012), recorded some bat species

mainly at higher altitudes, mid-altitudes and others pre-

ferred both low and high altitudes. They further pointed

out that bat activity and capture rates in the tropics are

greater at lower altitudes because water is not a limiting

factor.

Although many surveys have focused on the mamma-

lian fauna of Cameroon, few of these studies concerned

bats until recently. To the best of our knowledge none

of these studies assessed how bat species richness var-

ies with altitude in heterogeneous landscapes such as the

West region of Cameroon. Moreover, bats are not includ-

ed in conservation and wildlife management programs

in tropical ecosystems despite their ecological and eco-

nomic importance (Bakwo Fils 2009, 2010). This lack of

ecological information about the bats fauna of Cameroon

hinders any development and implementation of conser-

vation strategies (Bakwo Fils 2010).

In the western region of Cameroon elevations reach as

high as 2,000 m a.s.l. in some areas such as the Bambou-

tos and dip as low as 500 m a.s.l. in others such as the

Noun and Nkam valleys. To our knowledge, bat diver-

sity along an altitudinal gradient in the region has never

been studied. This study provides novel data for the West

region of Cameroon, a region poorly surveyed for bats.

Furthermore, knowledge of species-landscape relation-

ship and species distribution is essential for proper plan-

ning and efficient management of biodiversity (Jaberg &

Guisan 2001).

The present study aims to investigate patterns of dis-

tribution of bat species, species richness and abundance

along an elevational gradient in the western region of

Cameroon. We hypothesize that altitudinal pattern of bat

assemblages in the region would vary with altitude and

habitat heterogeneity, and that abundance and species

richness would decrease with increasing elevation.

MATERIALS AND METHODS

Study site

This study was conducted in the western region of Cam-

eroon. The region 1s situated between 5° and 6° N and

10° and 11°30’ E. The region covers a total surface area

of 13.892 km? (Olivry 1975; Brenac 1988). The vegeta-

tion is principally woodland savannah of the Sahel type,

Bonn zoological Bulletin 69 (1): 45-54

interspersed among open dry forest. Very little of the

natural vegetation still exists because deforestation has

turned most of the area into grassland (Temgoua 2011).

The climate of the western region of Cameroon ts of the

Equatorial, Guinean type characterized by two major

seasons: a rainy season from mid-March to November

with peak precipitation in August and a dry season from

December to April. The annual rainfall varies between

1,000 mm and 2,000 mm depending on the year (Riviere

2000). The average annual temperature varies between

21.3°C and 29°C (Brenac 1988).

Bats capture and identification

The survey was conducted from December 2016 to

November 2018 at different altitudinal ranges (Fig. 1).

Sampling was conducted over 95 nights across 32 sites.

Bat activity was investigated in six different elevational

ranges that represent a mosaic of different landscapes of

the West region of Cameroon as described by Temgoua

(2011), notably mountainous relief, plateaus and plains:

Mbo plain (< 750 m as.l.), Tika plain (750-1,000 m

a.s.1.), Noun plain (1 ,000—1,250 m a.s.1.), Bamoun plateau

(1,250—1,500 maz.s.l.), Bamileke plateau (1,500—1,750 m

a.s.1.) and the isolated volcanic massif (> 1,750 maz.s.1.).

During each sampling night, mist nets (12 m x 2.5 m;

mesh, 40 mm) were deployed at particular sites based

on prior knowledge of bat activity (over slow-flowing

streams, cultivated farms, clearings, cave openings and

tree hollows). Mist nets were deployed at each site be-

tween 6 pm to 12 midnight and checked every 15 min.

For each bat captured, morphometric measurements

were taken using a Vernier caliper (Ecotone-Poland

150/0.1 mm), weight was recorded using a Pesola spring

balance (Ecotone-Poland Light Line 200g/0.2), the sex,

reproductive conditions and age class were also noted.

Morphological measurements from each captured bat

were used for the identification of each species using the

keys in Rosevear (1965), Hayman and Hill (1971), Pater-

son and Webala (2012) and Happold & Happold (2013).

Bats were released after identification and species that

could not be identified in the field were kept as voucher,

and preserved in 70% alcohol and deposited at the Lab-

oratory of Biological Sciences of the University of Ma-

roua-Cameroon. The geographical positions of each site

sampled were recorded using a hand-held GPS (Garmin

eTrex).

Data Analysis

In order to test the relationship between abundance and

species richness, the Generalized Linear Mixed-effects

Modes (GLMMS) was used to discern the potential

effects of some altitudinal variables. We performed a

Kruskal-Wallis ANOVA followed by HSD tests (at 95

% family-wise confidence level) in order to determine

©ZFMK

Diversity of bats along an altitudinal gradient in the western region of Cameroon 47

Bae SR ee

eh , 2

gy =e @

‘ Niin : ~

Legend

@ Sampling sites

Sub divisions

Altitude Range (m)

1) 230-750

760-1000

HN 1100-1300

HN 1400-1500

HH 1600-1800

HM 1900-2700

Fig. 1. Map of Cameroon showing the West Region, and sites sampled for bats from November 2016 to November 2018.

if species richness, abundance, diversity and equitability

differed among elevation ranges. The software Estimate

S 9.0 (Colwell 2013) was used to calculate the number of

species (X) using the averages of Chao | (mean), ACE

(mean), Jack 1 (mean) and Bootstrap (mean) and to gen-

erate a species accumulation curve. The sampling effi-

ciency was calculated based on the formula below:

Observed number of species

Sampling efficiency = —————___——_———.__ x 100

estimated number of species

Cluster analysis was performed for all altitudinal rang-

es to test the degree of similarity between them and to

test if bat communities represent different assemblages.

The Sorensen index (Sorensen 1948), was calculated

and used in cluster analysis following the UPGMA (Un-

weighted Pair-Group) method using the arithmetic aver-

Bonn zoological Bulletin 69 (1): 45-54

age (Magurran & McGill 2011). Sorensen/Bray-Curtis

similarity dendrogram was then plotted using packages

of R software version 3.4.1 (R Core Team 2017).

RESULTS

Species richness and sampling success

During 95 sampling nights, we recorded a total of 442

bats, comprising 25 species, 16 genera and six families.

The family Pteropodidae had 7 species, followed by Hip-

posideridae with 6 species, Vespertilionidae with 5, Rhi-

nolophidae with 4, Molossidae with 2, and Nycteridae

with 1 species (Table 1). The species with the highest

capture frequency in the region was Myonycteris ango-

lensis (Bocage, 1898) (18.1% of all captures), followed

©ZFMK

48 Ervis Manfothang Dongmo et al.

Table 1. Individuals per species captured along an elevational gradient in the West region of Cameroon sampled from December

2 esto-NGvember DBs. a

Taxon Rangel Range Il Range III Range IV Range V Range VI Total

<750m 750-1,000m 1,000-1,250m = 1,250-1,500m_ = 1,500—-1,750m >1,750m

Pteropodidae

Micropteropus pusillus 2 18 20 12 it l 60

Eidolon helvum 1 1 18 4] 0) 0) 61

Myonycteris torquata 0 l 2 6 2 0 1]

Myonycteris angolensis 0 0 8 42 30 0 80

Rousettus aegyptiacus 13 0 1 0 0 0 14

Hypsignathus monstrosus 0 0 l 0 0 0 l

Epomops franqueti 0 1 0 0 0 0 l

Vespertilionidae

Pipistrellus nanulus 0 0 0 0 0 l l

Pipistrellus grandidieri 2 0 0 0 0 0 2

Neoromicia nana 1 0) 2 0) 4 0) 7

Scotoecus hirundo 1 0 0) 0) 0) 0) 1

Neoromicia tenuipinnis 0) 0) 4 0 0 0 4

Hipposideridae

Hipposideros abae 1 0 0 0 0 0 1

Hipposideros beatus 2 0 0 0 0 0 2

Doryrhina cyclops 11 0 3 0 0 0 14

Hipposideros ruber 15 26 0 0 0 0 4]

Hipposideros caffer 0 1 0 0 0 l

Hipposideros fuliginosus 25 0 4 0 0 0 29

Molossidae

Chaerephon pumilus 0 0) 29 0) 4 0 33

Mops nanulus 0 0 15 0 0 0 15

Rhinolophidae

Rhinolophus landeri 0) 28 0) 8 0) 1 37

Rhinolophus clivosus 0 l 0 0 0 0 l

Rhinilophus simulator 0 22 0 0 0 0 22

Rhinolophus alcyone 2 0 0 0 0 0 2

Nycteridae

Nycteris arge 0 1 0) 0) 0 0 1

Species abundance 76 99 108 109 47 3 442

Species diversity 12 9 13 5 5 3 25

Shannon diversity( H’) 2.8 ple 3.0 1.9 17 1.6 a7

by Eidolon helvum (Kerr, 1792) (13.8%) and Microptero-

pus pusillus (Peters, 1868) (13.6%) (Table 1).

Species richness was highest in elevational range II

(1,000-1,250 m a.s.l.) (13 species) and its bat fauna was

represented by Pteropodidae, Vespertilionidae, Hippo-

sideridae and Molossidae (Table 1). Chaerephon pumi-

lus (Cretzschmar, 1826) (n = 29), was the most abundant

species captured at this elevational range, followed by

Micropteropus pusillus (n = 20) and Mops (Xiphonyct-

eris) nanulus J. A. Allen, 1917 (n = 15). In elevation

range I (<< 750 m as.l.), we recorded a total of 12 spe-

Bonn zoological Bulletin 69 (1): 45-54

cles, represented by Pteropodidae, Vespertilionidae,

Hipposideridae and Rhinolophidae. Hipposideros fulig-

inosus (Temminck, 1853) was the most abundant (n =

25), followed by Hipposideros ruber (Noack, 1893) (n=

15) and then Rousettus aegyptiacus (E. Geoffroy, 1810)

(n = 13). In elevational range II (750—1,000 m a.s.1.), we

recorded 9 species, belonging to Pteropodidae, Hippo-

sideridae, Rhinolophidae and Nycteridae. Rhinolophus

landeri Martin, 1838 was the most frequently captured

bat (n = 28), followed by Hipposideros ruber (n = 26)

and then Rhinolophus simulator K. Andersen, 1904 (n=

©ZFMK

Diversity of bats along an altitudinal gradient in the western region of Cameroon 49

22). At elevational range IV (1,250—1,500 m) we record-

ed 5 species, represented by the families Pteropodidae

and Rhinolophidae. Elevation range VI (> 1,750 maz.s.1.)

was the least diverse, with 3 species (Pipistrellus nan-

ulus, Rhinolophus landeri and Micropteropus pusillus).

There was considerable difference in species diversity

and abundance across the different elevational ranges

(Table 1; Fig. 2).

@ Species richness

120

100

Range | Range Il

Range Ill

Species similarity along the elevational gradient

The Sorensen/Bray Curtis similarity test revealed that the

bat community structure of the six different elevational

ranges were similar (r-value = 0.8395) (Fig. 4). Range

I (< 750 m) and range II (750—1,000 m) form a simi-

lar cluster, and range III (1,000—1250 m) and range IV

(1,250—1,500 m) also form a similar cluster, indicating

O Species abundance

Range IV Range V Range VI

Fig. 2. Species diversity and abundance recorded at each elevational range in the West Region of Cameroon from November 2016

to November 2018.

Species richness and diversity along the elevational

gradient

Estimated species richness using Chao 1 (mean), ACE

(mean), Jack 1 (mean) and Bootstrap (mean) is 31.9;

38.5; 36.7; and 30.2 species respectively. The average

(x) of these four estimators is 34.3 species. The species

accumulation curve in the study area did not reach an

asymptote (Fig. 3), indicating that our sampling was in-

complete. The sample efficiency was 72.8 %, which in-

dicates that additional survey work is needed. The results

of the non-parametric one-way Kruskal-Wallis ANOVA

showed that mean species abundance of the six altitu-

dinal ranges did not differ statistically significantly at p

< 0.05 level (x?= 2.8651, df= 5, P= 0.7208). There was

also no statistically significant difference in species rich-

ness between elevational ranges (x? = 0.38798, df = 3,

p = 0.9427).

Bonn zoological Bulletin 69 (1): 45—54

similarity in bat community structure. The dendrogram

also indicates that bat community structure of elevational

range V (1,500—1,750 m a.s.l.) and elevational range IV

was quite different from the cluster formed by range I (<

750 m) and range I (750—1,000 m) and that formed by

range III (1,000—1250 m) and range IV (1,250—1,500 m)

(Fig. 4).

Altitudinal species richness and abundance relation-

ship

The results of the Generalized Linear Mixed-effects

Modes (GLMMS) showed that there is variation in bat

species richness and abundance along the altitudinal gra-

dient. There 1s also a negative relationship between bat

species richness and altitude. Indeed, it summarizes the

output of the binary logistic model used to discern the po-

tential effects of some altitudinal range on the observed

©ZFMK

50 Ervis Manfothang Dongmo et al.

Number of bats

0 100

—— S(est)

Estimated species

200

Number of iadiveate

S(est) 95% Cl Lower Bound

400

500

— — S(est) 95% Cl Upper Bound

Fig. 3. Species accumulation curve of bats captured in the West Region of Cameroon from November 2016 to November 2018.

Horizontal line (34.3) = average of four species richness estimators.

Similarity Coeffident (Dice)

[= = a

Range VI

Range V

Range IV

Range III

Range II

Range |

Fig. 4. Sorensen/Bray — Curtis similarity test Dendrogram for

altitudinal ranges of bats captured in the West region of Camer-

oon from November 2016 to November 2018.

Bonn zoological Bulletin 69 (1): 45-54

total species richness. The model showed no statistically

significant difference in species richness at p < 0.05 lev-

el among the six elevational ranges (estimate = 0.757 +

0.357, t= 2.118, p= 0.0341). The smallest t-value found

between the elevational ranges I and III, showed no sta-

tistically significant difference in species composition.

The t-values of comparisons of the species composition

between the groups, IV, V and VI showed the highest dif-

ference.

Abundance was positively correlated with elevation-

al ranges I, IV and VI respectively (estimate = 1.216 +

0.195, z = 6.227, P < 0.001), (estimate = 0.824 + 0.360,

Zz = 2.290, P = 0.02200) and (estimate = -1.620 + 0.701,

Z = -2.309, p = 0.02092). However, the elevational range

III and V respectively (estimate = -0.17492, z = -1.084,

p = 0.27815), (estimate = -0.39744, z= -0.992, p =

0.32107) were negatively correlated with altitude.

DISCUSSION

Our data show that bat species richness in the western

region of Cameroon shows a low-plateau with a mid-el-

evational peak at elevational range IH (1,000—1,250 m

a.s.l.), after which species richness declines (Table 1).

A low-plateau with a mid-elevational peak was also ob-

served for bats at Mount Mulanje, Malawi (Curran et al.

©ZFMK

Diversity of bats along an altitudinal gradient in the western region of Cameroon 51

2012). A number of hypotheses have been proposed to

explain the decrease in species richness with altitude

among which the most frequently cited explanations in-

clude the mid-domain effect (MDE) (Rahbek 1997) and

environmental factors such as climatic variables, pro-

ductivity and habitat heterogeneity (Nogués-Bravo et al.

2008; Sanders & Rahbek 2012). Indeed, Peters et al.

(2016) stressed the importance of temperature as the

main predictor of species diversity in both plant and ani-

mal communities. Furthermore, Peters et al. (2019) spec-

ified that variation in species diversity in tropical moun-

tains is mostly driven by the interaction of both climate

and human land use changes. The MDE on the other hand

suggest that if species ranges are randomly shuffled with-

in a bounded geographical domain free of environmental

gradients, ranges overlap increasingly toward the center

of the domain, creating a “mid-domain” peak of species

richness (Colwell & Hurtt 1994; Colwell & Lees 2000).

According to McCain (2009) water availability is higher

at lower elevations. More open water leads to an increase

in activity of insects and subsequently to an increase in

activity of insectivorous bats (Korine & Pinshow 2004).

Furthermore, MacArthur & MacArthur (1961) argued

that lower elevations may also possess greater structur-

al complexity in vegetation that provide more resources

and hence support a larger number of species. However,

differences in species richness pattern observed along

the elevational gradient may also be explained by the in-

teraction between climatic factors, vegetation structure

and anthropic land use. Also, more species were captured

at lower and intermediate elevations than at the highest

elevation, this can be partly explained by the fact that

relatively fewer sites were sampled at higher elevations.

Twenty-five bat species were recorded at different el-

evational ranges. Myonycteris angolensis was the most

abundant bat captured. This forest species 1s common

in Cameroon, and was previously recorded in Buea

(Matschie 1891), Bibundi, Bonge, Ndiang, (Sj6stedt

1897a, b), Bimbia, Tombel (Eisentraut 1941), Eseka

(Haiduk et al. 1981), Ngaoundere (Muller et al. 1981),

Dja Reserve (Bakwo Fils 2009), and Mpem and Djim

National Park (Atagana et al. 2018). The abundance of

this species at mid-elevations may be due to the existence

of numerous natural and manmade structures that pro-

vide day roosts. Meredith Happold pointed out that Myo-

nycteris angolensis is apparently common in some local-

ized areas where fruiting trees and caves or cave-like day

roosts are present (Happold 2013a — as Lissonycteris an-

golensis). Indeed, ACR (2018) established that Myonyct-

eris angolensis is widely distributed at elevations ranging

from sea level to 4000 m a.s.l. in Africa. Micropteropus

pusillus was recorded in all ranges and its distribution

in not homogeneous across the elevation gradient. Ac-

cording to Atagana et al.(2018), Micropteropus pusillus

is widespread in Cameroon, and inhabits forest, savan-

nah, plantation and ecotone areas. Eisentraut (1973)

Bonn zoological Bulletin 69 (1): 45—54

also recorded Micropteropus pusillus at elevations up to

1,800 m at Mount Manengouba. Eidolon helvum, Rouset-

tus aegyptiacus and Myonycteris torquata were recorded

at low and mid-elevations. Eidolon helvum was recorded

at elevations between 750 m and 1,500 m. Curran et al.

(2012) on Mount Mulanje in Malawi recorded E. hel-

vum only at mid-elevation (1,220-1,320 m). Indeed,

this species also preferred disturbed habitats and forms

large colonies around human habitations. Rousettus ae-

gyptiacus was only recorded at elevation below 1,250 m

and was conspicuously absent at higher altitudes. This

result contrast with that obtained in West Africa by Ver-

schuren (1976) and Denys et al. (2013) who reveal the

abundance of Rousettus aegyptiacus at high elevations.

Kwiecinski & Griffiths (1999) showed that the abun-

dance of Rousettus aegyptiacus at high elevation may be

due to the existence of numerous caves that provide day

roost. In Cameroon, this forest species was previously re-

corded in both primary and secondary forest by Sanborn

(1936), Sanderson (1940), Maisel et al. (2001), Bakwo

Fils (2009) and Atagana et al. (2018). Epomops franqueti

(Tomes, 1860) was recorded at mid-altitudes. These find-

ings are similar to those obtained by Eisentraut (1973)

who recorded Epomops franqueti at an altitude below

1,000 m on Mount Cameroon. Our study recorded only

a single individual of Hypsignathus monstrosus H. Allen,

1861 at mid-altitudes. According to Bergmans (1989),

Hypsignathus monstrosus 1s common in the rainforest,

and its abundance is determined by the availability of

ripe fruits. This species inhabits areas below 1,800 m and

was not recorded beyond this elevation (Happold 2013b).

This study revealed that vespertilionids were record-

ed in all altitudinal ranges. Pipistrellus nanulus Thomas,

1904 and Neoromicia tenuipinnis (Peters, 1872) were re-

corded at high and mid-altitudes respectively. Pipistrel-

lus cf. grandidieri (Dobson, 1876) and Scotoecus hirun-

do (de Winton, 1899) were recorded at low altitudes.

However, Neoromicia nana was recorded at both low

and mid-altitudes. According to Soriano (2000), some

species of vespertilionids may be better adapted to higher

altitudes with colder climate despite their size. Bat spe-

cies of the family Molossidae were captured at mid-alti-

tudes around man-made structures that provide day roost.

These findings corroborate those of McWilliam (1989)

and Esbérard (2003) who suggested that there is a high

probability of sampling molossids in front of their exit or

near possible roosts in roof linings of human residences.

Bats of the family Hipposideridae, Rhinolophidae and

Nycteridae have a higher richness and abundance in both

low and mid-altitudes. Our result is consistent with the

findings of Curran et al.(2012) who previously captured

a higher amount of bat species of the families Hipposide-

ridae, Rhinolophidae and Nycteridae between 630 and

1,030 m altitude on Mount Mulanje in Malawi. Rosevear

(1965), Schober & Grimmberger (1997), Georgiakakis

(2010) and Happold & Happold (2013) suggested that

©ZFMK

52 Ervis Manfothang Dongmo et al.

the distribution of some species like Hipposideros ruber,

H. fuliginosus, Rhinolophus landeri and R. simulator are

most consistently associated with day roosts and food

availability. Our data reveals the presence of a single

individual of Rhinolophus landeri Martin, 1838 at high

altitude in a cultivated area. At Mount Cameroon, Rose-

vear (1965) recorded R. /anderi in montane vegetation at

1,400 m, while Largen et al. (1974) captured it in Ethio-

pia from 515 to 1,800 m and found no marked altitudinal

preference. We recorded only a single individual each of

Hipposideros abae J. A. Allen, 1917, H. caffer (Sunde-

vall, 1846), Rhinolophus clivosus Cretzschmar, 1828,

and Nycteris arge Thomas, 1903 in our study, probably

indicating the rarity of these species.

This study has allowed us to obtain data on the distri-

bution of bat species with respect to the landscape of the

western region of Cameroon. However, we observed that

insectivorous bats are more diversified (18 species) but

less abundant (214 individuals) compared to frugivorous

bats that are less diverse (seven species), but more abun-

dant (228 individuals). This may be related to a bias in the

capture method that involved the use of understory mist

nets that are known to be efficient at capturing sub-can-

opy frugivorous bats (Fleming 1982). Additionally, it is

well established that mist nets have good success only

in Open environments (streams, cultivated farms, clear-

ings) (Martins et al. 2015). As pointed out by Kaftuch &

KriStin (2006), Rhinolophidae, Hipposideridae and some

Vespertilionidae can easily avoid mist nets because of

their efficient echolocation calls. Therefore, for more

exhaustive studies we recommend the use of harp traps,

echolocation recording and canopy netting to supple-

ment standard mist-netting. Our sampling efficiency was

estimated as 72.8%, confirming that additional surveys

might significantly improve our chances of recording

species new to the area. The similarity found between

the elevational ranges IV and V, and between elevation

ranges III and IV, V, is probably be related to the higher

turnover of bat species between these elevations (Mar-

tins et al. 2015). According to Lomolino (2001), biotic

turnover varies along the elevation gradient and depends

directly on the richness of the overlapping community.

In conclusion, our study provides baseline data on the

altitudinal ranges of bats in the western region of Camer-

oon. Species richness and abundance was higher at low

and mid-elevations but lower at higher altitudes. This

pattern of diversity is probably driven by differences in

ecological heterogeneity among the different elevational

ranges that provide suitable habitats for a number of spe-

cies. However, further research may be required to eval-

uate the impact of different habitats types on populations

of bat species in the western region of Cameroon.

ACKNOWLEDGMENTS. We express our appreciation to

IDEA WILD for providing field material. Our grateful thanks

goes to the lecturers of the Department of Animal Biology Uni-

Bonn zoological Bulletin 69 (1): 45-54

versity of Maroua for their constructive criticisms and sugges-

tions during field work. The research permit was granted by

Cameroon Ministry of Scientific Research and Innovation (Ref:

0000011 /MINRESI /BO00 /C00/C10/C 14).

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Bonn zoological Bulletin 69 (1): 55—83

2020 - Kerbis Peterhans J.C. et al.

https://do1.org/10.20363/BZB-2020.69.1.055

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub: 1 FD4D09C-D160-4159-A50D-20B6FBC7D9E9

Four new species of the Hylomyscus anselli group

(Mammalia: Rodentia: Muridae)

from the Democratic Republic of Congo and Tanzania

Julian C. Kerbis Peterhans' *, Rainer Hutterer’, Jeffrey B. Doty’, Jean M. Malekani*, David C. Moyer’,

Jarmila Krasova‘, Josef Bryja’, Rebecca A. Banasiak’® & Terrence C. Demos?

‘College of Arts & Sciences, Roosevelt University, 430 S Michigan Ave, Chicago, IL USA 60605

1.3.8.9 Science and Education, Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL 60605, USA

?Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany

3U.S. Centers for Disease Control and Prevention, Poxvirus and Rabies Branch, 1600 Clifton Rd. Atlanta, GA 30333, USA

‘Département de Biologie, Faculté des Sciences, Université de Kinshasa, Kinshasa, Democratic Republic of Congo

"> PO. Box 691, Iringa, Tanzania

6 Department of Zoology, Faculty of Science, University of South Bohemia, Ceské Budéjovice, Czech Republic

‘Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic

’Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic

* Corresponding author: Email: jkerbis@fieldmuseum.org

'urn:Isid:zoobank.org:author:3B4A 1 A6B-B0O1E-4FF8-ADF1-6CF1FE102D20

2urn:lsid:zoobank.org: author: 16023337-0832-4490-89A9-846AC3925DD8

3urn:Isid:zoobank.org:author:33 A FA407-C88F-4A 8C-B694-A F29E3F894D7

4urn:Isid:zoobank.org:author:B1445794-1COA-4861-8AED-1A8C3434BBD3

Surn:lsid:zoobank.org:author:D73C593 D-82B0-4587-8C70-52E3AA72B538

6urn:lsid:zoobank.org:author: 1 Fl FFB1 B-E594-404B-AE93-EB8D9B9BA 101

7urn:Isid:zoobank.org:author:63C1A788-1102-4CBC-A0D3-B2434097359D

Surn:Isid:zoobank.org:author:5 DD1017E-0692-4049-8420-C4705EB2B505

°urn:Isid:zoobank.org:author:90A9F9F 1-8113-4B5E-BOE2-DA0212D118E4

Abstract. As in many other small mammal groups from the Afrotropics, the number of species recognized within the ge-

nus Hylomyscus has increased considerably over the past dozen years. The last comprehensive review (2005) of the genus

recognized eight species. Since that time, nine additional species have been elevated from synonymy (n = 4) or described

as new (n = 5). Here we describe four additional new species supported by morphological and molecular evidence, all

collected by the late William Stanley. Two of the new taxa are sympatric and come from the poorly known left bank (di-

rection source to mouth) of the Congo River. One of these (Hy/omyscus pygmaeus sp. nov.) is easily recognized, as it is

tiny and significantly smaller than any known species of the genus; the second new species (Hylomyscus thornesmithae

sp. nov.) is also small, and syntopic with the first. The third new species (Hylomyscus stanleyi sp. nov.), from the SW

corner of Tanzania, is quite large and had been previously included within the hypodigm of Hylomyscus anselli following

its recognition from within the synonymy of Hy/omyscus denniae. The fourth species (Hylomyscus mpungamachagorum

sp. nov.) is from Mahale Mountains National Park, western Tanzania. Our study reveals a much higher species diversity of

the genus than previously known, providing insights into additional Afrotropical and Afromontane centers of endemism

that require further exploration.

Key words. Afrotropics, biodiversity, endemism, Murinae, molecular phylogeny, systematics, alpha-taxonomy, biogeo-

graphy.

INTRODUCTION

Members of the genus Hy/lomyscus (wood mice) are

widespread in the forests of sub-Saharan Africa, north of

the Zambezi River. They are small (15-35 g), with tails

longer than head and body and have skulls with a short

upper tooth row and narrow zygomatic plates. Their short

broad feet suggested to their describer that they were

Received: 17.09.2019

Accepted: 31.01.2020

more arboreal than their relatives in the genus Praomys

from which they were split (Thomas 1926). In 2005,

Musser and Carleton recognized eight species within the

genus: Hylomyscus aeta (Thomas, 1911); H. alleni (Wa-

terhouse, 1838): H. baeri Heim de Balsac & Aellen, 1965;

H. carillus (Thomas, 1904); H. denniae (Thomas, 1906);

H. grandis Eisentraut, 1969; H. parvus Brosset et al.

1965; and H. stella (Thomas, 1911). Within one year, this

Corresponding editor: J. Decher

Published: 28.02.2020

56 Julian C. Kerbis Peterhans et al.

total increased to 12 (Carleton et al. 2006) with the de-

scription of H. arcimontensis Carleton & Stanley, 2005;

and the elevation from synonymy of H. anselli (Bish-

op, 1979), H. vulcanorum (Lonnberg & Gyldenstolpe,

1925), and H. endorobae (Heller, 1910). Since that time,

one additional species has been elevated from synonymy

(H. simus Allen & Coolidge, 1930) and four have been

described as new: H. heinrichorum Carleton et al., 2015,

H. kerbispeterhansi Demos et al., 2014, H. pamfi Nicolas

et al., 2010 and H. walterverheyeni Nicolas et al., 2008,

bringing the total to 17. Carleton et al. (2006), using

phenetic characters, proposed six species groups within

the genus (‘H. aeta’, ‘H. alleni’, ‘H. anselli’ , ‘H. baerv’,

‘H. denniae’, and ‘H. parvus’ groups). Eight characters

were used to define the ‘H. ansel/li’ group, four of which

distinguished it from the ‘H. denniae’ group with which

it had been previously lumped: six mammae (instead of

eight), shorter rostrum, shorter incisive foramina and a

medium-sized subsquamosal foramen (compared to a

tiny or absent subsquamosal foramen). Two species of

the ‘H. anselli group (H. anselli and H. arcimontensis)

and three of the “H. denniae’ group (H. denniae, H. vul-

canorum and H. endorobae) were recognized at that time.

Today, the ‘H. denniae’ group is restricted to the mon-

tane highlands of the Albertine Rift and the Kenya High-

lands whereas the *‘H. ansel//i’ group 1s distributed from

the Kenya Highlands through the Eastern Arc and South-

ern Highlands of Tanzania (and northernmost Malawi),

into the gallery forests of northern Zambia and the high-

land plateau of Angola. The other four species groups are

confined to the tropical regions of the continent. Here we

redefine this geographic pattern by describing four new

species of the ‘H. anse/li’ group from a previously un-

documented area of the Congo Basin and two isolated

forests in western Tanzania.

MATERIAL AND METHODS

Specimens, morphology, morphometrics, collecting

Specimens are from the Field Museum of Natural His-

tory, Chicago (FMNH), National Museum of Zambia,

Livingstone (NMZ) and British Museum Natural His-

tory, London (BMNH). Additional Zambian and Ango-

lan records use the initials from their collectors (RS, R

Sumbera) or country of origin (ANG, Angola) and are

deposited in the Faculty of Sciences, University of South

Bohemia (USB) in Ceské Budéjovice (carcasses) and in

the Institute of Vertebrate Biology (IVB) of the Czech

Academy of Sciences, Studenec (tissues and skulls), both

in the Czech Republic. Field measurements, in millime-

ters, include: Total Length (TL), Tail vertebrae (TV),

Hind foot length (HF), Ear length (EL), Weight (Wt, in

grams); subtraction of TV from TL provides the head-

and-body length (HB) unless measured separately in the

Bonn zoological Bulletin 69 (1): 55—83

field. All external measurements were taken from orig-

inal field data by respective collectors. Only two spec-

imens of H. heinrichorum have weight recorded (both

ANG). Length of hind foot includes the claw. Hind foot

measurements of Hylomyscus heinrichorum from Angola

and all Hylomyscus anselli from Zambia specified ‘su’

(sans unguinal). Accordingly, 1.0 mm was added to HF

for missing claw length measurements. We employed the

following 16 cranial measurements in millimeters (Car-

leton & Van der Straeten 1997): occipito-nasal length

(ONL), condyle-incisive length (CI), greatest zygomatic

breadth (ZB), breadth of the braincase measured across

the parietal flanges behind the zygomatic arches (BBC),

breadth across the occipital condyles (BOC), least inter-

orbital breadth (OB), length of nasals (LN), breadth of

the rostrum (BR), post-palatal length (PPL), length of the

bony palate (LBP), length of the incisive foramen (LIF),

length of upper diastema (LD), breadth of the zygomat-

ic plate (BZP), length of the auditory bulla, oblique to

tooth row (LAB), coronal (rather than alveolar) length

of the maxillary toothrow (CLM), and width of the first

upper molar (WM1). We define rostral length as length

of nasals divided by occipito-nasal length (LN/ONL). In

order to estimate relative age and ontogenetic growth,

we adopt dental wear stages from Verheyen & Bracke

(1966). Specimens were measured and weighed, and e1-

ther prepared as skins and skeletons or fixed in formalin

and later transferred to 70% ethanol, and deposited at

FMNH or USB. DRC refers to the Democratic Republic

of Congo and TZ refers to Tanzania. An aliquot of tissue

was taken from the specimen at the time of capture and

preserved in ETOH until it was transferred to cryogenic

storage at -180 °C at FMNH.

Principal components analysis (PCA) of 16 log-trans-

formed cranio-dental variables based on a variance-cova-

riance matrix was used to assess morphometric variation

and visualize the morphometric distinctiveness of named

and putative species for an eight species data set (159

specimens: H. anselli, H. arcimontensis, H. heinricho-

rum, H. kerbispeterhansi, H. sp. nov. 1 (pygmy Hylomy-

scus from DRC), H. sp. nov. 2 (small Hylomyscus from

DRC), H. sp. nov. 3 (Mbizi Hylomyscus from Tanzania),

H. sp. nov. 4 (Mahale Hylomyscus from Tanzania) and a

four species data set (136 specimens: H. arcimontensis,

H. kerbispeterhansi, H. sp. nov. 3 (Mbizi Hylomyscus

from Tanzania) and H. sp. nov. 4 (Mahale Hylomyscus

from Tanzania). Standard summary statistics were calcu-

lated from univariate measurements for 16 cranio-den-

tal and six external characters. All statistical analyses

were performed using the software PAST (Hammer et al.

2001).

Permission for the collection and export of specimens

was provided by the Republic of Tanzania and the Dem-

ocratic Republic of Congo. Approval for the import of

specimens into the USA was provided by the US Fish

and Wildlife Service. Relevant documents pertaining to

©ZFMK

Four new Hylomyscus (Muridae) from Africa 57

export and import are housed at FMNH under the follow-

ing Accession Numbers: Z-20745, Z-20738, Z-19855,

Z-19599. All euthanized specimens followed the proto-

col approved by the American Society of Mammalogists

(Sikes et al. 2011). The study was approved by the Field

Museum of Natural History Institutional Animal Care

and Use Committee (09-3).

DNA extraction, amplification, and sequencing

Whole genomic DNA was extracted from tissue samples

of H. aeta (n = 1, Uganda), H. stella (n = 1, Uganda),

H. heinrichorum (n = 4, Angola), H. sp. nov. 1 (pygmy

Hylomyscus from DRC, n = 1), H. sp. nov. 2 (small Hy-

lomyscus from DRC, n = 5), H. sp. nov. 3 (Mbizi Hy-

lomyscus from Tanzania, n = 5), H. sp. nov. 4 (Mahale

Hylomyscus from Tanzania, n = 3) using the QIAGEN

DNeasy Blood and Tissue Kit (Germantown, MD). An

additional 34 Hylomyscus cytochrome-b (Cytb) sequenc-

es were downloaded from GenBank (Appendix 2). Mas-

tomys natalensis, a close relative of Hylomyscus (Step-

pan & Schenk 2017), was chosen as an outgroup using

a Cytb sequence downloaded from GenBank. In total,

sequence data was generated or downloaded from Gen-

Bank for 16 of 18 currently recognized species (Mam-

mal Diversity Database 2019) from all six Hylomyscus

Species groups. Frozen tissues and GenBank accessions

were unavailable for H. carillus (Angola). Specimens

were sequenced for Cytb using the primers L14723 and

H159125 (Lecompte et al. 2002). PCR amplification was

performed on 25 wL reactions using the following ther-

mal conditions: an initial denaturation step at 94 °C for

3 min, followed by 38 cycles consisting of 30 s at 94 °C,

30 s at 50 °C, and 1 min at 68 °C, followed by a final

extension step of 5 min at 68 °C. Amplified PCR prod-

ucts were purified using ExoSAP-IT (Thermo Scientific,

MA, USA). Sequencing was carried out in both direc-

tions on an ABI 3100 thermocycler (Applied Biosystems,

CA, USA) at the Pritzker Laboratory for Molecular Sys-

tematics and Evolution (FMNH). Chromatographs were

checked manually and assembled and edited using Ge-

neious 11.1.5 (Biomatters Ltd.). Sequences were aligned

for Cytb using MUSCLE Alignment within the Geneious

platform with default parameters. Sequence data from

Cytb were translated into amino acids and the alignment

was inspected for deletions, insertions, and premature

stop codons to exclude possible nuclear pseudogenes.

Molecular data and phylogenetic analyses

The best supported model of nucleotide substitution for

Cytb was determined using the BIC on the maximum

likelihood topology inferred in ;jMODELTEST2 v.2.1.6

(Darriba et al. 2012) on CIPRES Science Gateway v.3.3

(Miller et al. 2010). Interspecific uncorrected sequence

divergences (p-distances) were calculated in MEGA

Bonn zoological Bulletin 69 (1): 55—83

7.0.26 (Kumar et al. 2016). Maximum likelihood infer-

ence of a Cytb gene tree was made using the program

IQ-TREE v1.6.10 (Nguyen et al. 2015) on the CIPRES

portal. We conducted analyses using the best-scoring ML

tree search algorithm under the GTR+I+G model with

1,000 bootstrap replicates. Bayesian gene tree analyses

were carried out using MRBAYES v.3.2.6 (Ronquist

et al. 2012) on the CIPRES portal to infer a Cytb gene

tree. Two replicates were run to facilitate proper mixing.

Four Markov chains with default heating values were

conducted for 10,000,000 generations and sampled every

1,000th generation. Stationarity of the MCMC chain was

assessed using TRACER v.1.7.1 (Rambaut et al. 2018).

The first 2,500 samples were discarded as burn-in and the

remaining 7500 samples comprised the posterior proba-

bility (PP) distributions. A majority rule consensus tree

was generated from the analysis. All newly generated

sequences were deposited in GenBank with accession

numbers MN857618—MN857637 (Appendix 2). We use

these gene tree analyses to test the concordance of spe-

cies limits inferred using morphological data with clades

supported by genetic data, estimate support for mono-

phyly of recognized and putative species, and assess phy-

logenetic relationships among them.

RESULTS

The specimens from the Congo basin (DRC) were clearly

undescribed members of the H. anselli clade based on

their morphological characters: short feet, teat formula

(2+4 for Hylomyscus sp. nov., small Hylomyscus), short

incisive foramen, thin stapedial strap and medium-size

subsquamosal foramen. Their small size confirmed their

unique status within the H. anselli clade. Subsequent ge-

netic analyses were instrumental in revealing the exis-

tence of the two cryptic Tanzanian species.

Morphometrics

Two principal component analyses were performed on

16 log-transformed cranio-dental variables. The first in-

cluded all eight putative species of the H. anselli group

(Fig. 1); the second (Fig. 2) included those four species

found east of the Albertine Rift Valley (Fig. 3). In the

eight species PCA (Fig. 1), the small-sized Congo Ba-

sin taxa (H. sp. nov. 1, pygmy Hylomyscus from DRC

and H. sp. nov. 2 (small Hylomyscus from DRC) are dis-

tinguished from all other species in the H. anselli group

along the first axis and will not be discussed further. The

Angolan taxon (H. heinrichorum) is distinguished along

the second axis from the Zambian taxon (H. anselli).

In the four species PCA (Fig. 2), H. kerbispeterhan-

si and Hylomyscus sp. nov. 3 (Mbizi Hylomyscus from

Tanzania) are readily distinguished along the second

axis. Hylomyscus sp. nov. 3 (Mbizi Hylomyscus from

©ZFMK

58 Julian C. Kerbis Peterhans et al.

sp. nov. 2 (small

Hylomyscus from DRC)

sp. nov. 3 (Mbizi

Hylomyscus from

Tanzania) (*)

anselli (m)

sp. nov. 4 (Mahale Hylomyscus (@)

from Tanzania)

PC2 8.2%

¥ sp.nov. 1 (pygmy Hylomyscus

from DRC)

-0.7 -0.6 -0.5 -0.4 -0.3

kerbispeterhansi (CO)

heinrichorum (x)

-0.2 -0.1 6.0 0.1 0.2

PC1 68.1%

Fig. 1. Principle component analysis of cranial measurements of all eight members of the Hylomyscus anselli group.

Tanzania) has only modest overlap along the 1% and

2™ axes with H. arcimontensis, but H. kerbispeterhansi

and H. arcimontensis show overlap along both principle

components. Hylomyscus sp. nov. 4 (Mahale Hylomy-

scus from Tanzania) does overlap with H. arcimontensis

in PCA multivariate space (Fig. 2) but they are allopatric

and occupy different biogeographic regions: Hylomyscus

arcimontensis 1s confined to the Eastern Arc montane ar-

chipelago while Hylomyscus sp. nov. 4 (Mahale Hylomy-

scus from Tanzania) is known only from the Albertine

Rift; see Fig. 3).

In the eight species PCA, the first two principle com-

ponents accounted for 76% of the cumulative variance

(Table 1). The major contributing variables on PC1 were

all correlated with the length of the rostrum: length of in-

cisive foramen (LIF), length of nasals (LN) and length of

Bonn zoological Bulletin 69 (1): 55—83

diastema (LD). On PC2 the major contributing variables

were breadth of zygomatic plate (BZP), length of nasals

(LN), and length of bony palate (LBP). In the four spe-

cies PCA the first two principle components accounted

for 64% of the cumulative variance (Table 2). The major

contributing variables on PC1 were identical to PC1 on

the eight species PCA: length of diastema (LD), length

of incisive foramen (LIF) and length of nasals (LN). On

PC2, the most important variables were breadth of zy-

gomatic plate (BZP), length of bony palate (LBP) and

crown length of molars (CLM).

Genetic analyses

The mtDNA gene tree (Fig. 4) supports the monophy-

ly of the Hylomyscus anselli group minus H. sp. nov. 1

©ZFMK

Four new Hylomyscus (Muridae) from Africa 59

Table 1. PCA loadings from all eight members of the Hy/omy-

scus anselli group.

Variable Correlations

PCl PC2

ONL 0.240 0.106

CI 0.253 0.095

ZB 0.192 0.102

BBC 0.138 0.040

BOC 0.143 -0.096

IO O41 52 -0.094

LN 0.359 0.427

BR 0.209 0.183

PPL 0.212 0.089

LBP 0.208 0.359

LIF 0.381 -0.220

LD 0.302 0.196

BZP 0.281 -0.636

LAB 0.234 -0.015

CLM O.297 -0.208

WMI 0.267 -0.251

Cumulative % variance 68.1 76.3

Eigenvalue 0.0081 0.0010

(pygmy Hylomyscus from DRC; bootstrap [BS] = 99,

posterior probability [PP] = 1.0). The new species, Hy-

lomyscus sp. nov. 1 (pygmy Hylomyscus from DRC)

from the western Congo basin, is highly divergent from

other H. anselli group species (10.9-12.1% Cytb p-dis-

tance), and moderately well supported as sister to all

other H. anse/li group members (BS = 82, PP = 0.96).

The new species Hylomyscus sp. nov. 2 (small Hylomy-

scus from DRC), H. sp. nov. 3 (Mbizi Hylomyscus from

Tanzania) and H. sp. nov. 4 (Mahale Hylomyscus from

Tanzania) are well supported clades (bootstrap = 100,

posterior probability = 1.0). Carleton and Stanley (2005)

and Carleton et al. (2006, 2015) assigned specimens from

the Mbizi Mountains, Tanzania, to H. anselli based on

similar phenetics and geographical proximity. However,

our PCA (Fig. 1) shows little overlap between H. anselli

and H. sp. nov. 3 (Mbizi Hylomyscus from Tanzania), al-

though we had access to only four members of H. ansel-

li. Further, our newly available genetic data indicate

that this assignment was incorrect. The Mbizi Hylomy-

scus population is now assigned to distantly related H.

sp. nov. 3 (Mbizi Hylomyscus from Tanzania, Fig. 4), il-

lustrating how ‘cryptic’ these species are. H. anselli and

H. sp. nov. 3 (Mbizi Hylomyscus from Tanzania) are not

even sister; the genetic distance between them is 8.2% at

Cytb (Table 3). Hylomyscus sp. nov. 3 (Mbizi Hylomy-

scus from Tanzania) + H. sp. nov. 4 (Mahale Hylomyscus

Bonn zoological Bulletin 69 (1): 55—83

- Variable

Table 2. PCA loadings from four members of the Hylomyscus

anselli group found east of the Albertine Rift.

Correlations

PEA PE?

ONL 0.231 0.102

CI 0.267 -0.027

ZB 0.211 0.037

BBC 0.155 0.107

BOC 0.146 -0.006

IO 0.160 0.216

LN 0.314 0:3827

BR 0.278 -0.131

PPL 0.260 0.044

LBP 0.208 0.392

LIF 0325 -0.229

LD 0.340 -0.222

BZP 0.280 -0.546

LAB 0.298 -0.209

CLM 0.215 0.375

WMI 0.197 0.258

Cumulative % variance 52:6 64.3

Eigenvalue 0.0034 0.0008

from Tanzania) + H. kerbispeterhansi form a distinct and

highly supported East African clade (BS = 82, PP = 0.96)

distributed in montane habitats in Kenya and Tanzania.

These species exhibit allopatric distributions within the

H. anselli group, although H. kerbispeterhansi 1s sympat-

ric with H. endorobae (H. denniae group) on the Mau Es-

carpment in west-central Kenya (see Demos et al. 201 4a,

b; 2015). The relationship of H. arcimontensis from Tan-

zania 1s weakly supported (BS = 79, PP = 0.87) as sister

to the aforementioned three East African H. anselli group

species. Hylomyscus sp. nov. 2 (small Hylomyscus from

DRC), also from the western Congo Basin, is strongly

supported (BS = 92, PP = 1.0) as sister to the geograph-

ically distant and disjunct East African H. anselli group

clade. Hylomyscus anselli, now restricted to Zambia on

the basis of data from this study, is strongly supported

(BS = 100, PP = 1.0) as sister to H. heinrichorum from

Angola, and this clade (H. anselli + H. heinrichorum) is

strongly supported (BS = 99, PP= 1.0) as sister to a clade

that includes representatives of the H. ansel/li group from

both East Africa and the western Congo Basin.

New taxa

All four new species (Hy/omyscus sp. nov. 1, sp. nov. 2,

sp. nov. 3, sp. nov. 4) described here nest within the H.

anselli group. Of the characters suggested to define the H.

©ZFMK

60 Julian C. Kerbis Peterhans et al.

arcimontensis

PC2 11.7%

sp. nov. 4 (Mahale

Hylomyscus from Tanzania)

-0.20 0.16 -0.12 -0.08 -0.04

sp. nov. 3 (Mbizi

Hylomyscus from Tanzania)

0.00 0.04 0.08 012 0.16

PC1 52.6%

Fig. 2. Principle component analysis of cranial measurements of the four members of the Hy/omyscus anselli group found east of

the Albertine Rift.

anselli group (Carleton et al. 2006), the most reliable in-

clude abbreviated incisive foramina, the absence of pecto-

ral mammae (total mammae = 2+4) and the thin, elongate

hamular process providing for enlarged sub-squamosal

foramina (discussed and illustrated in Carleton & Stanley

2005: fig. 6). These characters distinguish the H. anselli

group from the H. denniae group, the only two groups

with montane representatives to the east and south of the

Congo Basin. All of the four new taxa described below

possess these three characters; however, in Hylomyscus

pygmaeus sp. nov. (pygmy Hylomyscus from DRC), teats

are not visible, as the specimen is young.

Bonn zoological Bulletin 69 (1): 55—83

Hylomyscus pygmaeus sp. nov. Kerbis Peterhans, Hut-

terer & Demos

urn: lsid:zoobank.org:act: 1B7A9BDE-24A0-47DE-9B66-F3 B40DISEES4

Dendromus sp. — Doty et al. (2017)

Holotype. Field Museum of Natural History, Division

of Mammals number FMNH 219684 (field number WT

Stanley 11,575; CDC 207), collected by W.T. Stanley, 13

June 2012 (listed in field notes as Dendromus sp.) during

the first small mammal survey in the area. The specimen,

consisting of a study skin and skull with carcass in al-

cohol, is a young adult female with first upper molar in

early wear (stage IV of Verheyen & Bracke 1966). The

basisphenoid-occipital suture is unfused. External mea-

©ZFMK

Four new Hylomyscus (Muridae) from Africa 61

Table 3. Uncorrected cytochrome-b p-distances (%) within (bolded numbers on diagonal) and between Hylomyscus anselli group

species, calculated in MEGA 7.0.26 (Kumar et al. 2016).

Taxon 1 2 8) 4 5 6 7 8

1 anselli 1.1

2 arcimontensis 8.1 1:5

3 mpungamachagorum sp. nov. See 6.0 0.0

4 heinrichorum 44 Oo 8.4 0.3

5 kerbispeterhansi 8.1 6.6 4.7 8.0 0.0

6 stanleyi sp. nov. 8.2 6.3 49 93 a 0.0

7 thornesmithae sp. nov. 8.6 6.6 6.6 8.3 6.9 6.4 0.0

8 pygmaeus sp. Nov. ES LO 10.9 10.9 10.8 dS) | | na

= = = denniae group

denniae

endorobae

vulcanorum

anselli_group

anselli

arcimontensis

thoresmithae

heinrichorum

mpungamachagorum

pygmaeus

stanleyi

kerbispeterhansi

Biege

ee. Ly "

0 125 250

Fig. 3. Map of the distributions of members of the Hylomyscus denniae and Hylomyscus anselli groups.

surements were made in the field: TL 132, TV 76, HF 14, — Type locality. Democratic Republic of Congo, Tshuapa

EL 12, Wt 5.8. Specimen caught in a pitfall trap (PF 4, Province, 4 km N of Boende, Baliko (0.24127 S, 20.8833

Bucket 10). E), right side Tshuapa River, elevation of 358 m.

Bonn zoological Bulletin 69 (1): 55—83 ©ZFMK

97/1.0

95/1.0

100/1.0 | Tanzania Mahale FMNH177889

100/1.0

79/0.87

100/1.0

92/1.0

99/1.0

82/0.96

96/1.0

82/-

73/0.73

62/0.78 97/1.0

49/0.96 83/0.83

81/0.98

parvus Cameroon JQ735555

baeri Guinea JQ735509

aefa Uganda FMNH160492

10 100/1.0

grandis Cameroon JQ735513

39/.

92/1.0

denniae Uganda FMNH144526 KF876479

(— Mastomys natalensis JX292865

0.03

endorobae Kenya FMNH190467 KF810158

vuleanorum DRC FMNH203881 KF810176

Julian C. Kerbis Peterhans et al.

Kenya Cherangani FMNH217384 KF810206

Kenya Cherangani FMNH217385 KF810203

Kenya Cherangani FMNH217383 KF810205

Kenya Elgon FMNH217358 KF810200

Kenya Elgon FMNH217325 KF810239

Kenya Elgon FMNH217601 KF810240

Kenya Mau FMNH210000 KF810226

Kenya Mau FMNH210001 KF810231

Tanzania Mbizi FMNH171362

Tanzania Mbizi FMNH171363

100/1.0) Tanzania Mbizi FMNH171360

Tanzania Mbizi FMNH171352

Tanzania Mbizi FMNH171353

Tanzania Mahale FMNH177888

kerbispeterhansi

99/1.0

sp. nov. 3 (Mbizi Hylomyscus

from Tanzania)

sp. nov. 4 (Mahale

Tanzania Mahale FMNH177890 Hylomyscus from Tanzania)

Malawi Misuku FMNH196311 KF876469

Malawi Misuku FMNH196753 KF876468

Malawi Nyika FMNH211576 KF876476

Malawi Nyika FMNH211577 KF876477

Tanzania Usumbara FMNH147476 KF810191

Tanzania Usumbara FMNH150118 KF810192

Tanzania Usumbara FMNH150143 KF810193

DRC Tshuapa FMNH219611

DRC Tshuapa FMNH219612

DRC Tshuapa FMNH219613

DRC Tshuapa FMNH222524

DRC Tshuapa FMNH219689

Zambia RS1113 JX126613

Zambia RS1606 JX126616

Zambia RS1114 JX126614

Zambia RS1115 JX126615

r Zambia RS811 JX126618

Zambia RS818 JX126619

Zambia RS803 JX126621

Zambia RS810 JX126617

Zambia RS793 JX126620

Angola ANG0210

100/1.0 } Angola ANGO215

Angola ANGO0237

Angola ANGO259

DRC Tshuapa FMNH219684

pamfi Benin JQ735527

simus |vory Coast JQ735557

alleni Gabon AF518328

stella Uganda FMNH160511

walterverheyeni CAR JQ735614

arcimontensis

dnoi6 jasue

sp. nov. 2 (small

Hylomyscus from DRC)

seri anselli

heinrichorum

sp. nov. 1 (pygmy

Hylomyscus from DRC)

alleni group

parvus group

baeri group

} ——_____________» aeta group

|________» denniae group

Fig 4. Phylogenetic tree, using cytochrome-d, of the genus Hylomyscus with focus on the Hylomyscus anselli group. Bootstrap

values for maximum likelihood analysis followed by posterior probabilities for Bayesian analysis are indicated above branches.

Diagnosis. Easily recognized by its small size: HB 56,

Wt 5.8, CI 15.9, CLM 2.6, WM1 0.8. All are signifi-

cantly smaller than any other members of the H. ansel-

li group (Figs 5a, c, 6a, c, e; Tables 4-5), or, for that

matter, any member of Hylomyscus. Ears exceptionally

long (Fig. 5c), 23% of HB. Incisors slightly pro-odont

(Fig. 6e). Braincase inflated, round and bulbous (Figs 6a,

e). Rostrum extremely short (Fig. 6a, LN/ONL = 26.7%).

Comparisons. This species is by far the smallest mem-

ber of the Hylomyscus anselli group as reflected in Ta-

bles 4—5: e.g., crown length of upper molars 2.6, com-

pared to 3.0-4.5; HB 56, compared to 76—109 for other

members of the group.

Bonn zoological Bulletin 69 (1): 55—83

Description. Size very small (HB 56, mass 5.8). Tail

36% longer than HB. Tail unicolor with 21—23 annula-

tions per cm. Ears long, 23% of HB, 13 mm re-measured

from dry study skin (vis a vis field notes = 12 mm). Bel-

ly hairs 3 mm, basal 50% slate grey, distal 50% slightly

ochraceous. Dorsal hairs 4 mm, basal 2.5 mm slate grey,

tipped with carmel brown. Dorsum of head appearing

more grey, due to shorter ochraceous tips (perhaps in

molt). Upper lip creamy white. Vibrissae ‘long’ — up to

25 mm in length —, ventral vibrissae white; dorsal vibris-

sae black and shorter. Young adult female with mammae

not visible on dry skin. The number of fleshy pads on the

hind foot are not determinable from the single study skin.

The number of fleshy palatal ridges are not visible in the

single cleaned skull.

©ZFMK

Four new Hylomyscus (Muridae) from Africa 63

Table 4. Craniodental measurements in millimeters (mean + 1 SD and range) for eight species in the Hy/omyscus anselli group.

Abbreviated variables are defined in the text.

Variable kerbispeterhansi stanleyi mpungamachagorum arcimontensis thornesmithae anselli heinrichorum pygmaeus

(n=51) (n= 22) (n= 4) (n= 53) (n=5) (n = 4) (n= 13) (n= 1)

ONL 26.36 + 0.75 27.16 + 0.56 25.25 + 0.08 23,09 0,695 2284-20-61" 25,0825 030" “2673S 0779 17.45

(24.68-27.96) (26.20—28.48) (25.17—25.36) (24.12-27.25) (22.09-23.39) (25.74-26.39) (25.52—28.12)

Cl 24.73 + 0.87 24.84 + 0.56 23.34 40.31 23.80+£0.70 21424047 23.9840.57 24.77+40.75 15.89

(22.66-26.53) (23.60—26.42) (22.95—23.70) (22.43—-25.61) (21.06-22.08) (23.28-24.68) (23.68-26.18)

ZB 13.19+0.42 B50 25 12 65202 12.85+045 11664010 12.84+40.22 12.99+0.38 9.68

(12.25-14.19) (12.86—13.95) (12.48-12.73) (11.91-13.89) (11.55-11.80) (12.53-13.05) (12.52—-13.70)

BBC 11.81 0.27 12.14+0.24 11.65 + 0.16 11.6640.34 11.07+049 11804039 11.81+0.22 O27

(11.25-12.51) (11.62-12.48) (11.51-11.83) (10.90-12.47) (10.64-11.62) (11.24-12.12) (11.55-12.29)

BOC 6.10+0.18 OAL O 12 SE Ou OnlZ 022 562-2017 6.18£0.18 6.26: 2042 4.94

(5.58-6.45) (5.93-6.32) (5.78-6.05) (5.55-6.54) — (5.42-5.81) (6.00-6.40) (6.06—6.43)

IO 4.35+0.10 460+ 0.12 4.52+0.21 4.36+0.15 3.89 + 0.08 4.41+0.16 4.53 + 0.08 3.74

(4.17-4.57) (4.46-4.91) (4.34-4.80) (4.09-4.66) (3.77-3.99) (4.20-4.57) (4.42-4.69)

LN 9.45 + 0.46 10.14 + 0.33 8.71 + 0.07 9192035 7,69 +£0.31 GAS 2027 9.16 + 0.49 4.66

(8.44-10.69) (9.26-10.61) (8.64-8.81) (8.44-9.76) = (7.32-7.97) (8.81—9.38) (8.06—9.94)

BR 4.56 + 0.27 4.55+0.14 4.43+0.11 4.45 + 0.20 4.11+0.20 4.59 + 0.07 4.35 + 0.24 3.23.

(4.16—5.60) (4.27-4.97) (4.27-4.50) (4.08-4.96) — (3.94-4.42) (4.48-4.63) (4.01-4.73)

BPE 9.03 + 0.44 9.36 + 0.27 8.98 + 0.24 8.96 + 0.31 8.62 + 0.33 9.11+0.24 9.40 + 0.44 6.28

(8.12-10.32) (8.75—10.05) (8.69-9.28) (8.37-9.63) (8.23-8.94) (8.87-9.45) — (8.58-10.20)

LBP 4.50+0.18 4.76+0.18 4.26 + 0.06 4.42+0.21 4.18+40.14 4.79 +£0.17 4.45 + 0.20 201

(3.92-4.81) (4.36—5.09) (4.19-4.34) (3.95-4.83) (4.00-4.37) (4.60-4.93) (4.08-4.77)

LIF S09 2025 5.48 + 0.16 5.09 £0,19 S38 O30 4.38 + 0.22 523022 5.84 + 0.27 2.83

(5.02-6.06) (5.29-5.78) (4.89-5.34) (4.78-6.11) (4.10-4.67) (5.09-5.55) (5.33-6.33)

LD L&LE O32 759 +£0.17 6.95 £0.19 FIDO 25 6.55: 4+:0.29 TAGEOAD 7.47 + 0.35 4.39

(7.25-8.62) (7.38-8.03) (6.74-7.20) (6.76-7.83) (6.14-6.82) (7.03-7.41) (7.05—8.15)

BZP DSO EA 2 2.28 £0.13 2.30 + 0.05 2 se Wale 1.90 + 0.09 2.34+0.14 2.64 + 0.17 1.76

(2.16—2.75) (2.07-2.57) (2.24-2.36) (2.01-2.54) (1.79-2.00) (2.17-2.47) (2.31—2.80)

LAB 4.59+0.21 4.51+40.12 4.23 +0.13 4.23 +0.12 3.86 + 0.14 4.55 +0.07 4.45+0.11 3:23

(4.26—5.23) (4.28-4.74) (4.04-4.34) (3.98-4.43) — (3.73-4.05) (4.48-4.63) (4.23-4.61)

CLM 3.80 + 0.07 4.1340.12 3.78 + 0.05 3.85 +0.18 3.16 + 0.09 4.10+0.09 417+40.14 2.60

(3.66-3.93) (3.97-4.51) (3.74-3.85) (3.40-4.17) — (3.02-3.25) (3.97-4.18) (3.99-4.52)

WMI! 1.20 + 0.04 1.24 + 0.04 1.13+0.01 1.18 40.05 0.95 + 0.09 1.24 + 0.04 1.28 + 0.06 0.82

(1.12-1.29) (1.14-1.30) (1.12-1.13) (1.06-1.28) (0.86—1.06) (1.19-1.28) (1.17-1.34)

Skull tiny (ONL 17.45, CRM 2.6). Rostrum excep-

tionally short (LN/ONL = 26.7%) but this is expected to

increase in older individuals. Inter-orbital region propor-

tionately broad. Upper incisors slightly pro-odont. Inci-

sive foramina fall short of upper tooth row. T3 on M?

is present but a tiny vestige. Braincase bulbous and dor-

so-ventrally inflated. Hamular process of the squamosal

long and thin, providing for a very large subsquamosal fe-

nestra which is about 40% the size of the postglenoid fo-

ramen (see Carleton & Stanley 2005: fig. 6). Maxillo-pal-

atal suture located at the rear third of the M! (Figs 6c, 8a).

Post palatal foramina large, starting between M! and M?

and extend back to middle of M? (Figs 6c, 8a). Fronto-pa-

rietal suture broadly U-shaped. Zygomatic plate narrow

(1.34 mm) and without any sinuosity but gently sloping

Bonn zoological Bulletin 69 (1): 55—83

forward throughout. Mesopterygoid fossa rounded and

open widely at rostral end.

As a divergent member of the Hy/lomyscus anselli

group, some of the following characters contrast the Car-

leton et al. list of characters (2006: table 7) defining this

group: 1) pectoral mammae unknown (not available as

the holotype is a young adult), 2) upper incisors slightly

pro-odont (Fig. 6e), whereas Carleton et al. (2006) char-

acterized the H. anse/li group as opisthodont, 3) T3 on

M! is distinct and sub equal with tl rendering it ‘large’

per Carleton et al. (2006); the anterior chevron is more or

less symmetrical (Fig. 7g), whereas Carleton et al. (2006)

characterized the ‘H. anselli group as having a ‘medium’

sized t3 (e.g., smaller than tl), 4) t9 on M! is distinct

(Fig. 7g),whereas Carleton et al. (2006) characterized the

©ZFMK

Julian C. Kerbis Peterhans et al.

Table 5. External measurements (mean + SD, range, and sample size) of all eight members of the Hy/omyscus anselli group.

Measurements are in millimeters and mass is in grams. Abbreviated variables are defined in the text. *See text, totals have 1.0 mm

added.

Variable kerbispeterhansi — stanleyi —§ mpungamachagorum arcimontensis thornesmithae anselli heinrichorum pygmaeus

TOT 2302 12 NSS Ona al 234.3 + 6.6 DALE Bie vette (Us| 204.447.6 22244134 233.3412. sz

(201-260) (233-264) (230-244) (205-262) (193-212) (205-254) (207-255)

50 32 + 50 5 16 21 1

HB 92.6+5.6 101.74+3.8 97.8+1.9 91.3+5.6 83.2444 87.2 +64 94.8468 56

(80-103) (93-109) (95-99) (77-104) (76-87) (78-101) (82-106)

50 32 ut 50 5 16 21 1

TAIL 137.6+8.8 14515 2541 138.3463 136.0 + 9.0 Niles 353 135.2492 13852474 76

(117-158) (136-159) (132-147) (115-161) (117-125) (121-153) (121-150)

50 32) - 50 5 16 21 1

HF 20.4+0.9 DTI OFS 2073 205 DOr, 18.0+1.0 20.7% BOS 22:0" 09 14

(19-22) (20-23) (20-21) (18-22) (17-19) (19.5-21.5)* = (19.5-23)*

49 3D - 50 5 24 21 1

EAR 19.8+1.0 199+0.8 19.0 0.0 18.2+1.0 148+0.8 18.0+0.7 18.6+ 1.0 1

(17.5-22) (18-21) (19) (17-21) (14-16) (16.5-19) (17-21)

AT Eo) 4 50 5 24 21 1

Wt 24.9+4.0 27:63 ,.1 21.841.2 220i 397 13.9+1.4 20.4+ 4.0 NA 5.8

(17-39) (22-34.5) (20.5—23) (15-29.5) (11.5-15) (16-30.5)

48 3 + 50 5 15 1

TAIL/HB see Oel 1440.0 14+0.1 es 0 uh 1.4+0.1 LOrE-0. I Nese 296) 1.4

(1.2-1.7) (1.4-1.5) (1.3-1.5) (1.2-1.7) (1.4-1.5) (1.4-1.8) (1.3-1.7)

50 Sy - 50 5 16 21 1

‘H. anselli’ group as ‘indistinct’ 5) interorbital constric-

tion is amphoral, whereas Carleton et al. (2006) charac-

terized the ‘H. anselli’ group as having a ‘weak shelf,

6) rostral length is extremely short (Fig. 6a), whereas

Carleton et al. (2006) characterized the ‘H. ansell?’ group

with a ‘medium’ length rostrum, 7) incisive foramen is

short, falling well short of the alveoli of M' (Figs 6c, 8a)

as opposed to the Carleton et al. (2006) characterization

as ‘medium’ (reaching anterior root of M'), 8) the hamu-

lar strap is long and thin, subsquamosal foramen is large

in size (see Carleton & Stanley 2005: fig. 6; Fig. 6e). In

sum, several characters of this new species are unique

or align more with the Hy/omyscus alleni group than

the H. anselli group: more proodont, distinct T9 on M!,

amphoral inter-orbital region, extreme shortening of the

rostrum, and shorter incisive foramina. Perhaps these

contrasts are not surprising given the basal position of

this taxon.

Ecology. The habitat is seasonally flooded primary for-

est, ‘edaphic forest’ (Verhegghen et al. 2012). However,

the pitfall line was set in a drier part of the forest and

was less subject to flooding. The area supports two dry

seasons (January to early March, and June to early Sep-

tember) with the rest being rainy averaging ca. 210 cm

per year. Daily temperature average between 24 °C and

30°C (Doty et al. 2017). Type specimen was caught in a

generally dry area of the forest.

The vegetation of the Tshuapa region is mainly char-

acterized by sempervirent or semi-sempervirent rain

forests bound to hydromorphic soils, secondary forests

Bonn zoological Bulletin 69 (1): 55—83

and grassy vegetation (Evrard 1968). The sempervirent

rain forests of terra-firma are distinguished by their struc-

tural density, distinct stratification and epiphytism (Leb-

run & Gilbert 1954), while the upper stratum can reach

40-45 m in height. There are two types of forest bound to

hydromorphic soils in swampy zones. These include pe-

riodically flooded forests (including where the type spec-

imen was collected) comprising the following species:

Parinari congolensis, Guibourtia demeusei, Zeyrrhella

longipedisellata and swampy forests composed of En-

tandrophragma palustre, Alstonia congolensis, Coelo-

caryon botryodes, and Sterculia tragacantha. The second

forest type is composed of bushy forests along the banks

of large rivers including Alchornea cardifolia, Lacosper-

ma secundiflorum, waterside forests with Coelocaryon

botryodes, Erispermum microspermum, Sclerosperma

manirii, and Cleistanthus mycrophyllus. Secondary for-

ests are found around villages, roads and on former sites

of forest extraction. Species frequently observed are

Musanga cecropioides, Harungana madagascariensis,

Trema_ orientalis, Oncoba subtomentosa, Pycnanthus

angolensis, Petersianthus macrocarpus, Ricinodendron

heudelotii, Canarium schweinfurthii, Alstonia boonei,

and Elaeis guineensis. Grassy vegetation results from

forest degradation and includes frequently burnt fallow

fields, mainly with Graminaceae of the genera Panicum,

Pennisetum, Imperata, Serata, and Sorghum (Evrard

1968).

Reproduction. The sole specimen is a young female

with teats that are neither developed nor visible.

©ZFMK

Four new Hylomyscus (Muridae) from Africa 65

LBS

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27 DRS

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Zlaz Auac F]

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une

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Fig. 5. Skins of two new species of the Hylomyscus anselli group from the Democratic Republic of Congo. (a) ventral and (c) dorsal

views of Hylomyscus pygmaeus sp.nov., and (b) ventral and (d) dorsal views of Hylomyscus thornesmithae sp.nov.

Etymology. Named for its diminutive size. We recom-

mend “pygmy wood mouse” as an English common

name.

Hylomyscus thornesmithae sp. nov. Kerbis Peterhans,

Hutterer & Demos

urn:lsid:zoobank.org: act: DAE95 BEF-D424-42C2-8415-A1805F 494ADC

Hylomyscus sp. — Doty et al. (2017)

Holotype. Field Museum of Natural History, Division

of Mammals number FMNH 222524 (field number WT

Stanley 11,664; CDC 746), collected by W.T. Stanley, 27

June 2013 (originally listed as Hylomyscus sp.). The type

specimen, consisting of an alcoholic carcass with skull

removed, is an adult female with first upper molar in ear-

Bonn zoological Bulletin 69 (1): 55-83

ly wear (advanced age stage IV) and large teats (2+4).

The basisphenoid-occipital suture is fused. External mea-

surements were made in the field: TL 210, TV 124, HF

18, EL 15, Wt 15. Specimen caught in a standard snap

trap; apparently held by tail in trap as tail is broken

way down. Type specimen captured just behind camp in

secondary growth forest on the edge of a forest that may

occasionally be subject to flooding.

Type locality. Democratic Republic of Congo, Tshuapa

Province, rt side Tshuapa River, 14 km north of Boende

by road, Quatorz (0.16919° S, 20.92611° E) at an eleva-

tion of 322 m.

©ZFMK

66 Julian C. Kerbis Peterhans et al.

Fig. 6. Skulls of two new species of the Hylomyscus anselli group from the Democratic Republic of Congo. (a) Dorsal (c) ventral

and (e) lateral views of Hylomyscus pygmaeus sp.nov. (b) Dorsal, (d) ventral and (f) lateral views of Hylomyscus thornesmithae

Sp. nov.

Paratypes (n = 4). All caught in conventional trap lines

from Democratic Republic of Congo, Tshuapa Province,

4 km N of Boende, Baleko (0.24127° S, 20.8833° E)

at an elevation of 358 m: FMNH 219611 (WTS 11471,

CDC 103), alcoholic carcass with extracted skull, old

scrotal male; FMNH 219612 (WTS 11592, CDC 224)

alcoholic carcass with extracted skull, old female, teats

2+4; FMNH 2119613 (WTS 11594, CDC 226), alcohol-

ic carcass with extracted skull, old scrotal male; FMNH

219689 (WTS 11481, CDC 113), skin and skull with car-

cass preserved in alcohol, old scrotal male, testes 10x5.

Diagnosis. Easily differentiated within the Hy/omyscus

anselli group by its small size (second smallest, but still

much larger than preceding species): HB 83 (mean), Wt

13.9 (mean), ONL 22.8 (mean), CLM 3.2 (mean). All

are significantly smaller than all other members of the

H. anselli group (Tables 4-5), excepting the previously

described species.

Bonn zoological Bulletin 69 (1): 55—83

Comparisons. Upper incisors orthodont, contrasting

with the proodont condition in Hylomyscus pygmaeus.

Crown length of upper molars 3.0—3.25 mm, much larg-

er than Hylomyscus pygmaeus (under 2.6 mm). External

and cranio-dental measurements smaller than all other

members of the H. anse/li group (excepting Hylomyscus

pygmaeus).

Description. Size very small (mean HB = 83, mean mass

= 13.9). Tail 46% longer than HB, unicolor with ca. 18

annulations per cm. Ears of normal size, 18% of HB; ear

color dark grey. Belly hairs 5 mm, basal 3 mm slate grey,

distal 2 mm white. Dorsal hairs 7 mm, basal 5 mm slate

grey, apical 2 mm orange, more bright orange towards

flanks. Vibrissae up to 33 mm in length, mostly black

but with 2—3 white hairs; upper lip with white fur patch

behind vibrissae. Teats 2+4. The hind foot possesses the

standard murine complement of 6 pads (see Ibe et al.

2014: fig. 2, Il for reference); there is a single accessory

pad on the 1“ and 4" interdigital pads; the first is clear

and well-defined while the 4" is larger and more integrat-

©ZFMK

Four new Hylomyscus (Muridae) from Africa 67

3%)

Fig. 7. Sketches of right upper (top row) and lower tooth rows (bottom row) of members of the Hylomyscus anselli group, including

four new species described herein: (a) H. stanleyi sp. nov. (FMNH 171512), (b) H. anselli (BMNH 74.250), (c) H. kerbispeterhansi

(FMNH 209995), (d) H. mpungamachagorum sp. nov. (FMNH 177889), (e) H. arcimontensis (FMNH 147271), (f) H. thorne-

smithae sp. nov. (FMNH 222524), (g) H. pygmaeus sp. nov. (FMNH 219684). Scale = 1 mm.

Fig. 8. Sketches of the bony palates of Hy/omyscus anselli and the four new species of the Hy/omyscus anselli group: (a) H. pyg-

maeus sp. nov. FMNH 219684, (b) H. thornesmithae sp. nov. FMNH 222524, (c) H. mpungamachagorum sp. nov. FMNH 177889,

(d) H. stanleyi sp. nov. FMNH 171362, and (e) H. anse/li BMNH 74.250. Scale = 5 mm.

Bonn zoological Bulletin 69 (1): 55—83 ©ZFMK

68 Julian C. Kerbis Peterhans et al.

10 mm

A B

FMNH 222524

H. thornesmithae

FMNH 193233

H. mpungamachagorum

Cc D

FMNH 171516 RS 1113

H. stanleyi H. anselli

Fig. 9. Sketches of feet and plantar tubercles of four species of the Hylomyscus anselli group: (a) H. thornesmithae sp. nov., (b)

H. mpungamachagorum sp. nov., (c) H. stanleyi sp. nov., and (d) H. anselli.

ed (Fig. 9a). The number of fleshy palatal ridges are not

visible on any of the prepared skulls.

Skull small (mean ONL = 22.8, mean CRM = 3.2).

Rostrum short, LN/ONL = 33.7%. Upper incisors ortho-

dont. Incisive foramina fall well short of upper tooth row.

T3 on M? is tiny. Braincase elongated. Hamular process

of the squamosal long and thin, providing for a large

subsquamosal fenestra which is about 35% the size of

the post glenoid foramen (see Carleton & Stanley 2005:

fig 6; Fig 6f). Maxillo-palatal suture zig-zags through

the middle of the M! (Figs 6d, 8b). Post palatal foramina

large, starting at rear 3 of M! or between M! and M? and

continues through to the 1* third of M?. Zygomatic plate

Slightly sinuous. In aged individuals (FMNH 219611,

FMNH 219612), the incisive foramina fall even shorter

of the UTR, the maxillo-palatal suture is located more

forward at the first half of M! and the post palatal foram-

ina are more forward at the rear half of the M!. Frontopa-

rietal suture broadly rounded, U-shaped. Zygomatic plate

narrow (1.9 mm) and virtually orthogonal to skull profile

but gently sloping forward in lower third. Mesopterygoid

fossa rounded at rostral end.

Bonn zoological Bulletin 69 (1): 55—83

As a member of the Hylomyscus anselli group (sensu

Carleton et al. 2006: table 7), the following characters

are relevant: 1) mammae: 2+4, 2) upper incisors ortho-

dont (Fig. 6f), 3) T3 on M! is ‘medium’ in size (smaller

than t1), the anterior chevron is moderately asymmetrical

(Fig. 7f), 4) T9 on M! is distinct but reduced (Fig. 7f), 5)

interorbital constriction is amphoral in shape (Fig. 6b).

6) rostral length is short, LN/ONL = 33.7% (Fig. 6b), 7)

incisive foramen is very short, falling short of the roots

of M1 (Figs 6d, 8b), 8) the hamular strap is short but

thin and delicate and allows for a large subsquamosal fo-

ramen, which is about 25% the size of the postglenoid

foramen (Fig. 6f).

Distribution. Known only from two locations, both are

ca. 250 km S of the Congo River, off the right bank of

the Tshuapa River, Tshuapa Province, Democratic Re-

public of Congo. In addition to the type locality (n = 1),

four paratypes are from 4 km N of Boende at Baleko

(0.24127° S, 20.8833° E, elevation 358 m).

Ecology. Type specimen and 3 paratypes all caught in

standard mammal snap traps while the fifth was caught

©ZFMK

Four new Hylomyscus (Muridae) from Africa 69

Fig. 10. Live photos of two new species of the Hylomyscus anselli group from Tanzania: (left) H. stanleyi sp. nov. and (right)

H. mpungamachagorum sp. nov.

in a Sherman live trap. Type specimen captured in re-

generating secondary forest on the edge of a seasonally

flooded forest. One specimen captured in a trap line that

was never flooded during heavy rain events while three

came from a trap line that was prone to flooding.

Reproduction. All animals captured (n = 5) were adult.

Type is adult female with swollen teats 2 + 4. A second

female (FMNH 219612), despite having well-worn mo-

lars (beyond stage VII), had small teats that are difficult

to decipher. Three adult males all with scrotal testes; tes-

tes of FMNH 219689 measured 10 x 5 in the field.

Etymology. Ellen Thorne Smith was a “professional vol-

unteer” serving 2—3 days per week, sorting and organiz-

ing the bird collections at the Field Museum, and con-

ducting original published research from the mid 1930’s

until the 1970’s. During World War II with the museum’s

ornithologists away in Washington, she ran the Division

of Ornithology. We recommend “Mother Ellen’s wood

mouse” as an English common name.

Hylomyscus stanleyi sp. nov. Kerbis Peterhans, Hutter-

er & Demos

urn: lsid:zoobank. org: act: 45 12E5DE-2139-46CB-B2F9-823C9C3B1IBAD

Hylomyscus anselli — Carleton & Stanley (2005); Car-

leton, Kerbis Peterhans & Stanley (2006); Demos, Ag-

wanda & Hickerson (2014a); Carleton, Banasiak & Stan-

ley (2015)

Hylomyscus cf. anselli — Nicolas et al. (2020)

Holotype. Field Museum of Natural History, Division

of Mammals number FMNH 171362 (field number WT

Stanley 4968), collected by Cosmos, 03 August 2001

Bonn zoological Bulletin 69 (1): 55—83

(originally listed as Hylomyscus sp.). The specimen, con-

sisting of a skin, skull and alcoholic carcass, is an adult

pregnant female with first upper molar well worn (stage

IV of Verheyen & Bracke 1966). Teats 2+4, large, embry-

os 4L, 1R (CR 14). The holotype was captured in a local

snare baited with corn. The basisphenoid-occipital suture

is fused. External measurements were made in the field:

TL 256, HB 106, TV 154, HF 21, EL 20, Wt 29.

Type Locality. Tanzania, Rukwa Region, Sumbawanga

District, Mbizi Forest Reserve, 0.5 km N, 4 km E of W1-

panga, elevation 2200 m, 7.8639° S, 31.6694° E.

Paratypes (n = 32). Mbizi Forest Reserve, 0.5 km N,

4 km E of Wipanga, elevation 2200 m, 171357-171361,

171363=) AS67751 171518866, 6-1).«/ 863925.

31.6694° E; Mbizi Forest Reserve, 0.5 km S, 3 km E of

Wipanga, 2300 m, 171342-171356, 171512—-171516

(12 m, 8 f), 7.8639° S, 31.6694° E.

Diagnosis. UTR >3.97 mm, maxillo-palatal suture locat-

ed at the rear third to the rear half of M! (Fig. 8d), rostrum

elongate (LN/ONL= 37.33, LN>9.3; Fig. 12b, Table 4),

very large posterior palatal foramen (ca. 0.7-0.9 mm)

starting between M! and M? and extending into anterior

half of M? (Figs 8d, 12d), very large sub-squamosal fo-

ramen (30-40% area of postglenoid foramen, Fig. 12f),

fronto-parietal suture shallow V-shaped, zygomatic plate

only slightly sinuous in lateral view, incisive foramina

fall either just short of the alveoli of M' or barely reach-

ing alveoli of M! (Figs 8d, 12d). Tl of M1 deflected far

posteriorly (Fig. 7a).

©ZFMK

70 Julian C. Kerbis Peterhans et al.

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Fig. 11. Skins of two new species of the Hy/omyscus anselli group from Tanzania. (a) Ventral and (c) dorsal views of Hylomyscus

mpungamachagorum sp. nov., (b) Ventral and (d) dorsal views of Hylomyscus stanleyi sp. nov.

Comparisons. One of the largest members of the H.

anselli group with an upper molar crown length over 4.0,

thereby needing comparison with only Hylomyscus hein-

richorum and H. anselli. Compared to H. heinrichorum,

H. stanleyi is typically orthodont vs. slightly opisthodont,

see Carleton et al. 2015: fig. 7c (as H. stanleyi) vs. fig.

7b, has longer nasals (mean of 10.1 vs. 9.2; Ibid. 6c as

H. anselli vs. 6b) with a more narrow zygomatic plate

(Ibid. fig. 6c as H. anselli vs. fig. 6b, mean of 2.3 vs.

2.6) and with incisive foramina that do not penetrate the

upper tooth row or alveoli (Ibid. fig. 6c as H. anselli vs.

6b). Since the sample size of available H. ansel/li is small

(n = 4), we expect these differences may become more

Bonn zoological Bulletin 69 (1): 55—83

ambiguous as older individuals and additional samples

of H. anselli become available.

Description. Size large (mean HB = 102, mean mass

= 27.5 g; Table 5). Tail 43% longer than HB. Tail uni-

color with ca. 15 annulations per cm. Belly hairs ca.

9 mm, basal 6 mm slate grey, apical 3 mm white. Dorsal

hairs ca. 11 mm, basal 6 mm slate grey, terminal 3 mm

tipped with light brown. Dorsum of head same color as

dorsum of body. Upper lip with whitish hairs but with

grey roots. Ears with blackish skin, hairs barely visible.

Vibrissae long, up to 35 mm, black in color. Pes dirty

white in appearance due to white hairs overlaying darker

skin. Manus white. The hind foot possesses the standard

©ZFMK

Four new Hylomyscus (Muridae) from Africa 71

Fig. 12. Skulls of two new species of the Hy/omyscus anselli group from Tanzania. (a) Dorsal, (c) ventral and (e) lateral views of

Hylomyscus mpungamachagorum sp. nov., (b) Dorsal, (d) ventral and (f) lateral views of Hylomyscus stanleyi sp. nov.

murine complement of 6 pads (see Ibe et al. 2014: fig. 2.

II for reference); there 1s a single accessory pad on each

of the 1‘, 2nd and 4" interdigital pads; the first is larger

and well-integrated into the 1* interdigital pad, the 2" 1s

small but distinct from the 2" interdigital pad, while the

4" is smaller but distinctly separate from the 4" interdig-

ital pad (Fig. 9c). There are seven fleshy palatal ridges:

two are continuous and pre-dental, one is discontinuous

and pre-dental, and the last four are discontinuous and

inter-dental (Fig. 13).

Skull large (mean ONL = 27.2, mean CLM = 4.1, Ta-

ble 4). Rostrum much longer than other members of the

‘H. ansell’ group (LN/ONL = 37.3%), with nasals ex-

ceeding 9.3 mm (Table 4). Upper incisors generally or-

thodont, but a few slightly opisthodont. Incisive foramina

fall short of upper tooth row crown but may reach alveoli.

T3 on M? is large. Braincase elongate rather than rounded

or globular. Hamular process of the squamosal thin, al-

lowing for a large subsquamosal fenestra (ca. 30% of post

glenoid foramen). Maxillo-palatal suture at third lamina

of the M'. Post palatal foramina large (0.7—0.9 mm), be-

ginning between M! and M? and continuing through the

1* third or half of the M?. Frontoparietal suture V-shaped.

Bonn zoological Bulletin 69 (1): 55—83

Zygomatic plate narrow (mean breadth = 2.3 mm) and

orthogonal to the long axis of the skull. Mesopterygoid

fossa more rectangular at rostral end.

As a member of the Hylomyscus anselli group, the

following characters are relevant: 1) mammary formu-

la 2+4, 2) upper incisors orthodont with some individ-

uals (5 of 33) slightly opisthodont, 3) T3 on M! is large

and is more or less equal in size to T1, but T1 is deflect-

ed further posteriorly (Fig. 7a), 4) T9 on M! is distinct

(Fig. 7a), 5) interorbital constriction has a weak shelf, 6)

rostral length is long, LN/ONL = 37.3%, 7) incisive fora-

men is short, falling just short of the M' or barely meet-

ing the beginning of the alveolus, 8) the hamular strap is

thin allowing for well-developed subsquamosal foramen

but which is proportionately smaller than in the two new

DRC species (Figs 6e-f vs. Figs 12e—f).

Habitat. Mbizi is the largest area of montane cloud forest

(ca. 2,000 ha) remaining on the denuded Ufipa Plateau.

All of the extant forest is contained within the Mbizi For-

est Reserve and is discontinuous with forest patches in-

terspersed with grasslands. There is very little continuous

canopy cover due to removal of commercially valuable

©ZFMK

72 Julian C. Kerbis Peterhans et al.

Fig. 13. Sketch of soft palate of Hylomyscus anselli from Zam-

bia displaying the 2+(1+4) dental ridges format typical of the

Hylomyscus anselli group: from tip of rostrum (to the left): 2

continuous pre-dental ridges, 1 discontinuous pre-dental ridge,

4 discontinuous inter-dental ridges.

timber species and exploitation for firewood and charcoal

(Rodgers et al. 1984). The forest is on the eastern facing

escarpment overlooking the Rukwa Trough. Surveys of

the vegetation at Mbizi include those by Mtuy & Mkude

(1974), Rodgers et al. (1984), and Rufo & Mabula (1987).

The forest canopy reaches 25 m in places with dominant

tree species being Aguarista salicifolia, Allophyllus ab-

yssinicus, Croton megalocarpus, Macaranga capensis,

Neoboutonia macrocalyx, Olea chrysophylla, Olinia

rochetiana, and Prunus africana (Rodgers et al. 1984).

The understory is between 8—20 m with the most com-

monly encountered tree species being: Bersama abyssi-

nica, Cathula edulis, Clerodendron sthulmanii, Bridelia

brideliifolia, Polyscias fulva, and Rhus natalensis (Rod-

gers et al. 1984, Rufo & Mabula 1987). The most striking

aspect of Mbizi forest is scattered Euphorbia amplophyl-

la that emerge above the canopy up to 35 m (Rodgers

et al. 1984). Forest cover has been fragmented by past

fires and smaller patches are now isolated on the periph-

ery and in sheltered valleys. These are surrounded by

species-rich grasslands maintained by nearly annual fires

(Rufo & Mabula 1987). The central forest block is more

or less continuous and covers an area of over 2000 ha.

However, much of this is disturbed as the reserve is sur-

rounded by villages and heavily exploited for firewood

and charcoal. The area has many endemic plants (e.g.,

Brillantaisia richardsiae, Glossostelma mbisiense, Pach-

ycarpus pachyglossus, Spermacoce azurea, Sebaea per-

pava, Afrotysonia pilosicaulis) and several undescribed

plant species including a possible new species of Ocotea

(Q Luke, pers. comm. ).

Bonn zoological Bulletin 69 (1): 55—83

Reproduction. Of the 33 examples of the new species

collected (July—Aug 2001), there were 18 males and 15

females. All can be considered adult (3 molars in ad-

vanced wear). Of the 15 females, 14 were inspected inter-

nally: 7 were pregnant, 7 were not. All pregnant females

had either 4 or 5 embryos with an average crown rump

length of 12-13 mm. The pregnant females averaged 28

g in weight while those that were not pregnant weighed

an average of 25 g. All males were adult with scrotal tes-

tes. The entire population had well-worn molars, at least

in advanced wear stage IV (Verheyen & Bracke 1966).

Distribution. Known only from two montane forest lo-

calities within Mbizi Forest, SW Tanzania: the type lo-

cality at % km S and 3 km E Wipanga, 2300 m (31.6667°

E, 7.875° S) and a second locality % km N, 4 km E Wi-

panga, 2200 m (31.6694° E, 7.8639° S).

Etymology. Named for William T. Stanley (1957-2015)

who directed the collection of all known specimens (n =

33) of this species from the Mbizi Mountains of Tanzania

in 2001 as well as the type specimen of the other three

species described in this manuscript (and many more).

We recommend “Stanley’s wood mouse” as an English

common name.

Hylomyscus mpungamachagorum sp. nov. Demos,

Hutterer & Kerbis Peterhans

urn: |sid:zoobank.org:act:283 1A D81-BSBF-41FC-82D3-35F 2069CO016A

Holotype. Field Museum of Natural History, Division

of Mammals, FMNH 177889 (field number WT Stanley

5988), collected by WT Stanley, 25 Aug 2003 (originally

listed as Hylomyscus sp.). The specimen, consisting of a

study skin and skull with postcranial skeleton, is an adult

scrotal male (testes 13 x 8 mm) with worn first upper mo-

lar (stage IV of Verheyen & Bracke 1966). The basisphe-

noid-occipital suture is fused. External measurements

were made in the field: TL 244, HB 99, TV 147, HF 20,

EL 19, Wt 20.5. The holotype was collected in a standard

snap trap (Museum Special).

Type locality. Tanzania, Kigoma Region, Kigoma Dis-

trict, Mahale Mountains, Mahale National Park 2100 m,

0.5 km NW Nkungwe Hill summit (29.77895° E,

6.10433° S).

Paratypes (n= 11). Tanzania, Mahale National Park, Ma-

hale Mountains, Mahale National Park 2100 m, 0.5 km

NW Nkungwe Hill summit (29.77895° E, 6.10433° S)

178011, 177888, 177890-177892, 177911; Kabezi Riv-

er, 1180 m, 193233 (29.8317° E, 6.1131° S); Mahale

National Park, Mfitwa Mt, 2440 m, 193234, 193218

(29.7939° E, 6.1317° S); Mahale National Park, 0.5 km

S of Pasagulu Hill, 1420 m (29.75353° E, 6.06618° S),

177886, 177887.

©ZFMK

Four new Hylomyscus (Muridae) from Africa 73

Diagnosis. A member of the H. anse//i group with a short

rostrum (nasals are 34.5% of ONL, Table 4), posterior

palatal foramen located posteriorly (at the first lamina of

M’, Figs 8c, 12c), and maxillo-palatal suture located pos-

teriorly — either between second and third lamina of M!

or at level of third lamina of M! (Figs 8c, 12c). Zygomat-

ic plate slightly sinuous in lateral view. Sub-squamosal

fenestra moderate (ca. 25-30% of postglenoid foramen;

i.e., Carleton & Stanley 2005: fig. 6; Fig. 12e). Incisive

foramina penetrate the alveoli of the upper tooth row

(Figs 8c, 12c). Frontoparietal suture shallowly U-shaped.

Comparisons. A mid-sized member of the Hylomyscus

anselli group with an upper molar crown length ca.

3.8 mm, needing comparison only with H. kerbispeter-

hansi and H. arcimontensis. It is unique among these

three in the location of its posterior palatal foramina, lo-

cated at the beginning of the second molar (Figs 8c, 12c);

in H. kerbispeterhansi it is located at the third lamina of

the M!, while in H. arcimontensis it is located between

M! and M?’. The morphometrics of H. mpungamachago-

rum align closely with H. arcimontensis; indeed, it falls

completely within its morphometric space (Figs 1-2).

Compared to H. kerbispeterhansi, the skull is smaller (CI

23.3 vs 24.7, Table 4) and with shorter nasals (LN 8.7 vs

9.45) and diastema (LD 6.95 vs. 7.82) (Table 4).

Description. Size medium (mean HB = 98, CLM 3.74—

3.85, mean mass = 22 g). Mean tail length 41% longer

than HB. Tail unicolor with ca. 15 annulations per cm.

Belly hairs 6 mm, basal 3 mm slate grey, distal 3 mm

light brown. Dorsal hairs 10 mm, basal 8 mm slate grey,

apical 2 mm light brown. Dorsum of head same color as

back. Upper lip with white hairs, dark grey roots. Vibris-

sae long, black, up to 35 mm in length. Pes dirty white

in appearance due to white hairs overlaying darker skin.

Manus white. Ears black, hairs inconspicuous. The hind

foot possesses the standard murine complement of 6 pads

(see Ibe et al. 2014: fig. 2 Il for reference); there is a

single accessory pad on each of the 1* and 4" interdig-

ital pads; the first is large and well-integrated into the

1‘ inter-digital pad, while the 4" is smaller and distinct

from the 4" interdigital pad (Fig. 9b). There are seven

fleshy palatal ridges: two are continuous and pre-dental,

One 1s discontinuous and pre-dental, and the last four are

discontinuous and inter-dental (as in Fig. 13).

Skull medium (mean ONL=25.25 mm, mean CLM =

3.8 mm). Rostrum moderate (nasals 34.5% GLS). Upper

incisors orthodont but slightly opisthodont in younger in-

dividuals. Incisive foramina just reach the M! alveoli. T3

on M? is tiny but distinct as in the other species described

here. Braincase elongated. Hamular process of the squa-

mosal long and thin, allowing for a moderate subsqua-

mosal fenestra (ca. 25% of postglenoid foramen). Maxil-

lo-palatal suture either falling between 2™ and 3 lamina

of M1 or at 3 lamina of the M1. Post palatal foramina

Bonn zoological Bulletin 69 (1): 55—83

small, lying level with 1‘ lamina of M?. Zygomatic plate

narrow (mean = 2.3 mm) and slightly sinuous. Mesopter-

ygoid fossa rounded at rostral end.

In comparison with other members of the H. anselli

group, the following characters are relevant: 1) mamma-

ry formula 2+4, 2) upper incisors orthodont but younger

individuals (wear stage III and IV, 1.e., FMNH 177890-

1778892, 193218) slightly opisthodont, 3) T3 on M'! is

large, the anterior chevron more or less equal in size to

Tl and T1 not as deflected far posteriorly as in H. stan-

leyi (Fig. 7d), 4) T9 on M! is distinct (Fig. 7d), 5) interor-

bital constriction has a weak shelf, 6) rostral length (LN/

ONL) is moderate at 34.5%, 7) incisive foramen meets

the beginning of the M! alveoli (in the four younger in-

dividuals the incisive foramina penetrate the upper tooth

row crowns), 8) the hamular strap is long and thin and the

subsquamosal foramen is well developed but proportion-

ately smaller than in the new Congolese species (H. pyg-

maeus, H. thornesmithae) described above (Figs 12e).

Unlike other species described herein, several skulls of

this taxon show anomalous patterns of the palate includ-

ing extra post palatal foramen (FMNH 177887, 177888,

193218) and interrupted incisive foramina (FMNH

177886, 177887). One specimen (FMNH 193234) also

displays a white tail tip.

Distribution. Known only from Mahale National Park,

1180-2440 m, western Tanzania.

Reproduction. Of the specimens collected, there were

7 males and 5 females. The reproductive condition of

4 females was inspected: females collected on Aug 25 &

28, 2005 had no embryos (FMNH 177888, 177890) but

the former was lactating. Two others were in the ear-

ly stages of pregnancy: FMNH 178011, collected on

25 Aug., 2003 (CR = 5 mm) and FMNH 193233, collect-

ed 9 Nov., 2005 (CR = 7 mm).

Habitat. The Mahale Peninsula is predominately cov-

ered with Brachystegia (Miombo) woodland, but higher

elevations on the Mahale Ridge are covered in montane

grasslands and forest (Itani 1990). Forest is also found

on the western and southwestern slopes from the ridge at

2400 m down to lowland forests at 780 m on the shore

of Lake Tanganyika. The montane forest vegetation is an

outlier of the Albertine Rift forests. Over 1,170 plant spe-

cies, of which 39 are Albertine Rift endemics, have been

recorded at Mahale (Nishida & Uehara 1981; Nishida

1990; Plumptre et al. 2007).

One specimen was collected in riverine forest along

the Kabezi River. This river and other smaller tributar-

ies flowing down the Mahale and Kabezi ridges are lined

with riverine forest surrounded by tall Miombo wood-

land with stands of solid-stemmed bamboo, Oxytenan-

thera abyssinica. Higher up on the Mahale Ridge, the

Miombo gives way to tall montane grassland dominated

©ZFMK

Julian C. Kerbis Peterhans et al.

_ Central African Republic

pee

ie pe

, ukuga

ade

Tanzania’ - =

Fig. 14. Map of current biogeographic units and their possible barriers in eastern Africa as relevant to the H. anselli and H. denniae

groups.

©ZFMK

Bonn zoological Bulletin 69 (1): 55-83

Four new Hylomyscus (Muridae) from Africa 7d

by Hyparrhenia spp., Themeda triandra, and Festuca

sp., with scattered Protea gauguedi, Erythrina abyssini-

ca, Cussonia arborea and isolated Parinari curatellifo-

lia. The riverine forest canopy reaches 30 m in places

and is dominated by Newtonia buchannanii, Parinari ex-

celsa, Bridelia micrantha, and Spathodea campanulata,

with occasional TZabernaemontana stapfiana, Ficus sur,

Ficus thonningii, Zanha golungensis, Prunus africana,

and Myrianthus holstii. The understory 1s dominated by

woody shrubs and Aframomum alboviolaceum (Plumptre

et al. 2003; Moyer 2006).

Two specimens originated in the Mfitwa Forest, on

the SE side of the Mfitwa Peak (6°7°54” S, 29°47°38”

S, 2440 m) which is surrounded by extensive areas of

species-rich montane grasslands. The dominant species

included Festuca sp., Themeda triandra, and Hyparrhe-

nia rufa. Mature parts of Mfitwa forest in sheltered val-

leys reach a canopy height of 30 m. Dominate species in-

clude: Polyscias fulva, Parinari curatellifolia, Agaurista

salicifolia, Croton megalobostrys, Croton sylvaticus,

Bersama abyssinica, Trichilia emetica, Ficus thonningii,

Myrianthus arboreaus, Maesa lanceolata, and Syzygium

caminnii. The diverse forest understory is dominated by

Olyra latifolia, Dracaena laxissima, Mondia whitei, Re-

nealmia engleri, Psychotria sp., dense stands of bracken

fern, Pteridium aquilinum, in light gaps and at the for-

est edge. Large areas of the forest are covered in nearly

impenetrable monodominant stands of montane bamboo,

Oldeania alpina, with very few other species penetrat-

ing this heavily shaded zone. Occasionally a forest tree

emerges through the canopy in such stands; these areas

are likely to be secondary, and at least some of them were

under cultivation in the past (Itani 1990).

Etymology. The species is named for Noah E. Mpunga

and Sophy J. Machaga, who run the Southern Highlands

Conservation Program for the Wildlife Conservation

Society. These leading conservationists have dedicated

the last 20 years to helping describe, advocate for, and

protect some of Tanzania’s most threatened and iconic

species. We recommend “Mahale wood mouse” as an

English common name.

DISCUSSION

Comments on cryptic diversity

With the results presented here, the numbers of recog-

nized species of Hylomyscus have increased from 8 to 21

since 2005. The 160% increase documented here over the

past 14 years for Hylomyscus is an extraordinary number

for a continental system; typically, sites of high increase

in newly described species diversity are found on island

systems (e.g., Madagascar, Goodman & Soarimalala

2018; Indonesia, Demos et al. 2016; Philippines, Heaney

Bonn zoological Bulletin 69 (1): 55—83

et al. 2016). For Hylomyscus, such increases are due to

the resurrection of synonymized taxa, new explorative

surveys, and the recognition of cryptic species through

genetic methods. Recently, based on molecular results,

Nicolas et al. (2020) have shown that an additional 8—10

Species remain undescribed from the genus, including

potentially one more from the anse/li group (figs 1-2:

H. sp7). Accordingly, we predict a further increase of at

least 30% over the next decade within the genus, because

other species groups, especially those primarily distrib-

uted in the Congo Basin, have not yet been satisfactorily

collected, documented or analyzed. We predict compa-

rable increases will be attained in several other African

small mammal groups including Graphiurus, Dendro-

mus, Crocidura and various microbat species complexes

currently being documented by Demos, Patterson, Es-

selstyn, Voelker, Kerbis Peterhans and colleagues (e.g.,

Demos et al. 2018, 2019a, 2019b; Patterson et al. 2019).

Such cryptic, typically nocturnal, small mammal species

that form the bulk of mammalian diversity (>70%), are

often unrecognized by the scientific community. As an

alternative, the work of Krasova et al. (2019) has tak-

en a different approach in their review of the Mus triton

complex; despite relatively important genetic multilocus

differences among allopatric populations they have not

split the complex into multiple species. Genetic analyses

provided here are crucial in uncovering cryptic diversity

within Hylomyscus. Although similar morphologically,

H. stanleyi is only distantly related to true H. anselli,

with which it had been co-mingled. Its close geograph-

ic proximity (ca. 400 km) and similar phenetics made it

tempting to include the two as a single taxon (Carleton &

Stanley 2005; Carleton et al. 2006; Demos et al. 2014a;

Carleton et al. 2015; Nicolas et al. 2020).

Sadly, despite the lip-service, this is an era marked by

declining resources and opportunities for field work and

surveys, closure of dozens of natural history collections,

a collapse in the number of trained alpha taxonomists

and a lack of appreciation for the importance of biodi-

versity and the willingness to document it (Winker 1996;

Tewksbury et al. 2014). Further, some conservation ad-

ministrators feel 1t more important to protect individual

organisms rather than entire ecosystems (Goodman &

Lanyon 1994), a short-sighted strategy easily maintained

by arm-chair ‘conservationists’. Although this strategy

may make sense among high profile taxa like gorillas or

pandas, many ecosystems do not boast such charismatic

species. The high fecundity of most small mammal spe-

cies makes them quite resilient to collecting, but habitat

loss reduces viable populations permanently. Further,

integrative taxonomic revisions of small mammals can

identify the regions with the highest (most valuable) evo-

lutionary diversity and therefore provide straightforward

suggestions for prioritization of conservation efforts.

©ZFMK

76 Julian C. Kerbis Peterhans et al.

Comments on biogeography

The Cytb data (Fig. 4) suggest that the once united clades

of H. anselli and H. denniae (under Hylomyscus denniae)

are not only distinct, reciprocally monophyletic, and not

each other’s sisters, but also have separate lowland for-

est origins. This answers the question posed by Carleton

et al. (2006: 318) on whether or not these two montane

species groups shared a recent common ancestor, rela-

tive to taxa from the Guineo-Congolian lowlands. The

occurrence of two new members of the H. anse/li group

in the heart of the Congo Basin, including the first one to

diverge, suggests a lowland origin for the group. Other

members of core Congo Basin taxa (1.e., H. alleni and H.

parvus groups) form a clade sister to the H. anselli group.

In addition, within the H. anse/li group, H. pygmaeus

from the Congo Basin is sister to all other members. Hy-

lomyscus thornesmithae from the Congo Basin is sister

to our East Africa clade (Kenya, Tanzania and Malawi).

Additional material from the Guineo-Congolian rainfor-

est, especially from the left bank of the Congo/Lualaba

River, may shed light on these biogeographic relation-

ships, as would ancestral area reconstruction, which was

not carried out in this study.

A significant phylogeographic break, shown here be-

tween the H. anselli/H. heinrichorum clade and the

rest of the H. anselli clade (excepting H. pygmaeus and

H. thornesmithae but including H. kerbispeterhansi,

H. stanleyi, H. mpungamachagorum, and H. arcimonten-

sis) has been depicted by Chapin (1932: fig. 18) in his

delimitation of bird distributions. Chapin distinguishes a

Rhodesian Highland District (= Zambian, including the

ranges of H. heinrichorum and H. anselli; Chapin 1932:

fig. 18, zone 14; see our Fig. 14) from an East African

Highland District (zone 13, known known here as the

East African clade), including the remaining taxa. It may

be that these zones are separated by the Luangwa River

Valley in northeastern Zambia as has been shown for the

divide between Praomys delectorum of northern Malawi

and Praomys jacksoni of NE Zambia (Ansell 1978: Map

187; Bryja et al. 2012: fig. 2c). The Luangwa River also

seems to be the eastern limit in the distribution of Hy-

lomyscus anselli (as “Praomys denniae’ in Ansell 1978:

Map 188; Bryja et al. 2012: fig. 2d). Further collecting

on both sides of the upper Luangwa River is necessary to

determine if this break holds for other small mammals.

This biogeographic break, as well as additional potential

barriers to extant small mammal distributions, are de-

picted in Fig. 14. Although not as strongly supported, the

sister relationship of H. arcimontensis to other members

of the East African clade (Fig. 4), demonstrates the long

term isolation of the Eastern Arc Mountains from adja-

cent East African montane systems.

Mbizi Forest is, by definition, an Albertine Rift Forest,

as it is adjacent to the SW end of Lake Tanganyika. It

also lies ca. 200 km NW of the Southern Highlands of

Bonn zoological Bulletin 69 (1): 55—83

Tanzania and floristically is most closely related to these

latter forests and the mountains around the northern end

of Lake Malawi (Kerfoot 1964; White et al. 2001). There

is no clear geographical barrier to montane forest species

between Mbizi Forest and the forests around the northern

end of Lake Malawi in the Southern Highlands. These

areas are connected by high ground that could have

supported montane forest in a wetter and colder period.

However, there may have been a rain-shadow from the

Southern Highlands that would have limited the extent of

forest in this area (Moreau 1966).

Mbizi also contains elements of the forests of the Ken-

yan Highlands (Lovett 1990) as well as the Albertine

Rift forests (30 of the 70 tree species are Albertine Rift

endemics; Plumptre et al. 2007). Looking to the north,

mixed affinities and disjunctions in distribution may be

explained by the Karema Gap (Moreau, 1966), which

forms an ecological barrier between Mbizi forest and the

forested habitats of the Mahale Mountains (aka Kungwe

Forest). This is a trough nearly 100 km wide extending

from the shore of Lake Tanganyika southeast to the Ruk-

wa Valley (further discussion below). Much of the terrain

in the Karema Gap lies below 1000 m and forms a major

biogeographical barrier to montane forest bird species

distribution (Moreau 1966). It is apparent that this gap is

also an important barrier for mammals.

Mbizi Forest is at the southern end of the postulated

southwestern dispersal route for Guineo-Congolian for-

est species into the Eastern Arc (Lovett & Wasser 1993).

However, Mbizi falls within the Lake Tanganyika cli-

mactic zone (Lovett 1990) and has notable faunistic dif-

ferences. A number of neo-endemic and relictual forms

of birds, reptiles, amphibians, and mammals are found in

Mbizi with varying affinities to taxa in the Eastern Arc,

Southern Highlands, Albertine Rift, and Guineo-Con-

golian forests (Vesey-Fitzgerald 1964; Moreau 1966;

Britton 1980; Channing & Howell 2006; Plumptre et al.

2007). This is reflected in our phylogeny (Fig. 4) as

the Mbizi population (Hy/omyscus stanleyi) is sister to

H. kerbispeterhansi from the Kenyan Highlands rather

than the more proximate Mahale population (H. mpunga-

machagorum).

There are significant differences between the small

mammal communities of Mbizi and the Southern High-

lands: Mbizi is inhabited by Praomys jacksoni (Mize-

rovska et al. 2019), whereas the Southern Highlands are

inhabited by the phylogenetically distant Praomys delec-

torum (Bryja et al. 2014; Sabuni et al. 2017). Though they

are sister species, Mbizi houses the endemic Lophuromys

sabunii, while Southern Highlands are inhabited by Lo-

phuromys machangui (Verheyen et al. 2017; Sabuni et al.

2018). Finally, Mbizi is inhabited by Crocidura montis

1b, while Southern Highlands are inhabited by Crocidu-

ra montis 3 = ‘luna’ (Sabuni et al. 2018: fig. 2b). On the

other hand, the dry forest species living in woodland ec-

otones were able to disperse from northern part of South-

©ZFMK

Four new Hylomyscus (Muridae) from Africa 77

ern Highlands to the northwest along Lake Tanganyika

(e.g., Mus triton, clade D, Krasova et al. 2019; Gram-

momys surdaster, clade su4, Bryja et al. 2017).

The montane forests of the Mahale Mountains are also

an outlier of the Albertine Rift forests (Plumptre et al.

2007). To their south is the Karema Gap while to their

north lies the 70 km. wide Kigoma-Malagarasi River

Gap, separating Mahale from the Burundi Highlands

(Moreau 1966). In an earlier, unfortunately overlooked

paper, Moreau (1943) reviewed geological evidence for

the origins of the Karema Gap and pointed to an ancient

west to south-east trough of a geological age exceeding

that of the Lake Tanganyika basin. On the west side of

Lake Tanganyika, this trough is filled by the Lukuga

River, which exits the lake at Kalemie (formerly Al-

bertville). The age of this trough may explain why HAy-

lomyscus stanleyi is more closely related to Hylomyscus

kerbispeterhansi in southern Kenya (almost 1000 km to

the northeast) than to the more proximate taxon, Hylomy-

scus mpungamachagorum, less than 300 km to the north.

Moreau was convinced that Karema Gap is of much

greater biogeographic significance than the Malagarasi

River Gap.

On their western slope, Mahale forest cover is near-

ly continuous from the montane forests on the ridge at

2400 m down to lowland forests at 780 m on the shore

of Lake Tanganyika. Only 39 of the 1,170 plant species

recorded at Mahale are Albertine Rift endemics (Nishi-

da & Uehara 1981; Plumptre et al. 2007). The lowland

forests harbor mammal species more typical of the

Guineo-Congolian lowland forests (Moyer 2006), in-

cluding Pan troglodytes schweinfurthii, Manis gigantea,

and Protoxerus stangeri ssp., aS well as birds (e.g.,

Phyllastrepus scandens) and reptiles (e.g., Dendroaspis

jJamesoni). At least two small mammal species from the

W.T. Stanley 2003 Mahale survey have an origin in the

Southern Highlands of Tanzania (including Mt. Rungwe)

with extensions into the Marungu Highlands of DRC.

These are Otomys lacustris Allen & Loveridge, 1933 and

Rhynchocyon cirnei reichardi Reichenow, 1886: see dis-

cussions in Taylor et al. (2009), Corbet & Hanks (1968),

and Rathbun (2017: fig. 3). Small mammals originat-

ing in the Albertine Rift include Grammomys cf. dryas,

Praomys jacksoni and Sylvisorex aff. ruandae. On the

other hand, both new species of Tanzanian Hylomyscus

described here (H. mpungamachagorum, H. stanleyi) are

closely related to forms from the Kenyan Highlands and

the Eastern Arc montane archipelago (Fig. 4). It is likely

that when the ancestor of the Eastern Afromontane clade

of H. anselli group dispersed from the Congo Basin, the

Albertine Rift Mountains were already inhabited by the

H. denniae clade. They were able to colonize the periph-

eral (southern) parts of these mountains, from where they

colonized the Eastern Arc Mountains up to parts of the

Kenyan Highlands. In both the Kenyan and Tanzanian

Highlands, the H. anselli and H. denniae groups are typi-

Bonn zoological Bulletin 69 (1): 55—83

cally mutually exclusive; only in the Mau Forest (Kenya)

are both species groups found in sympatry.

Several other breaks in the distribution of the Hylomy-

scus denniae and Hylomyscus anselli clades, referenced

in Figure 14 are worthy of mention. One of them is the

restriction of Hylomyscus denniae to the Ruwenzori

Mountains of western Uganda and eastern DRC as first

demonstrated by Huhndorf et al. (2007) and subsequent-

ly by Demos et al. (2014a). This break is reinforced by

the Semliki River to the south and the Victoria Nile to

the north. Surveys of the Blue Mountains to the north

of the Ruwenzoris would be enlightening in this regard.

The arid corridor of northeastern Uganda, here called

the Karamoja Gap (Fig. 14), further isolates species of

H. denniae (sensu strictu) from other Hy/momyscus ssp.

in western Kenya (e.g., Mt Elgon and Cherangani Hills;

Demos et al. 2014a). Our collections and surveys have

failed to detect members of the Hylomyscus denniae or

Hylomyscus anselli groups in the Imatong Mountains of

southern Sudan and their foothills in northern Uganda

(i.e., Agora Agu Forest Reserve); only Hylomyscus stella

has been recovered from these forests. Butynski (in litt.)

believes that the primate communities (1.e., galagos and

vervets) of Agora Agu/Imatong Forests are slightly more

closely allied with the Albertine Rift forests than with the

Kenya Highlands and further, that the Victoria Nile, de-

Spite its young age may have been a factor in isolating the

chimpanzee (Pan troglodytes) to the Albertine Rift (al-

though they have older mid-Pleistocene fossils in Kenya;

McBrearty & Jablonski, 2005).

Another arid corridor, the Tsavo Gap (Fig. 14), sep-

arates the northernmost population of Hylomyscus ar-

cimontensis (Taita Hills in SE Kenya) from another

relative of the Hylomyscus anselli group in the Kenya

Highlands (Hylomyscus kerbispeterhansi) as well as the

more distantly related Hylomyscus endorobae (Mt. Ken-

ya, the Aberdares and Mau Escarpment). It is curious

that no Hylomyscus spp. have persisted in the Volcanic

Highlands of northern Tanzania (Mt. Kilimanjaro, Mt.

Meru, Arusha, Ngorongoro Crater) despite our collect-

ing efforts in these areas. In this regard, specimens from

northern Tanzania (Tengeru, Ngorongoro) referred to Hy-

lomyscus anselli by Bishop (1979) in his seminal paper,

were misidentified.

The distribution of Hylomyscus arcimontensis (indeed

the genus Hylomyscus) comes to an abrupt end in Mwen-

embwe Forest, Nyika National Park, northern Malawi.

This gap, called here, the central Malawi Gap, at about

12° south, lies ‘between Nyika and Mount Ntchisi within

the central highlands of Malawi’ (Kaliba 2014: 213 in

his discussion of bird and mammal distributions; see his

fig. 6.1). In her review of avian biogeography in Mala-

wi, Dowsett-Lemaire (1989) pinpoints the major Malawi

avian break slightly further south, at 14°.

These biogeographic factors have received little atten-

tion since Moreau’s (1966) discussion of their impacts on

©ZFMK

78 Julian C. Kerbis Peterhans et al.

bird distributions. The biotic impacts of these isolating

mechanisms must be considered in future conservation

management decisions. Given this faunal mosaic, the

discovery of pockets of endemism, and the likelihood

of discovering further unknown biodiversity, we call for

new surveys of the virtually undocumented highlands of

the Albertine Rift along the shores of Lake Tanganyika

including the Marungu Highlands of southeastern Dem-

ocratic Republic of Congo (not surveyed since 1884 by

Richard Bohm; Noack 1887) and Gombe Mountain NP,

well known for its chimpanzees but little else.

Key to Afromontane Hylomyscus (excepting W Afri-

ca) plus all members of the H. anselli group

1. Supra-orbital shelf strongly beaded .........0...00000..

AEP et rome ihr» cet oe: litte H. aeta (Thomas, 1911)

2. Supra-orbital shelf not beaded... 3

3. Sub-squamosal foramen tiny/absent, hamular

process short & thick (H. denniae group) .............. 5

4. Sub-squamosal foramen large, hamular process

Taso inna9 ce ers sh mee na ae 8 age 2 shoe cae ae rae so 9

5. Only found in Ruwenzori montane forests, size large

ONL 25 .6-27.8 00.0... H. denniae (Thomas, 1906)

6. Found in other East African montane forests ........ 7

7. Size large, CI 26.8—28.6, Kenya only: Mt Kenya,

Aberdares & Mau forests ..0.......0.cccccccccccseeeeteeens

Bets. ance ee a nel H. endorobae (Heller, 1910)

8. Size small, Cl 24-26 mm, Albertine Rift S of

Ruwenzoris (not including Tanzania) ...........0.....00..

....H. vulcanorum (Lonnberg & Gyldenstolpe, 1925)

9. Teats 4+4, incisors orthodont ............0.00000cc ee

pn ON Ree NES 2 ReaD H. stella (Thomas, 1911)

10. Teats 2+4, incisors proodont, orthodont or weakly

opisthodont (HA. anselli group) ..........00..ccccecceees 1

1la.Crown length of upper tooth row under 3.3 (Congo

FFAS SITIAL YM. 0, fk de TO ay Ree ee Soa tes 13

11b.Crown length of upper tooth row 3.3—4.0

(AirOMOn Caine: A CCH iM, ste oN aso 22 ss ate ee 15

llc.Crown length of upper tooth row over 4.0

(Atromeontane. lated) ewes se: eres ee 2 a 19

13. Crown length of upper tooth row under 1.8, slightly

PROOCONE. © x, hE!) Ae eae H. pygmaeus (sp. nov.)

14. Crown length of upper tooth row 3.0-3.25,

OLLNOGOMUpS ae. 2 ame los St H. thornesmithae (sp. nov.)

15. Post palatal foramina at rear (3™ lamina) of M1, LD

and NL longer, Table 4 (montane Kenya only) ........

TO Meee H. kerbispeterhansi Demos et al., 2014

16. Post palatal foramina between M1 and M2 or at

beginning of M2, LD and NL shorter, Table 4 ..... 17

17. Post palatal foramina between M1 and M2, incisive

foramina fall just short of upper molar alveoli, upper

incisors orthodont (Eastern Arc only) ............0.0..04.

Sener H. arcimontensis Carleton & Stanley, 2005

18. Post palatal foramina at beginning of M2, incisive

foramina reach upper molar alveoli, upper incisors

Bonn zoological Bulletin 69 (1): 55—83

typically opisthodont (Mahale Mts only) ................

Armee need fet aoe ew a ke H.. mpungamachagorum (sp. nov.)

19. Incisive foramina penetrate CLM, © slightly

opisthodont (Angola only)... ecceceeeees

pograh gears. 08. 22 H. heinrichorum Carleton et al., 2015

20. Incisive foramina do not penetrate CLM ............. A

21. Occipito-nasal length under 26.4, nasal length under

9.4 (Zambia only) ............. H. anselli (Bishop, 1979)

22. Occipito-nasal length over 26.3, nasal length over

9.3 (Mbizi Mts only) ............... H. stanleyi (sp. nov.)

Acknowledgements. Thanks to A Ferguson, Collections

Manager and JD Phelps, Assistant Collections Manager (both

Field Museum) for their assistance. T Hanrahan assisted with

data gathering. P Jenkins, R Portela-Miguez, and L Tomsett

(BMNH) provided access to collections at the Natural History

Museum (London). C Mateke (Curator of Mammals, Nation-

al Museum of Zambia, Livingstone) provided photographs of

the field data of all Zambian-based specimens of Hylomyscus

anselli, where the majority of specimens from this taxon are

housed. Figs. 13 1s courtesy of R Kistinger. Fig. 9d are based on

photos of palate and feet taken by M Lovy and L Ple8tilova re-

spectively, using material collected during fieldwork organized

by R Sumbera (Zambia) and J Krasova (Angola). J Weinstein,

Field Museum, Photography, provided the skull and skin pho-

tos of the type specimens (Figs. 5, 6, 11, 12). We thank the Col-

laborative Invertebrate Laboratories at the Field Museum, Dr

M Thayer for use of imaging equipment (funded by NSF grant

EF-0531768/subcontract 144-439), the Grainger Foundation,

and S Ware for layered photography of Hy/omyscus palates and

tooth rows. WT Stanley took the photos of the live specimens

of H. mpungamachagorum and H. stanleyi. SO Bober (FMNH)

prepared Fig 3. Q Luke updated botanical taxonomy and pro-

vided important botanical input for Tanzanian localities. MA

Rogers has provided crucial data and assistance throughout. We

acknowledge the One Health Office, Center for Disease Con-

trol and Prevention (Atlanta, USA) and National Institute of

Health’s grant 1RO1TW008859-01: Sylvatic Reservoirs of Hu-

man Monkey Pox for having funded two trips (2012, 2013) to

DR Congo. Fieldwork in Angola was supported by the Grant

Agency of the University of South Bohemia no. 018/2017/.

For work, permits and funding the senior author extend thanks to

the following. Burundi: L Davenport, AJ Fisher, A Nibizi, and P

Trenchard, with permit approval from the Institut National pour

Environment et la Conservacion de la Nature (Mr A Nyokindi &

Dr L Ntahuga, Directeurs General). For Uganda: M Grey, S Jen-

nings, PK Austin, R Kityo, K Musana, and E Tibenda with permit

approval from the Department of Game (Moses Okua) and the

Research and Monitoring Section of the Uganda Wildlife Author-

ity. For work in the Democratic Republic of Congo: J Hart and

T Hart (TL2 and Epulu), with permit approval from the Institut

Nacional pour la Conservacion de la Nature; the scientific team at

Lwiro (Centre de Recherché des Sciences Naturelles, Dr A Bash-

wira, Scientific Director), including J Mwanga, B Ndara Ruszi-

ga, R Kizungu, P Kaleme and R Nishuli. For work in Rwanda: T

Mudakikwa (MINIRENA), Minister of Environment; N Ntare,

Michel Masozera, Nerissa Chao (all of Wildlife Conservation

Society), Rwanda Development Board and National Universi-

ty of Rwanda. For work in Kenya: B Agwanda and S Musila

with permits and logistical support from Kenya Forest Service,

Kenya Wildlife Service, and the National Museums of Kenya.

For financial support, we acknowledge the Barbara Brown Fund,

the Ellen Thorne Smith Fund, the Marshall Field HI Fund of The

©ZFMK

Four new Hylomyscus (Muridae) from Africa 79

Field Museum, the John D and Catherine T MacArthur Founda-

tion, the World Wide Fund for Nature (WWEF-Itombwe) and the

Wildlife Conservation Society (WCS-Rwanda, DR Congo). F

Dowsett-Lemaire, R Dowsett, J Bates and T Butynski provided

helpful input on biogeography of birds in Malawi and primates

in northern Kenya. Comments from Ryan Norris and one anon-

ymous reviewer are gratefully acknowledged. This project be-

gan some 2’ years ago when one of us (RH) noticed that the

identification of a specimen from WT Stanley’s collection from

the DR Congo did not look like ‘Dendromus’ as it had been

catalogued.

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APPENDIX 1

Specimens examined in this study (n = 199). Specimens

included in the morphometric analyses only are in stan-

dard type, those included in both morphometric and mo-

lecular analyses are in boldface type, and those included

in the molecular analyses only are indicated with an as-

terisk (*). All specimens include Field Museum of Nat-

ural History (FMNH) catalogue numbers except for the

Hylomyscus anselli type series from the British Museum

of Natural History (BMNH), National Museum of Zam-

bia (NMZ), Specimens from the Czech Republic located

at the University of South Bohemia and at the Institute of

Vertebrate Biology have the following acronyms: ANG

for specimens from Angola and RS for specimens from

Zambia.

Hylomyscus aeta (1): Uganda, Nteko Parish, edge of

Bwindi-Impenetrable NP, 1600 m: 160492*.

Hylomyscus anselli (19): Zambia, Mwinilunga Dist.:

Jimbe Stream, BMNH 74.250 (TYPE), NMZ 3639,

NMZ 3808; Kasombu Stream (‘Isombu’, see Ansell,

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The avian example. Conservation Biology 10: 703-707

1978), NMZ 3631; Nyanjowe Stream (‘Nyansowe’, An-

sell 1978), BMNH 74.251, NMZ 3638; Sakeyi Stream

(Sabeji, Sekezhi; see Ansell, 1978), BMNH 61.944;

Mpika Dist., Danger Hill, Lubikila Stream (‘Lubiliki-

la’, “Luitikila’; see Ansell 1978) BMNH 73.142, NMZ

2764-2767, NMZ 2769-2781; Kasanka National Park,

pontoon, RS 1113-1115; Kasanka National Park, Fib-

we, RS 1606-1607; Zambezi source, RS 803, 810, 811;

Kifubwa Rock Shelter Stream, RS 818; Nchila Wildlife

Reserve, RS 793.

Hylomyscus arcimontensis (58): Malawi, Misuku Hills,

Mughese Forest, 1625 m: 196303, 196311*, 196753,

196754—196759, 196761; Misuku Hills, Mughese Forest,

1890 m: 196762—196769; Nyika National Park, Mwen-

embwe Forest, 2233m: 211576*, 211577*; Tanzania, Mt

Rungwe, Rungwe FR, 5 km E Ilolo, 1870 m: 163584—

163588, 163590—163595; Mt Rungwe, Rungwe FR, 6 km

E, 1.2 km N of Ilolo, 2140 m: Mt Rungwe, Rungwe FR,

7kmE,2.5 km N of Ilolo, 2410 m: 163598—163600; East

Usambara Mts, 4.5 km ESE Amani, Monga Tea Estate,

870-900 m: 150120, 150121, 150123, 150124, 150125,

150142, 150143*, 150146, 150147, 150149, 150150,

©ZFMK

82 Julian C. Kerbis Peterhans et al.

150153, 150430; East Usambara Mts, 4.5 km WNW

Amani, Monga Tea Estate, 870—900 m, 150119, 151251;

East Usambara Mts, 4.5 km NW Amani, Monga Tea

Estate, 1100 m, 147291, 147476*; East Usambara Mts,

6 km NW Amani, Monga Tea Estate, 1100 m, 150118*:

West Usambara Mts., 12.5 km NW Korogwe, Ambangu-

lu Tea Estate, 1300 m, 150130, 150135, 150136, 150138,

150154, 150156, 150159.

Hylomyscus denniae (1): Uganda, Rwenzori Mts NP,

Mubuku R, rt bank, Nyabitaba Hut , 2667 m: 144526*.

Hylomyscus thornesmithae (5): Democratic Republic of

Congo, 14 km N of Boende, Quartorze, 326 m: 222524

(TYPE); 4 km N of Boende, Baliko, 358 m, 2119611-

219613,219689.

Hylomyscus endorobae (1): Kenya, Aberdare Range,

3.8km W & 2.5 km S of Gatarakwa, 2700 m: 190467*.

Hylomyscus heinrichorum (25). Angola, Mt Moco,

83793, 83795, 83796 (TYPE), 83797, 83799, 83801-

83807, 83895; Mt Soque, 83783-83792; Namba Village,

ANG 210, ANG 215, ANG 237, ANG 252, ANG 259.

Hylomyscus kerbispeterhansi (55): Kenya, Cheranga-

ni Hills, Kipkunnur Forest, 2740 m: 217377, 217381-

217382, 217383*, 217384, 217385*, 217386, 217390,

217394217395, 217408, 217422, 217605—217610,

217612—217614; Kapenguria, 153250, 2100 m; Mau

210000, 210001*, 210017 (TYPE), 210018, 210023,

210042: Mau Forest, 8.5 km N & 18.4 km E of Keri-

cho, 2320 m: 210061—210063, 210065, 210069, 210071,

Mt Elgon National Reserve, nr. Kimothon Gate, 2530 m:

217325*, 217327-217333, 217340-217342, 217345,

217354, 217358, 217597-217600, 217601, 217602,

217604.

Hylomyscus mpungamachagorum (6): Tanzania, Maha-

le Mts NP, Mahale Mts, 0.5 km NW of Nkungwe Sum-

mit, 2100 m: 177911, 177888, 177889 (TYPE), 177890;

Mahale Mts NP, Mahale Mts, 0.5 km S of Pasagulu Hill,

1420 m: 177886—177887.

Hylomyscus pygmaeus (1): Democratic Republic of

Congo, Baleko, 358 m, 219684 (TYPE).

Hylomyscus stanleyi (25): Tanzania, Mbizi Forest Re-

serve, 0.5 km N, 4 km E of Wipanga, 2200 m: 171357-

171359, 1171360, 171361, 171362 (TYPE), 171363,

171364—171367; Mbizi Forest Reserve, 0.5 km S,3 km E

of Wipanga, 2300 m: 171343, 171344, 171346—-171348,

171350, 171351, 171352, 171353, 171354-171356,

PANS 1S SASS

Hylomyscus stella (1): Uganda, Bwindi-Impenetrable

NP, Buhoma, 1500 m: 160511*.

Hylomyscus vulcanorum (1): Democratic Republic

of Congo, Itombwe Forest, 1.5 km S Lusasa, 2050 m:

Forest, 15.5 km N, 16.4 km E Bonet, 2350 m: 209997, 203881*.

APPENDIX 2

List of GenBank sequences.

Taxon Voucher No. GenBank No. Country

Hylomyscus aeta FMNH 160492 MN857618 Uganda

Hylomyscus alleni AF518328 Gabon

Hylomyscus anselli RS1113 JX126613 Zambia

Hylomyscus anselli RS1114 JX126614 Zambia

Hylomyscus anselli RS1115 JX126615 Zambia

Hylomyscus anselli RS1606 JX126616 Zambia

Hylomyscus anselli RS810 JX126617 Zambia

Hylomyscus anselli RS811 JX126618 Zambia

Hylomyscus anselli RS818 JX126619 Zambia

Hylomyscus anselli RS793 JX126620 Zambia

Hylomyscus anselli RS803 JX126621 Zambia

Hylomyscus arcimontenisis FMNH 196753 KF876468 Malawi

Hylomyscus arcimontenisis FMNH 196311 KF876469 Malawi

Bonn zoological Bulletin 69 (1): 55—83

Taxon

Hylomyscus arcimontenisis

Hylomyscus baeri

Hylomyscus denniae

Hylomyscus endorobae

Hylomyscus grandis

Hylomyscus heinrichorum

Hylomyscus kerbispeterhansi

Hylomyscus stanleyi

Hylomyscus pamfi

Hylomyscus parvus

Hylomyscus pygmaeus

Hylomyscus simus

Hylomyscus mpungamachagorum

Hylomyscus stella

Hylomyscus thornesmithae

Hylomyscus vulcanorum

Hylomyscus walterverheyeni

Four new Hylomyscus (Muridae) from Africa

Voucher No.

FMNH 211577

FMNH 147476

FMNH 150118

FMNH 150143

FMNH 144526

FMNH 190467

ANG0210

ANG0215

ANG0237

ANG0259

FMNH 217383

FMNH 217384

FMNH 217385

FMNH 217325

FMNH 217358

FMNH 217601

FMNH 210000

FMNH 210001

FMNH 171352

FMNH 171353

FMNH 171360

FMNH 171362

FMNH 171363

FMNH 219684

FMNH 177888

FMNH 177889

FMNH 177890

FMNH160511

FMNH 219611

FMNH 219612

FMNH 219613

FMNH 222524

FMNH 219689

FMNH 203881

GenBank No.

KF876477

KF810191

KF810192

KF810193

JQ735509

KF876479

KF810158

JQ735513

MN857622

MN857623

MN857624

MN857625

KF810205

KF810206

KF810203

KF810239

KF810200

KF810240

KF810226

KF810231

MN857627

MN857628

MN857629

MN857630

MN857631

JQ735527

JQ735555

MN857626

JQ735557

MN857619

MN857620

MN857621

MN857632

MN857633

MN857634

MN857635

MN857636

MN857637

KF810176

JQ735614

Country

Malawi

Tanzania

Guinea

Uganda

Kenya

Cameroon

Angola

Kenya

Tanzania

Benin

Cameroon

DR of Congo

Ivory Coast

Tanzania

Uganda

DR of Congo

Central African Republic

Bonn zoological Bulletin 69 (1): 55—83

©ZFMK

BHL

Blank Page Digitally Inserted

Bonn zoological Bulletin 69 (1): 85-94

2020 - Souza-Costa C.A. et al.

https://do1.org/10.20363/BZB-2020.69.1.085

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:lsid:zoobank.org:pub:3C 1 5E85F-2FBD-473 1-A076-2AFE02490DA5

Squamate reptiles from seasonal semi-deciduous forest remnants

in southwestern Bahia, Brazil

Carlos Augusto Souza-Costa', Caio Vinicius De Mira-Mendes’, Iuri Ribeiro Dias’, Kaique Brito Silva‘,

Antonio Jorge S. Argélo*> & Mirco Solé**

'3>.6Graduate Program in Zoology, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado,

km 16, 45662-900 Ilhéus, Bahia, Brazil

?Graduate Program in Tropical Aquatic Systems, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado,

km 16, 45662-900 Ilhéus, Bahia, Brazil

*Institute of Geosciences, Universidade Estadual de Campinas, Rua Jodo Pandia Calogeras, Cidade Universitaria,

13083-870 Campinas, SGo Paulo, Brazil

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

* Corresponding author: Email: msoleQuesc.br

'urn:lsid:zoobank.org:author:3 1 A86EE5-1526-472A-9077-3953CE3A0947

2urn:Isid:zoobank.org: author: EOCB48CB-35D3-4FB9-AA 83-E786C 100AA9E

3urn:Isid:zoobank.org:author:8455227D-DC68-4785-9563-3B29A 7054900

*urn:Isid:zoobank.org:author: CFOBAB75-22F2-4C6F-9C46-402178CBEEEB

Surn:|sid:zoobank.org:author:A83A9207-39BF-4020-A035-92CA78381A71

Surn:Isid:zoobank.org:author:CO62E3CB-D966-44 1 A-8B77-1F94DC85FA92

Abstract. We present a list of Squamata from Serra do Mandim and Serra Azul, both in the Atlantic Forest domain of

Southern Bahia, Brazil. We recorded 27 species (21 snakes and six lizards). Most species can be characterized as gen-

eralists with a wide distribution as Phyllopezus pollicaris, Salvator merianae, Corallus hortulanus, Philodryas olfersii,

Oxyrhopus trigeminus and Pseudoboa nigra. However, some of the species are considered as being difficult to sample and

restricted to forest fragments such as Bothrops bilineatus, Dipsas sazimai and Echinanthera cephalostriata. The snake

fauna of both areas represents 70% of the species previously known for the semi-deciduous forests of the state of Bahia.

Although the study region is under severe anthropogenic pressure, especially due to the expansion of livestock areas, some

forest remnants still withstand a rich reptile diversity.

Key words. Snakes, lizards, richness, biodiversity, species distribution.

INTRODUCTION

Habitat loss and fragmentation are considered serious

threats for terrestrial reptiles (Bohm et al. 2013). Low

dispersion capacity, small home ranges and a low toler-

ance to temperature variations turn this group, especially

forest species, susceptible to changes in their natural en-

vironments (Gibbons et al. 2000). A recent study on the

conservation status of the world’s reptiles showed that

20% of the species are in some kind of threat category,

while another 20% are classified as data deficient (Bohm

et al. 2013). These authors also state that in tropical en-

vironments the number of threatened reptile species has

rapidly increased due to ongoing accelerated habitat de-

struction.

Despite Brazil harboring one of the largest reptile diver-

sities on the planet (Uetz et al. 1995; Costa & Beérnils

2018), a lack of information for a large part of this tax-

Received: 30.09.2019

Accepted: 05.02.2020

onomical group is the common share, mainly concern-

ing natural history aspects and distribution patterns (Ro-

drigues 2005). While a growing number of taxonomical

studies have recently led to the description of several new

species (e.g., Recoder et al. 2014; Fernandes & Hamdan

2014; Hamdan & Fernandes 2015; Barbo et al. 2016;

Rodrigues et al. 2017; Silveira & Santos-Jr 2018; Silva

et al. 2018), there is still a long way to go before this

rich reptile diversity is fully understood. The assessment

of the conservation status of 732 species and sub-species

showed that 13% of the species must be considered as

threatened or nearly threatened, while nearly 9% were

characterized as “data deficient” species (ICMBio 2014).

Knowledge of the conservation status of species is es-

sential for the implementation of conservation actions

in order to mitigate the effects of anthropic actions on

endangered species. In Bahia, the number of studies on

reptiles has increased recently and information is now

Corresponding editor: W. Bohme

Published: 10.03.2020

86 Carlos Augusto Souza-Costa et al.

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H lItarantin City

® Potiragua City

KE Serra do Mandim |

M Serra Azul

Elevation (m)

1181

550

~“\~— Highways

8240000”

“\-—~— Regional rivers

Fig. 1. Studied area in the Serra do Mandim (black clamp) in the municipality of Itarantim and in the Serra Azul (black square) in

the municipality of Potiragua, in southwestern Bahia, Brazil.

available for reptiles inhabiting the central (Freitas et al.

2012), western (Freitas et al. 2016a), northern (Freitas

2014; Freitas et al. 2016b; Marques et al. 2016; Freitas

et al. 2018; Freitas et al. 2019) and southern (Dixo 2001;

Argolo 2004; Dias et al. 2014) regions of the state, while

the southwestern part of the state still shows a large gap

concerning information on its reptiles.

The Mandim and Azul Mountains are located tn south-

western Bahia - Brazil, in the municipalities of Itarantim

and Potiragua, in a region classified as semi-deciduous

seasonal forest (Ibge 1997; Salino et al. 2006). They are

Bonn zoological Bulletin 69 (1): 85-94

within the boundaries of the Rio Pardo and Rio Jequitin-

honha basins, bordering the northeast of Minas Gerais.

While they belong to the Atlantic Forest domain, they

suffer great influence by the Caatinga and Cerrado do-

mains. A project entitled “Biodiversity and conservation

in the Jequitinhonha and Mucuri valleys” was carried

out in the region, which, through biological inventories,

showed that even suffering high levels of degradation,

the region still maintains a great amphibian, bird, and

mammal diversity (Pinto & Bede 2006). The same au-

thors identified several priority areas for conservation

©ZFMK

Squamates of Serra do Mandim and Serra Azul 87

Fig. 2. Study areas in the southwestern region of Bahia. Fugiama farm in the Serra do Mandim (A, C and E). A: Semi-deciduous

forest fragment; C: stream; E: permanent pond. Serra Azul farm in the Serra Azul (B, D and F). B: Semi-deciduous forest fragment;

D: stream; F: permanent pond.

and emphasized the importance of more research aimed Serra do Mandim, aiming to fill a gap in the knowledge

at other still under sampled groups, as, for example, rep- of the group for the state.

tiles. Therefore, the objective of our study was to inven-

tory squamate reptile species from the Serra Azul and

Bonn zoological Bulletin 69 (1): 85—94 ©ZFMK

88 Carlos Augusto Souza-Costa et al.

MATERIAL AND METHODS

Between January 2015 and March 2016 six field cam-

paigns were undertaken to sample squamate reptiles

in two Atlantic Forest areas characterized as season-

al semi-deciduous forest in southwestern Bahia: at the

“Serra do Mandim” (15°37’58” S, 39°59’01” W) in

the municipality of Itarantim, and at the “Serra Azul”

(15°52’01” S, 39°55’54” W) in the municipality of Poti-

ragua (Fig. 1). During every campaign each area was

sampled between three and four days and nights, result-

ing in a total sampling effort of 44 field days by two re-

searchers.

The climate of the region corresponds to the “Am”

type of Koéppen (1936), with average rainfall of 800 to

1100 mm and a temperature range between 23.5°C and

25°C (Ibge 1997). The mountains have gradients of 300—

800 m of altitude.

Reptiles were sampled through active search (Rodel &

Ernst 2004) at 14 sampling sites in each area, including

12 transects with 50 m length within the forest, a 120 m

transect along a stream and a permanent pond (Fig. 2).

All available microhabitats within five meters left and

right of the transects were sampled (fallen trunks, leaf

litter, vegetation and burrows). Due to increased humid-

ity and high concentration of amphibians at the ponds,

these sites were potentially more prone to reveal forag-

ing snakes. During each field expedition, forest transects

were sampled for 40 minutes and streams were sampled

for 90 minutes. The surroundings of the ponds were

searched for 30 minutes. The total sample effort was 60

hours in each of the areas. Occasional encounters during

the team’s displacement between sample points were

also recorded. Additionally to nocturnal sampling squa-

mate reptiles were also sampled during the day from 14h

to 17h on a 10 km trail leading to the areas where the

transects were located.

The reptiles were collected by hand or using snake

hooks and transferred to cotton bags or plastic boxes. The

license to capture reptiles was issued by ICMBio (num-

ber 13709). Specimens were killed with 20% benzocaine

(1mg/g), fixed in 10% formalin for seven days and stored

in 70% ethanol. They were further identified using orig-

inal descriptions available in the literature and deposited

in “Museu de Zoologia da Universidade Estadual de San-

ta Cruz-MZUESC” (Appendix I).

To evaluate sample efficiency, we constructed a rar-

efaction curve with 1000 randomizations, using the to-

tal number of registered individuals in the study area.

We used abundance data per sample to extrapolate the

richness through the non-parametric estimators Chao2,

Jackknife 1 and 2 and Bootstrap (Magurran 1998; Go-

telli & Colwell 2001). The analyses were made using the

software PAST 3.07 (Paleontological Statistics Software

Package for Education and Data Analysis).

Bonn zoological Bulletin 69 (1): 85—94

RESULTS AND DISCUSSION

During our study we recorded 27 species of Squama-

ta, 21 belonging to snakes and six to lizards (Table 1,

Figs 3-4). Among the snakes, the Dipsadidae family was

represented by 12 species, followed by Colubridae with

four. Regarding lizards only the family Tropiduridae was

represented by two species, while the other families only

had one representative. Of all recorded Squamata, none

is listed in the Brazilian list of threatened taxa (ICM-

Bio-Portaria MMA n° 444/2014 and n° 445/2014).

The comparison with the reptile fauna from surround-

ing areas near Serra do Mandim and Serra Azul is ham-

pered by the absence of such kind of studies. In general,

the recorded squamate fauna (n=27) can be considered

larger than that of other sampled areas in the region,

as some municipalities from the northeast of the state

of Minas Gerais (n=11, Feio & Caramaschi 2002) and

from the APA da Lagoa Encantada, between the cities

of Ihéus, Floresta Azul and Almadina (n=17, Dias et al.

2014). Other studies undertaken in Atlantic Forest areas

revealed larger squamate reptile richness, as the one by

Arg6élo (2004) reporting 61 species of snakes from co-

coa plantations in southeastern Bahia. It is worth men-

tioning that this study was conducted during a time span

of 12 years. Hamdan & Lira-Da-Silva (2012) reported

the occurrence of 30 species of snakes for the seasonal

semi-deciduous Forest of the state of Bahia. We managed

to report 70% of the species reported for this kind of veg-

etation in the state.

Most of the recorded species show a wide distribu-

tion, occurring both in the Atlantic Forest and in the

Caatinga domain, such as Phyllopezus pollicaris, Salva-

tor merianae, Corallus hortulanus, Philodryas olfersii,

Oxyrhopus trigeminus, Pseudoboa nigra and Xenodon

merremii (Vanzolini et al. 1980; Rodrigues 1986; Arg6-

lo 2009; Hamdan & Lira-Da-Silva 2012; Marques et al.

2012c). Others are typical from Caatinga environments,

such as Tropidurus hispidus (Vanzolini et al. 1980; Ro-

drigues 2003) while others are restricted to the Atlantic

Forest domain such as Dipsas sazimai and Echinanthera

cephalostriata. Despite having a wide distribution range

in the Atlantic Forest, D. sazimai has only been reported

thrice from the state of Bahia (Roberto et al. 2014). This

species 1s rare and typical of forest environments and fol-

lowing Fernandes et al. (2010) it should be considered

potentially endangered. Echinanthera cephalostriata can

be found in the Atlantic Forest domain from Santa Cata-

rina to southwestern Bahia state (Argolo & Jesus 2008).

In Bahia, it is considered a rare species, with occurrence

associated with montane forest, above 600m altitude (Ar-

gdlo 2009). These two species (D. sazimai and E. cepha-

lostriata) have been included in the recently launched list

of threatened species of the state of Bahia (SEMA 2017)

as vulnerable (VU) and endangered (EN), respectively.

©ZFMK

Squamates of Serra do Mandim and Serra Azul 89

Table 1. Richness and composition of Squamata species recorded at the Serra do Mandim and at the Serra Azul in southwestern

Bahia, Brazil. Sampling method: OE-opportunistic encounter; FT-Forest transect; P-pond; ST-Stream transect.

*Nomenclature follows Costa & Bérnils (2018).

Family/species* S. Mandim Serra Azul Total

LIZARDS

Phyllodactylidae

Phyllopezus pollicaris (Spix, 1825) — OE 01

Dactyloidae

Norops fuscoauratus (D’ Orbigny,Dumeril & Bibron, 1837) FT — 01

Leiosauridae

Enyalius catenatus (Wied, 1821) FT, ST, OE FT, OE 21

Tropiduridae

Tropidurus torquatus (Wied, 1820) P, OE — 02

Tropidurus hispidus (Spix, 1825) — P 01

Teiidae

Salvator merianae (Dumeéril & Bibron, 1839) — OE 01

SNAKES

Boidae

Corallus hortulanus (Linnaeus, 1758) FT, ST — 02

Colubridae

Chironius fuscus (Linnaeus, 1758) - FT, ST 03

Mastigodryas bifossatus (Raddi, 1820) OE POE 03

Oxybelis aeneus (Wagler in Spix, 1824) ST OE 02

Tantilla melanocephala (Linnaeus, 1758) — OE 03

Dipsadidae

Dipsas sazimai Fernandes, Marques e Argoélo, 2010 FT FT, OE 05

Echinanthera cephalostriata Di-Bernardo, 1996 — FT 02

Erythrolamprus miliaris (Linnaeus, 1758) OE P 02

Erythrolamprus poecilogyrus (Wied, 1825) — OE 03

Imantodes cenchoa (Linnaeus, 1758) - ST, OE 03

Oxyrhopus petolarius (Linnaeus, 1758) - FT 02

Oxyrhopus trigeminus Dumeéril, Bibron e Duméril, 1854 OE PE: 04

Philodryas olfersii (Liechtenstein, 1823) OE — 01

Pseudoboa nigra (Dumeril, Bibron & Dumeril, 1854) - OE 01

Sibynomorphus neuwiedi (Thering, 1911) FT FT 02

Thamnodynastes nattereri (Mikan, 1828) SJ]; OE EL. 04

Xenodon merremii (Wagler in Spix, 1824) OE OE 05

Leptotyphlopidae

Trilepida salgueiroi (Amaral, 1955) — OE 01

Viperidae

Bothrops jararaca (Wied, 1824) PE Sd ET, S17, OE 18

Bothrops leucurus Wagler in Spix, 1824 SL, P2OE P, OE 07

Bothrops bilineatus (Wied-Neuwied, 1821) ST — 02

Total 16 22 102

Bonn zoological Bulletin 69 (1): 85—94 ©ZFMK

90 Carlos Augusto Souza-Costa et al.

F #

| \

- /

! t

> '

“a. —_-

Pow aA m

Fig. 3. Squamata recorded at Serra do Mandim and Serra Azul in southwestern Bahia, Brazil. A. Norops fuscoauratus, B. Enyalius

catenatus (male); C. E. catenatus (juvenile); D. Chironius fuscus; E. Dipsas sazimai;, F. Imantodes cenchoa.

The rarefaction curve did not reach the asymptote and

remained in ascending function (Fig. 5), even though

69% to 86% of the species indicated by the richness es-

timators (Chao 2 = 32.1 + 4.3; Jacknife 1 = 36.2 + 4.2.

Jacknife 2 = 39.2 and Bootstrap = 31.4) were sampled.

However, the use of additional sampling methods as pit-

Bonn zoological Bulletin 69 (1): 85—94

falls (Cechin & Martins 2000) and funnel traps (Green-

berg et al. 1994) could lead to an increase in the diversity

of sampled Squamata for the region, since they allow the

record of species that have specific habits and are hardly

sampled during active search, such as fossorial snakes

and lizards (Macedo et al. 2008).

©ZFMK

Squamates of Serra do Mandim and Serra Azul

Fig. 4. Squamata recorded at Serra do Mandim and Serra Azul in southwestern Bahia, Brazil. A. Echinanthera cephalostriata,

B. Mastigodryas bifossatus, C. Oxyrhopus trigeminus, D. O. petolarius; E. Oxybelis aeneus, F. Trilepida salgueiroi, G. Bothrops

jararaca, H. B. bilineatus.

Bonn zoological Bulletin 69 (1): 85—94

92 Carlos Augusto Souza-Costa et al.

307

Number of species

25 50 75 100 125 150 175 200

Specimens

Fig. 5. Rarefaction curve based on individuals of Squamata for two regions of semi-deciduous seasonal forest in Serra do Mandim

and Serra Azul in southwestern Bahia, Brazil. The center line corresponds to the mean obtained with 1000 randomizations, and the

lines above and below correspond to the associated standard deviation.

The present study contributes to fill a gap in the knowl-

edge of Squamata of the southwestern region of Bahia,

presenting a list with 27 species of snakes and lizards

for the Serra do Mandim and Serra Azul. Although the

region is suffering great anthropic pressure, mainly re-

lated to the agricultural expansion, the forest remnants

still have conditions to support and maintain species con-

sidered difficult to sample in the Atlantic Forest, such as

Dipsas sazimai and Echinanthera cephalostriata.

Acknowledgements. We thank Cintia de Melo Souto Brige

(in memoriam) and family (Fugiama farm) and José Cord-

eiro de Almeida Filho (in memoriam) and family (Serra Azul

farm) for having allowed the research on their properties.

CASC thanks CAPES-Coordenagéo de Aperfeig¢oamento de

Pessoal de Nivel Superior and FAPESB-Fundacao de Amparo

a Pesquisa do Estado da Bahia, for scholarships. CASC also

thanks Universidade Estadual de Santa Cruz and the Programa

de Pos-Graduacéo em Zoologia for support. MS thanks CNPq,

CAPES and the Alexander von Humboldt Stiftung for grants.

IRD is grateful to CNPq-PDJ (CNPq—Project: 406899/2017-7,

Process: 167387/2017-0) for fellowships. CVMM is grateful to

Coordena¢ao de Aperfei¢oamento de Pessoal de Nivel Superior

(CAPES) for a fellowship (process PNPD/1682788).

Bonn zoological Bulletin 69 (1): 85—94

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APPENDIX I.

Uetz P, Freed P, Hosek J (1995) The Reptile Database. Online at

http://www. reptile-database.org [last accessed 30 Sept. 2019]

List of vouchers deposited in the Museu de Zoologia da Universidade Estadual de Santa Cruz-MZUESC.

LIZARDS

PHYLLODACTYLIDAE. Phyllopezus pollicaris: MZU-

ESC 15911. DACTYLOIDAE. Norops fuscoauratus:

MZUESC 15931. LEIOSAURIDAE. Enyalius catenatus:

MZUESC 15901-15906, 15916, 15917, 15920, 15921,

15922, 15930. TROPIDURIDAE. Tropidurus torquatus:

MZUESC 15939, 15942. Tropidurus hispidus: MZUESC

16546.

SNAKES

BOIDAE. Corallus hortulanus. MZUESC 15929. COL-

UBRIDAE. Chironius fuscus: MZUESC 15934, 15935.

Mastigodryas bifossatus. MZUESC 16541. Oxybelis

aeneus: MZUESC 15910, 15919. Tantilla melanoceph-

ala. MZUESC 15924, 15943, 16538. DIPSADIDAE.

Bonn zoological Bulletin 69 (1): 85—94

Dipsas sazimai: MZUESC 15908, 15913, 15926, 16548.

Echinanthera cephalostriata. MZUESC 15909, 15928.

Erythrolamprus miliaris. MZUESC 15907, 15940.

Erythrolamprus poecilogyrus: MZUESC 15944, 16540,

16543. Imantodes cenchoa: MZUESC 15914. Oxy-

rhopus petolarius. MZUESC 15945, 16544. Oxyrhopus

trigeminus: MZUESC 14687, 15923. Philodryas olfersi:

MZUESC 16547. Pseudoboa nigra: MZUESC 16537.

Sibynomorphus neuwiedi. MZUESC_ 15927, 15932.

Thamnodynastes nattereri: MZUESC 15912, 15933.

Xenodon merremii. MZUESC 16534-16536, 16539,

16542. LEPTOTYPHLOPIDAE. Trilepida_ salgueiroi:

MZUESC_ 16545. VIPERIDAE. Bothrops jararaca:

MZUESC 14469, 14470, 14471, 15915, 15918, 15936,

15937. Bothrops leucurus. MZUESC 15925, 15938.

Bothrops bilineatus: MZUESC 16549.

©ZFMK

Bonn zoological Bulletin 69 (1): 95—103

2020 - Trela J. et al.

https://do1.org/10.20363/BZB-2020.69.1.095

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:Isid:zoobank.org: pub: D821 9FBF-35E6-4791-9EC5-519120C3B543

Sexual morphs of the three native Nearctic species

of the genus Periphyllus van der Hoeven, 1863

(Insecta: Hemiptera: Aphididae),

with identification keys including introduced species

Joanna Trela', Lukasz Junkiert? & Karina Wieczorek>*

'23 Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences,

University of Silesia in Katowice, Bankowa 9, PL-40-007 Katowice, Poland

“Corresponding author: Email: karina.wieczorek@us.edu.pl

'urn:lsid:zoobank.org:author:7 DD6940F-70E6-4CEC-833C-D852E329F43 1

2urn:Isid:zoobank.org:author: AF78807C-2115-4A33-AD65-9190DA612FB9

3urn:Isid:zoobank.org:author:95A5CB92-EB7B-4132-A04E-6163503ED8C2

Abstract. Periphyllus van der Hoeven, 1863 (Hemiptera: Aphididae: Chaitophorinae) is a Holarctic genus, with just three

species native to Nearctic: Periphyllus americanus (Baker, 1917), P. brevispinosus Gillette & Palmer, 1930, and P. negun-

dinis (Thomas, 1878). Males and oviparous females of P. brevispinosus and P. negundinis and males of P. americanus are

described. Original keys to the identification of the known native and non-native sexual morphs of this genus, associated

with maples in the Nearctic Region, are given.

Key words. Aphids, distribution, maple, sexuales.

INTRODUCTION

Periphyllus americanus (Baker, 1917) (American Maple

Aphid), P. brevispinosus Gillette & Palmer, 1930 (Col-

orado Maple Aphid) and P. negundinis (Thomas, 1878)

(Boxelder Aphid) are the only Nearctic species within

the genus Periphyllus van der Hoeven, 1863 (Hemiptera:

Aphididae: Chaitophorinae) (Blackman & Eastop 2019).

Apterous and alate viviparous females of these species

were extensively collected, described and reported by

entomologists throughout the United States and Canada

(Gillette & Palmer 1930; Knowlton 1947; Essig & Ab-

ernathy 1952; Palmer 1952; Richards 1972). However,

the sexual morphs of these species seem to be extremely

rarely collected and their detailed description is still lack-

ing (Blackman & Eastop 2019). In particular, the male

of P. americanus was shortly described, as P. palmerae

Knowlton, 1947, the oviparous female of P. brevispino-

sus Was mentioned by Palmer (1952), whereas the brief

description of sexuales of P. negundinis was provided by

Essig and Abernathy (1952).

In the present study, based on the specimens deposited

in the Natural History Museum, London, UK, we re-de-

scribe or describe all known sexuales of Nearctic species

of the genus Periphyllus, except the oviparous female of

P. americanus, which remains unknown. In addition to

Received: 11.01.2020

Accepted: 30.03.2020

these three native species, three non-indigenous species

of the genus Periphyllus are also distributed in North

America: P. californiensis (Shinji, 1917), P. lyropictus

(Kessler, 1886), and P. testudinaceus (Fernie, 1852). Ac-

cording to Foottit et al. (2006), although P. aceris (Lin-

naeus, 1761) has been recorded by numerous authors as

introduced to North America, it seems that those records

refer to other species. As Periphyllus is a highly polymor-

phic genus, we provide original keys to differentiate all

known sexuales of native and non-native species of this

genus, associated with maples in North America.

MATERIAL AND METHODS

The specimens were examined using a Nikon Ni-U light

microscope equipped with a phase contrast system. The

drawings of the morphological details were done free-

hand on a Nikon Ni-U light microscope using a camera

lucida. In each drawing, the left side represents dorsal

view and the right side represents ventral view. On the

dorsal side only dorsal setae are shown and on the ventral

side only ventral setae are shown.

The measurements were done according to Black-

man & Eastop (2019).

Corresponding editor: X. Mengual

Published: 19.04.2020

96 Joanna Trela et al.

Abbreviations for morphological terms

BL = body length (from anterior border of

the head to the posterior border of anal

plate)

BW = greatest body width across middle of

abdomen

ANT = antenna or its length

ANTI-VI = antennal segments I-VI or their lengths

(ratios between antennal segments are

simply given as e.g., ‘VI-III’)

LSANTII = length of longest seta of ANT II

BD Il = basal articular diameter of ANT III

BASE = basal part of the last antennal segment

or its length

PT = processus terminalis of the last

antennal segment or its length

ARS = apical segment of rostrum or its length

FEMORA III = hind femora length

TIBIA III = hind tibia length

HT II = second segment of hind tarsus or its

length

ABD I-VIII_ = abdominal tergites I-VIII

Institutional abbreviations

NHMUK = Natural History Museum, London, UK

RESULTS

Periphyllus americanus (Baker, 1917)

Baker, 1917: 428

Fig. 1

This species 1s widely distributed in the United States

and Canada on several species of maples (Blackman &

Eastop 2019). Specifically, it is known in Colorado, Con-

necticut, Florida, Idaho, Maine, Massachusetts, New

York, North Carolina, Pennsylvania, Utah, Washington

and Wyoming (USA), and in British Columbia, New

Brunswick, Nova Scotia and Quebec (Canada) and its

recorded host plants are Acer floridanum, A. glabrum,

A. grandidentatum, A. pseudoplatanus, A. saccharinum,

A. saccharum (Essig & Abernathy 1952; Palmer 1952;

Richards 1972; Smith & Parron 1978; Knowlton 1983).

Material examined. UNITED STATES, Utah, Ogden,

19 October 1958, G. F. Knowlton leg., 1 alate male.

Alate male (Fig. 1). Colour in life: unknown; mounted

specimens with head, antennae, pronotum, sclerites, si-

phunculi and genitalia dark. Legs dark with basal part of

femur slightly paler. Body 2.92 mm long and 1.02 mm

width. Head with 4—6 pairs of long fine, pointed setae

0.16—0.22 mm long (Fig. la). ANT 6-segmented, 2.12—

Bonn zoological Bulletin 69 (1): 95—103

2.15 mm long (Fig. 1b), reaching ABD VI, 0.71-0.73 x

BL. ANT IV 1.50—-1.56 ANT V; ANT V always short-

er than ANT VI; PT 2.76—-3.00 x BASE; other antennal

ratios: VI:IIT 0.70-0.71, V:I 0.47—-0.48, IV:II 0.72-

0.74. ANT I with 4-8 setae, ANT II with 3-4 setae,

ANT III 0.67—0.70 mm long with 11-13 setae (7-8 long

pointed setae and 4—S thick pointed setae), ANT IV 0.50—

0.51 mm long with 5—6 setae (3-4 long pointed setae and

1—2 thick pointed setae), ANT V 0.32-0.34 mm long

with | setae, BASE 0.12—0.13 mm long with 2 setae, PT

0.36 mm long with 3 apical setae. ANT setae: fine, point-

ed, up to 0.1 mm long; thick, pointed up to 0.025 mm

long. ANT III setae 0.01-0.10 mm long. LS ANT III

2.5 x BD III. The whole ANT III—V covered by rounded

secondary rhinaria: ANT HI with 59-63 rhinaria, ANT

IV with 18-32 rhinaria, ANT V with 8 rhinaria. Rostrum

reaching hind coxae. ARS 0.13 mm long, 0.18-0.19 x

ANT III and 0.76—0.81 x HT II, with 4 accessory setae

(Fig. 1c). Legs with numerous, fine and pointed setae,

0.05—0.23 mm long. FEMORA III 0.90 mm long. TIBIA

II 1.30 mm long with numerous short spinules distributed

on distal 1/3 of tibiae. HT IH 0.16—0.17 mm long. Empo-

dial setae spatulate; first tarsal chaetotaxy 5:5:5 (Fig. 1d).

Fore wings with normal venation (Fig. le). Abdominal

tergites membranous, with large fused spinal sclerites,

pleural sclerites very small, irregularly placed, marginal

sclerites oval. Abdominal setae 0.07—0.22 mm long; mar-

ginal sclerites with 4—5 setae (0.1—0.2 mm long), pleu-

ral sclerites with 0-1 setae (0.11-0.17 mm long), spinal

sclerites with 4-5 setae (0.07—0.22 mm long) (Fig. 1f).

Siphunculi 0.17 mm long and 0.18—0.19 width, truncate,

reticulated on the whole length, with developed flange

and coalescent with each marginal sclerite of ABD VI

(Fig. 1g). Cauda 0.08 mm long, broadly rounded, with

8 setae (4 long and 4 short setae) 0.06—-0.13 mm long

(Fig. 1h). Genitalia well developed, strongly sclerotized

with roundish, lobate parameres, covered by numerous

spine—like setae. Basal part of phallus rectangular, short-

ened, with numerous short spinules (Fig. 11).

Periphyllus brevispinosus (Gillette & Palmer, 1930)

Gillette & Palmer, 1930: 546-547

Figs 2-3

This species 1s known western North America on Acer

glabrum (Blackman & Eastop 2019); specifically, it has

been recorded from Colorado, Idaho, Oregon, Utah,

Washington, and Wyoming (USA) and Alberta and Brit-

ish Columbia (Canada) (Essig & Abernathy 1952; Palm-

er 1952; Richards 1972; Smith & Parron 1978; Knowlton

1983).

Material examined. UNITED STATES, Colorado, Sky-

way, 15 September 1956, on Acer glabrum, Hottes &

H.R.L. leg., 2 alate males, 4 oviparous females, BM 1984

340.

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Sexuales of Nearctic species of Periphyllus 97

Alate male (Fig. 2). Colour in life: unknown; mount-

ed specimens with head, pronotum, sclerites, siphun-

culi and genitalia dark. Legs light dark with basal part

of femur and middle part of tibiae slightly paler. ANT

I-VI dark with ANT III-IV slightly paler at base. Body

2.25—2.37 mm long and 0.80—0.87 mm width. Head with

1mm

0.1 mm

4—6 pairs of long fine, pointed setae 0.09—-0.16 mm long

(Fig. 2a). ANT 6-segmented, 2.00 mm long (Fig. 2b),

almost reaching ABD VI, about 0.84 x BL. ANT IV

1.30-1.40 ANT V; ANT V about as long as ANT VI; PT

2.30-2.41 x BASE; other antennal ratios: VI:III 0.62—

0.65, V:III 0.45—0.49, IV:IIT 0.65—0.69. ANT I with 7 se-

Fig. 1. Periphyllus americanus (Baker, 1917), alate male. a. Head. b. Antenna. c. Apical segment of rostrum. d. Hind tarsus. e. Fore

wing. f. Abdomen. g. Siphunculus. h. Cauda. i. Genitalia.

Bonn zoological Bulletin 69 (1): 95—103

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98 Joanna Trela et al.

tae, ANT II with 7 setae, ANT III 0.63—0.69 mm log with

7-10 setae, ANT IV 0.41-0.48 mm long with 5-7 setae,

ANT V 0.31-0.34 mm long with 3—5 setae, BASE 0.12—

0.13 mm long with 2 setae, PT 0.29-0.30 mm long with

3 apical setae. ANT setae fine, pointed, 0.03—0.07 mm

long. LS ANT III 1.75—2.33 x BD HI. The whole ANT

1mm

III—V covered by rounded secondary rhinaria: ANT III

with 25—43 rhinaria, ANT IV with 13—23 rhinaria, ANT

V with 13-18 rhinaria. Rostrum reaching middle coxae.

ARS 0.11 mm long, 0.15—0.17 x ANT HI and 0.64—0.68 x

HT I, with 4 accessory setae (Fig. 2c). Legs with nu-

merous fine and pointed setae 0.02—0.09 mm long. FEM-

Fig. 2. Periphyllus brevispinosus Gillette & Palmer, 1930, alate male. a. Head. b. Antenna. ec. Apical segment of rostrum. d. Hind

tarsus. e. Fore wing. f. Abdomen. g. Siphunculus. h. Cauda. i. Genitalia.

Bonn zoological Bulletin 69 (1): 95—103

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Sexuales of Nearctic species of Periphyllus 99

ORA II 0.73-0.77 mm long. TIBIA III 1.02—1.05 mm __ with large fused spinal sclerites, pleural sclerites very

long. HT II 0.16-0.17 mm long. Distal part of tibiae small, irregularly placed, marginal sclerites oval; scler-

with many short spinules; empodial setae spatulate; first 1tes on ABD VII—VIII fused in cross bars. Abdominal

tarsal chaetotaxy 5:5:5 (Fig. 2d). Fore wings with nor- — setae 0.06—0.18 mm long; marginal sclerites with 2—5

mal venation (Fig. 2e). Abdominal tergites membranous, — setae (0.09-0.18 mm long), pleural sclerites with 0-1

Fig. 3. Periphyllus brevispinosus Gillette & Palmer, 1930, oviparous female. a. General view. b. Antenna. c. Apical segment of

rostrum. d. Hind tibia with pseudosensoria and tarsus. e. Siphunculus. f. Cauda.

100 Joanna Trela et al.

setae (0.07-0.13 mm long), spinal sclerites with 2-3

(0.06—0.17 mm long) setae. Siphunculi 0.11-0.13 mm

long and 0.11 width, truncate with developed flange, re-

ticulated, except at base where reticulation transforms

into flattened cells and coalescent with each marginal

sclerite of ABD VI (Fig. 2g). Cauda 0.06—0.07 mm long,

broadly rounded, with 14-15 setae 0.05—0.10 mm long

(Fig. 2h). Genitalia well developed, strongly sclerotized

with roundish, lobate parameres, covered by numerous

spine—like setae. Basal part of phallus triangular, short-

ened, with numerous short spinules (Fig. 21).

Oviparous female (Fig. 3). Colour in life: unknown;

mounted specimens with head, legs, scleroites and si-

phunculi dusky. ANT dusky with apices of ANT III-V

and ANT VI dark. Body 2.32—2.60 mm long and 1.40-—

1.55 mm width, pear-shaped (Fig. 3a). Head with 4 pairs

of fine, pointed setae 0.06—0.19 mm long. ANT 6-seg-

mented, 1.27—1.40 mm long (Fig. 3b), reaching ABD

I-IV, 0.48-0.59 x BL. ANT IV 1.20-1.56 ANT V; ANT

V always shorter than ANT VI; PT 0.92-1.16 x BASE;

other antennal ratios: VI:III 0.54—0.67, V:III 0.35—0.50,

IV: 0.50-0.65. ANT I with 4-8 setae, ANT II with 3-5

setae, ANT III 0.40-0.48 mm long with 7—9 setae, ANT

IV 0.24—-0.28 mm long with 3-6 setae, ANT V 0.16—

0.20 mm long with 34 setae, BASE 0.12—0.14 mm long

with 2 setae, PT 0.13—0.15 mm long with 3 apical setae.

ANT setae fine, pointed, 0.03—0.07 mm long. LS ANT III

1.25—2.33 x BD II. Rostrum almost reaching hind cox-

ae. ARS 0.10-0.11 mm long, 0.20-0.25 x ANT HI and

0.66—0.76 x HT II with 4 accessory setae (Fig. 3c). Legs

with numerous fine and pointed setae, 0.03—0.10 mm

long. FEMORA II 0.39-0.59 mm long. TIBIA HI 0.70—

0.80 mm long. HT II 0.13—0.16 mm long. Hind tibiae

with 69-150 8-shaped pseudosensoria distributed on the

whole length of tibiae. Distal part of tibiae with few short

spinules; empodial setae spatulate; first tarsal chaeto-

taxy 5:5:5 (Fig. 3d). Abdominal tergites membranous.

Abdominal setae 0.05—0.20 mm long; marginal sclerites

with 2—5 setae (0.05—0.20 mm long), pleural and spinal

sclerites with 3 setae (0.05—0.15 mm long). Siphunculi

0.11—0.12 mm long and 0.12—0.13 mm width, truncate,

with weakly visible 2—3 rows of reticulations which at

base transform into flattened cells and well-developed

flange (Fig. 3e). Cauda 0.09-0.10 mm long, broadly

rounded, with 20-25 pointed setae (Fig. 3f).

Periphyllus negundinis (Thomas, 1878)

Thomas, 1878: 10

Figs 4-5

Periphyllus negundinis is the most widely distributed in

North America among Nearctic species of Periphyllus

(Blackman & Eastop 2019); it has been recorded from

Alabama, Arizona, California, Colorado, Connecticut,

Delaware, District of Columbia, Florida, Illinois, Indiana,

Bonn zoological Bulletin 69 (1): 95—103

Iowa, Kansas, Louisiana, Maine, Maryland, Michigan,

Minnesota, Missouri, Mississippi, Montana, Nebraska,

New Jersey, New Mexico, New York, North Carolina,

North Dakota, Ohio, Oregon, Pennsylvania, South Car-

olina, South Dakota, Texas, Utah, Virginia, Washington,

West Virginia, Wisconsin, and Wyoming (USA); Alberta,

British Columbia, Manitoba, New Brunswick, Nova Sco-

tia, Ontario, Prince Edward Island, Quebec and Saskatch-

ewan (Canada) and Mexico (Mexico), being its main host

plants Acer negundo (Essig & Abernathy 1952; Palmer

1952; Richards 1972; Smith & Parron 1978; Knowlton

1983); also collected from A. pseudoplatanus (Palmer

1952).

Material examined. CANADA, Manitoba, Winnipeg,

25 September 1963, on Acer negundo, A. G. Robinson

leg., 1 oviparous female, BM 1964 630; 1 October 1964,

on Acer negundo, A. G. Robinson leg., 2 apterous males,

BM 1965 33.

Apterous male (Fig. 4). Colour in life: dark green (Es-

sig & Abernathy 1952); mounted specimens with body

pale with dusky sclerites; head, pronotum and genitalia

dark. Antennae dark with basal part of ANT III paler.

Legs dark with basal part of femora slightly paler. Body

1.60-1.72 mm long and 0.82-0.85 mm width. Head

with 6—8 pairs of long fine, pointed setae 0.10—-0.13 mm

long (Fig. 4a). ANT 6-segmented, 1.20—1.27 mm long

(Fig. 4b), reaching ABD IV, 0.70-0.79 x BL. ANT IV

the same or slightly longer than ANT V; ANT V always

shorter than ANT VI; PT 1.81—2.20 x BASE; other an-

tennal ratios: VIII 0.70—0.83, V:HI 0.51—0.55, IV:HI

0.54—0.72. ANT I with 4-5 setae, ANT I with 3-4 se-

tae, ANT III 0.35—0.36 mm long with 7-8 setae, ANT

IV 0.19-0.26 mm long with 3-4 setae, ANT V 0.18—

0.20 mm long with 2-3 setae, BASE 0.09-0.11 mm long

with 2 setae, PT 0.19—0.20 mm long with 3 apical setae.

ANT setae fine, pointed, 0.02—0.13 mm long. LS ANT

Il 3.25-4.00 x BD II. The whole ANT HJ—V covered

by rounded secondary rhinaria: ANT III with 16—23 rhi-

naria, ANT IV with 6-11 rhinaria, ANT V with 3—4 rhi-

naria. Rostrum reaching hind coxae. ARS 0.12—0.13 mm

long, 0.34—0.36 x ANT III and 0.75-0.76 x HT I, with

4 accessory setae (Fig. 4c). Legs with numerous fine and

pointed setae 0.06—0.16 mm long. FEMORA III 0.57—

0.58 mm long. TIBIA II 0.77-0.81 mm long. HT II

0.16-0.17 mm long. Distal part of tibiae with few short

spinules; empodial setae spatulate; first tarsal chaetotaxy

5:5:5 (Fig. 4d). Abdominal tergites membranous, with

large, fused spinal sclerites, pleural sclerites smaller than

spinal, irregularly placed, fused, marginal sclerites oval.

Abdominal setae 0.03—0.21 mm long; marginal sclerites

with 4-7 setae (0.03—0.21 mm long), pleural sclerites

with 1-3 setae (0.08—0.15 mm long), spinal sclerites with

2-6 setae (0.07-0.14 mm long) (Fig. 4a). Siphunculi

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Sexuales of Nearctic species of Periphyllus 101

0.17—0.18 mm long and 0.07—0.12 mm width, stump—

shaped with 2 rows of reticulation and developed flange

(Fig. 4e). Cauda 0.04—0.05 mm long, broadly rounded,

with 10 setae (Fig. 4f). Genitalia well developed, strong-

ly sclerotized with roundish, lobate parameres, covered

by numerous spine—like setae. Basal part of phallus

hook—shaped, shortened, with numerous short spinules

(Fig. 4g).

Oviparous female (Fig. 5). Colour in life: mottled green,

becoming darker as eggs mature within body (Essig &

Abernathy 1952); mounted specimens with body pale

with apices of ANT IV—V, ANT VI, tarsi and HTII dark.

Body 2.55 mm long and 1.20 mm width, egg-shaped

(Fig. 5a). Head with 5-7 pairs of fine, pointed setae 0.12—

0.20 mm long. ANT 6-segmented 1.30-1.35 mm long

(Fig. 5b), reaching ABD HI-IV, 0.50—0.52 x BL. ANT IV

slightly longer than ANT V; ANT V always shorter than

ANT VI; PT 2.27 x BASE; other antennal ratios: VI-III

0.58-0.69, V:IIT 0.55—0.61, [V:III 0.58—0.69. ANT I with

6-8 setae, ANT II with 4—5 setae, ANT III 0.36 mm long

with 8-10 setae, ANT IV 0.21—0.25 mm long with 3-4

0.2 mm

0.1 mm

Fig. 4. Periphyllus negundinis (Thomas, 1878), apterous male. a. General view. b. Antenna. c. Apical segment of rostrum. d. Hind

tarsus. e. Siphunculus. f. Cauda. g. Genitalia.

Bonn zoological Bulletin 69 (1): 95—103

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102 Joanna Trela et al.

setae, ANT V 0.20—-0.22 mm long with 3-4 setae, BASE

0.11 mm long with 2 setae, PT 0.25 mm long with 3 api-

cal setae. ANT setae fine, pointed, 0.02—0.12 mm long.

LS ANT III 3 x BD III. Rostrum reaching middle coxae.

ARS 0.13 mm long, 0.36 x ANT HI and 0.72—0.76 x HT

II with 4 accessory setae (Fig. 5c). FEMORA TI 0.64 mm

long. TIBIA III 0.89-0.90 mm long. HT II 0.17—0.18 mm

long Legs with numerous fine and pointed setae 0.04—

0.15 mm long. Hind tibiae with 120-130 rounded pseu-

dosensoria, sometimes fused and distributed on the whole

Vy Vis rf

0.1mm

length of tibiae except basal and distal part. Distal part of

tibiae with few short spinules; empodial setae spatulate;

first tarsal chaetotaxy 5:5:5 (Fig. 5d). Abdominal tergites

membranous. Abdominal setae numerous, fine, regularly

placed all over abdomen, 0.06—0.22 mm long. Siphunculi

0.10 mm long and 0.15—0.16 mm width, stump-shaped,

with 3-4 rows of reticulations and well-developed flange

(Fig. 5e). Cauda 0.08 mm long broadly rounded, with 12

setae 0.05—0.15 mm long (Fig. 5f).

Fig. 5. Periphyllus negundinis (Thomas, 1878), oviparous female. a. General view. b. Antenna. ec. Apical segment of rostrum. d.

Hind tibia with pseudosensoria and tarsus. e. Siphunculus. f. Cauda.

Bonn zoological Bulletin 69 (1): 95—103

©ZFMK

Sexuales of Nearctic species of Periphyllus 103

Key to males of species of Periphyllus (native and in-

troduced) known from the Nearctic

Dee FAMCIOUS: 2.20 ese bern. cine ARAN P. negundinis

Sie PV ATC oct canst lescsta Mets tate eek are alae, onsh ee ssa ace 2

2). SHind tibiag-unitornily darker. -! fe ea tape ecdee 3

— Hind tibiae pale, dusky or dark only on base and

PCE), An te BN oe thee A i ers 2 ole 4

3. Siphunculi reticulated on the whole length, PT 2.76—

SEUOU SAS LM A Boneh Mh a) P. americanus

— Siphunculi reticulated on apical 2/3, imbricated to

wider base, PT > 3.0 x BASE ........ P. californiensis

4. Hind tibiae pale or dusky. Cauda helmet-shaped .....

0. seme nied Le TaN aoe M9), ow P. lyropictus

— Hind tibiae dark on base and apex, pale at middle part.

Cauda broadly-rounded ..0.......0.0000ccccecceeeeeeeeees 5

5. PT 2.30-2.41 x BASE ........0. P. brevispinosus

— PT 5.70—5.90 x BASE .........0..0000.. P. testudinaceus

Key to oviparous females of the species of Periphyllus

(native and introduced) known from the Nearctic

1. Cauda helmet-shaped .......000..000000000.. P. lyropictus

— Cauda broadly rounded ............00c ccc eeeeeeeee 2

Ye 2A POSS ae 27 61 UNAS 6 V2 hed BAe rene seer ne ee me 3

— PT 3.00—3.50 x BASE ........00...000. P. testudinaceus

3. Body pear-shaped and dusky with dark ANT VI and

apices of ANT IN-V ..........00 ce. P. brevispinosus

— Body egg-shaped and pale with dark tarsi, hind

tibiae, ANT VI, and apices of ANT IV-V .............. 4

4. Siphunculi pale. On Acer negundo or

A, pSCudloplatanus ........0ccc cece cess P. negundinis

— Siphunculi dark. On Asian ornamental maples ........

Rac NectacnssacarranceneM dace, caste #eonra ane Mad ata 44.524, P. californiensis

Bonn zoological Bulletin 69 (1): 95—103

Acknowledgements. We would like to express our thanks to

Jon Martin and Paul A. Brown, the Natural History Museum,

London, UK for the loan of the slides and for all of their help

during the visit to the collection of the NHMUK. We are also

grateful to the Editor and to the two anonymous reviewers for

all valuable comments during the review process.

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www.aphidsonworldsplants.info/ [last accessed on Decem-

ber 20, 2019]

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California Press, Berkeley and Los Angeles, 166 pp.

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©ZFMK

BHL

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Bonn zoological Bulletin 69 (1): 105-110

2020 - Al-Sheikhly O.F. et al.

https://do1.org/10.20363/BZB-2020.69.1.105

ISSN 2190-7307

http://www.zoologicalbulletin.de

Scientific note

urn:|sid:zoobank.org:pub: CDO9EF99-49F6-48DD-B 132-5567EBF50815

New distribution range of the vulnerable wild goat

(Capra aegagrus Erxleben, 1777) (Artiodactyla: Bovidae)

to the south of its known extant in Iraq, with notes on its conservation

Omar F. Al-Sheikhly” *, Mukhtar K. Haba’, Ali N. Al-Barazengy* & Nadheer A. Fazaa‘*

' Department of Biology, College of Science, University of Baghdad, Baghdad, Iraq

?4Department of Biology, College of Science for Women, University of Baghdad, Baghdad, Iraq

>Center of Sustainable Management for Natural Ecosystem, Iraqi Ministry of Environment, Baghdad, Iraq

“Corresponding author: Email: alsheikhlyomar@gmail.com

'urn:lsid:zoobank.org:author:D8ADSFEE-E7FC-4E0C-8256-4B5E84AFC238

> urn:|sid:zoobank.org:author:C6B7D8FD-A9F6-48C0-89F0-34 1 8FEEDC969

3urn:Isid:zoobank.org:author:6B33B3E3-8A91-48D1-AB13-88A82B5A0FC1

*urn:Isid:zoobank.org:author:2F5EA9F7-COF8-4A0D-99CC-2D9 1 ESEEFEF9

Abstract. The wild goat (Capra aegagrus Erxleben, 1777) is a vulnerable ungulate confined to the rocky slopes of the

Zagros Mountains forest steppes ecoregion in northern and northeastern Iraq (Kurdistan Region). Scattered populations

had been reported from 31 sites distributed mainly in four Iraqi northern provinces; however, the species’ current zoogeo-

graphical distribution and population trends are enigmatic. From August 2017 to April 2018, four new sightings of the

wild goat were obtained from the foothills of the Zagros Mountains along the eastern and southeastern Iraq-Iran internati-

onal borders. These new localities represent a new distribution range to the southernmost of the species’ known extant in

Iraq. Moreover, the newly discovered wild goat populations in eastern and southeastern Iraq almost certainly originated

from the western Iranian populations assigned to the Capra a. aegagrus subspecies. Besides poaching, newly documented

threats such as trapping and young capturing which severely affect the wild goat populations in Iraq are discussed.

Key words. Bovidae, Capra aegagrus, protected areas, ungulates, wild mammals of Iraq.

INTRODUCTION

The wild goat (Capra aegagrus Erxleben, 1777) is a

threatened ungulate restricted to the mountainous habitats

of central Afghanistan, southern Pakistan, west through

Iran, western Turkmenistan, northern Irag, the Caucasus

region (Armenia, Azerbaijan, northeastern Georgia, and

southern Russia), and southwestern Turkey (Weinberg

et al. 2008; Macar & Gurkan 2009). In Arabia, the spe-

cies once occurred in Lebanon and Syria, United Arab

Emirates, and Jordan, but 1s now extinct in these regions

(Harrison & Bates 1991; Grubb 2005).

In Iraq, the species inhabits the rocky slopes, moun-

tain gorges, wooded hills, coniferous and Mediterranean

shrubland of the Zagros Mountains mainly in the ex-

treme northern and northeastern Iraq (Kurdistan Region)

(Al-Sheikhly et al. 2015). Previously, it has been report-

ed from Shanidar caves, mountain slopes near Zawitha,

Sarsank and Amadiya in Dohuk province, Baradust

Mountain, Barzan area, Zagarta Mountain, Shaglawa,

Harir Dagh, Rawanduz, Safin Dagh and Bekma Dam in

Received: 23.07.2019

Accepted: 31.03.2020

Erbil province, recorded also from Hazar Mard, Chem-

chemal and Derbendi Khan in Sulaimaniyah province

(Harrison & Bates 1991). Scattered small populations

have been reported from Barzan area, Zararan (Zerara),

foothills near Dukan Lake, Peramagroon, and Qara Dagh

mountains during 2010-2012 (Al-Sheikhly 2012b; Raza

et al. 2012: Haba 2013; Raza 2013). More recently, a

small population of wild goat has been found in Buzan

Valley in the Alqosh Mountain, a newly discovered local-

ity for this species in Nineveh province in northern Iraq

(Al-Barzangi et al. 2015). Furthermore, wild goats have

been reported for ten Key Biodiversity Areas (KBAs) in

the mountain chains of the Kurdistan Region in northern

Iraq (Nature Iraq 2017) (Fig. 1). The wild goat is listed

as Vulnerable (VU) by the International Union for Con-

servation of Nature (IUCN) Red List due to rapid popu-

lation decline attributed to over-exploitation (mainly by

poaching), competition for gazing areas with domestic

livestock, disturbance, and habitat destruction (Weinberg

et al. 2008).

Corresponding editor: E. Barmann

Published: 19.04.2020

106 Omar F. Al-Sheikhly et al.

New sites for wild goat in eastern

and southeastern Iraq

Four new sites for wild goat have been recently identified

within the Zagros Mountains forest steppes ecoregion

along Iraq-Iran eastern and southeastern international

borders, the foothills of (4) Zurbattyah (Zurbatia), (11)

Kani Sakht, (111) Kazaneah, and (iv) Al-Teeb (red-circled

sites in Fig. 1).

The foothills of Zurbatiyah (site 2 in Fig. 1) and Kani

Sakht (site 3 in Fig. 1) are extending to the northeast

of Badrah district in Wasit province, Kazaneah (site 1

in Fig. 1) extends to the southeast of Mandli district in

Diyala province (ca. 140 km far from Baghdad), and

Al-Teeb (site 4 in Fig. 1) extends to the to the north of

Myssan province. The general landscape of sites 1-3 is

characterized by rocky slopes, rocky outcrops and veg-

etated hills, while site 4 is mainly dominated by broad

rocky and gypsum valleys, arid plains, and grasslands.

These habitats seem to provide food resources, water

streams for drinking, hiding places, grazing areas, and

possibly mating sites for wild goats.

JORDAN

4000 m

3000 m

2500 m +

2000 m +

1500m +

1000 m —+—

750 m

500 m

400m -—

300 m

SAUDI ARABIA

Our intensive interviews with local hunters and villag-

ers indicated that several scattered herds of 15—80 wild

goats are frequently chased and persecuted by local hunt-

ers along the foothills of eastern and southeastern Iraq

where small resident populations may be present. In Au-

gust 2017, two adult males and an adult female with twin

offspring (ca. 3 weeks old) were shot in the rocky slopes

of Zurbatiyah foothills by local hunters (Fig. 2b). In Feb-

ruary 2018, three adult males were shot in the foothills of

Kani Sakht (Fig. 2e—f), and four adult males were shot in

the foothills of Kazaneah in November 2018 (Fig. 2g).

Recent reliable reports indicate that scattered nomadic

herds of wild goats were frequently observed and chased

by local hunters in the foothills of Al-Teeb in March-

April 2018 which represents the southernmost sighting of

this species in Iraq (BM AI-Tael, pers. comm. 2019). All

of the examined wild goat male carcasses showed a rus-

set-brown pelage with black stripes on the back, around

the withers, on the front of legs and on the edge of the

pale-brown belly, and black foreheads with long black

beards and long horns curved backwards.

Awiia Goat Capra aegagrus Literature records in Iraq

36°49'N 44°13'E

36°53'N 43°9'E

43°20'E

43°29'E

44°23'E

4P7'E

4e°7'E

44°19'E Harrison & Bates 1991

44°22'E

44°30'E

44°19'E

4416

4548'E

44°57'E

45°53'E

4P TE

44°12'E

44°50'E

1. Shanidar caves

2. mountains near Zawitha

3. Sarsank

4, Amadiya

5. Baradust Mountain

6. Barzan area

7. Zagarta Mountain

8. Shaglawa

9. Harir Dagh

10. Rawanduz

11. Safin Dagh

12, Bekma Dam

13. Hazar Mard

14. Chemchemal

15. Derbendi Khan

16, Barzan area

17. Zararan area

18. foothills near Dukan Lake 36° 4'N

19. Peramagroon Mountain 35°43'N 45°6'E ered aay

20.QaraDagh Mountain ss 35°43'N = 45°23'E AL Fa

21. Algosh Mountain 36°46'N 43°9'E Al-Barzangi et al. 2015

22. Dure area 43°30'E

23. Barzan area 44°7'E

24. Bradost Mountain 44°23'E

25. Sakran Mountain 44°58'E

26. Assos Mountain i 45°7'E

27. Permagroon Mountain 35°43'N 45°16'E

28. Qara dagh Mountain 35°3'N 45°23'E

29. Darbendikhan area 35° 8'N = 45°53E

30. Ahmed Awa 35°19'N 46°6'E

31. Hawraman area 35°S'N 46° BE

Raza et al. 2012

Haba 2013

Nature Iraq 2017

\.@ Wild Goat Capra aegagrus recent records in Iraq

33°36'N 45°53'E

33°14'N 46°10'E

33°18'N 46° 4'E

32°27'N §47°17'E

. Kazaneah

2. Zurbatiyah

3. Kani Sakht

4, Al-Teeb

[] Kurdistan Regional Government (KRG)

[] Nature Reserve

KUWAIT

400 Kilometers

Fig. 1. Literature and recent records of Wild goat Capra aegagrus Erxleben, 1777 in Iraq.

Bonn zoological Bulletin 69 (1): 105-110

©ZFMK

New distribution range of C. aegagrus Erxleben, 1777 to the south of its known extant in Iraq 107

The current zoogeographical range of wild goat in Iraq

is represented by a patchy distribution pattern of scat-

tered populations of the subspecies C. a. aegagrus which

mainly exist in northern and northeastern Iraq (Kurdistan

Region) (Al-Sheikhly & Haba 2014; Al-Sheikhly et al.

2015). However, the Iraqi largest sedentary populations

of wild goat are known from Peramagroon, Qara Dagh,

and Barzan mountains where they are protected by the

Kurdistan Forestry Police and preserved by tribal com-

munities for decades 1n the latter mountain (Raza et al.

2012; Haba 2013). The Forestry Police of Mergasur esti-

mated more than 1000 wild goats thriving in Barzan area,

from which over 200 individuals had died due to the out-

break of goat plague or Peste des Petits Ruminants (PPR)

in August 2010 and in 2011 (Nature Iraq 2017).

During a field expedition on 26" of August 2017, a

herd of 94 wild goats (46 adult males; 31 adult females;

17 juveniles) was counted using point count method

(e.g., Gundogdu 2011) in an area of 400 ha (0.235 indi-

vidual/ha) of wooded mountain slopes in Zerara (Barzan

area) in Erbil province in northern Iraq (Fig. 2c—d). Adult

males (> 2-3 years) were representing ca. 50% of the ob-

served population (Fig. 2a); a ratio supported by inter-

views with Kurdish villagers and forestry policemen. In

spite of surveying only a small proportion of Zerara area,

our count was higher than the previously known estimate

(80 individuals/summer 2010, Nature Iraq 2017). The in-

crease of wild goat population size in Barzan area may be

attributed to the protection provided by the local commu-

nities and Kurdistan Regional Government (KRG); yet,

further monitoring may reveal better estimates. However,

our newly discovered wild goat localities in eastern and

southeastern Iraq are distant ca. 200 km away from the

largest resident populations in northern Kurdistan and

represent the southernmost distribution range of the spe-

cies in Iraq.

The newly discovered wild goat populations in east-

ern and southeastern Iraq most certainly originated from

Iranian populations that inhabit the Zagros Mountains of

western Iran. Wild goat is widely distributed in Iran; it

has been recorded from 31 province s and reported from

190 protected areas throughout the country (Karami et al.

2008; Yusefi et al. 2019). In Ilam province in western Iran,

the Kolan (Golan) Protected Area (33°23’ N, 46°9’ E)

and Bina and Byar No-hunting area (33°41’ N, 45°56’ E)

are the most adjacent protected areas to our sites 1-3,

while Dinar Kuh (Dinar Kooh) (32°50’ N, 47°20’ E) Pro-

tected Area is the closest protected area to our site 4 (Dar-

vishsefat 2006; Yusefi et al. 2019; UNEP-WCMC 2020)

(Fig. 1). However, Dehloran city is placed between Dinar

Kuh Protected Area and site 4; therefore, wild goats are

probably using the free area of ca. 7 km of Iraq-Iran inter-

national border to reach site 4. Furthermore, the free area

of the international border seems important for wild goat

to move from well protected areas and no-hunting zones

in Iran to Iraq.

Bonn zoological Bulletin 69 (1): 105-110

In Iran, the mating season of wild goat starts in mid-fall

(October-December) and in November in southeastern

Turkey, when both sexes aggregate in herds and males’

courtship display starts (Korshunov 1994; Ziaie 2008;

Esfandabad et al. 2010). The dominant large adult males

push the young and sick goats out of the herd which mi-

grate to adjacent habitats in search for new hiding and

grazing places. Furthermore, after mating, the large adult

males move to new areas to spend the summer (Gundog-

du 2011). The increased conspecific competition among

wild goat males may force some individuals from the

Iranian western populations to migrate to eastern and

southeastern Iraq. Moreover, as we mentioned before, the

high numbers of different-aged wild goat males that were

recently hunted in eastern and southeastern Iraq seems to

support the claim that migrated animals survived the se-

vere poaching and were able to establish new populations

in eastern and southeastern Iraq. In addition, wild goat

females with recently born young are frequently chased

and trapped by local poachers, which confirms the breed-

ing of this species within the territory of Iraq. Therefore,

urgent and increased conservation and protection actions

should be taken to save these new populations.

Esfandabad et al. (2010) suggested altitudinal and sea-

sonal migration behaviors of wild goat as an adaptation

to survive in extreme temperature and to make use of

available resources throughout the year. In winter (Jan-

uary—March), the low accessibility to food resources

due to a thick layer of snow at higher elevations forc-

es the animals to use lower altitudes where they become

exposed to natural predators and poachers (Esfandabad

et al. 2010).

It is worth noting that the wild goat population of west-

ern Iran was assigned to the nominotypical subspecies

C. a. aegagrus Erxleben, 1777, while the eastern and

southeastern ones were assigned to C. a. blythi (Hume,

1875) (Ellerman & Morrison-Scott 1951; Heptner et al.

1988). Grubb (2005) synonymized both subspecies, and

therefore, only one subspecies (C. a. aegagrus) occurs in

Iran (Yusefi et al. 2019). Furthermore, the domestication

process of goats was intensively studied by Naderi et al.

using mtDNA (2007; 2008). The wild goat populations of

eastern and southeastern Iraq 1s therefore assigned to the

Iranian subspecies C. a. aegagrus.

Threats on the wild goat population in Iraq

Poaching

Hunting of wild goat has been identified as a major threat

on the species survival (Weinberg et al. 2008; Gundogdu

2011). The illegal hunting (shooting, trapping, and catch-

ing by dogs) is a major threat on the species in Iran which

increases during the rutting season in fall, when trophy

males are easier to detect by poachers (Ziaie 2008). The

wild goat population in Iraq had remarkably decreased

©ZFMK

108 Omar F. Al-Sheikhly et al.

due to excessive poaching compared to the 1920s (Hatt

1959; Al-Sheikhly 2012c). In northern Iraq (Kurdistan

Region), most of the wild goat populations were affect-

ed by habitat destruction and disturbance that occurred

during Iraq-Iran conflict in the 1980s (Al-Sheikhly et al.

2015). However, the hunting of wild goats was prohibit-

ed by the Kurdistan Regional Government in the 1990s

(Al-Barzangi et al. 2015). In eastern and southeastern

Iraq, the hunting of wild goats and other sympatric bo-

vid species is continued and seems to be uncontrolled by

the local authorities and warrants urgent governmental

protection. Two of our sites, Zurbatiyah and Al-Teeb

Fig. 2. a. Adult males wild goat Capra aegagrus Erxleben, 1777 grazing on rocky slopes of Zerara area in Erbil province in north-

ern Iraq. b. An adult male shot in Zurbatiyah foothills (red-circled site 2 in Fig. 1). e-d. Females with kids observed in Zerara area

in Erbil province in northern Iraq. e-f. Adult males shot in the foothills of Kani Sakht (site 3 in Fig. 1). g. An adult male shot in

the foothills of Kazaneah (site 1 in Fig. 1). h. Asiatic Mouflon Ovis orientalis gmelini shot in the foothills of eastern Iraq. i. A wild

goat kid captured from the foothills of eastern Iraq in order to be raised as a pet. Photos: a-d: ©Omar Al-Sheikhly; b—i: ©Basheer

Mohmmad AI-Taei.

Bonn zoological Bulletin 69 (1): 105-110

©ZFMK

New distribution range of C. aegagrus Erxleben, 1777 to the south of its known extant in Iraq 109

(Zubaidaat and Teeb Oasis) have national importance for

wildlife conservation. Both sites have been designated as

Key Biodiversity Areas (KBAs no. 57 and 67) respec-

tively and declared as nature reserves by the Ministry of

Environment of Iraq (Nature Iraq 2017; UNEP-WCMC

2020).

Besides wild goat, the Vulnerable Asiatic mouflon Ovis

orientalis gmelini (Blyth, 1841) (Fig. 2h) and the Vul-

nerable Persian goitered gazelle Gazella subgutturosa

(Guldenstaedt, 1780) are targeted by local hunters where

and whenever possible in order to be consumed as food

or raised as pets (Al-Sheikhly 2012a; c). Furthermore,

the Vulnerable Arabian Sand Gazelle G. marica (Thom-

as, 1897) probably exists in eastern and southeastern Iraq

(Fadakar et al. 2019). It is worth mentioning, that hunt-

ing the aforementioned species is banned by the Iraqi

Wild Animals Protection Law (no. 17 issued on 15" of

February 2010), but the weak enforcement encourages

hunters to pursuit their illegal quest. The local hunters

who are equipped with modern hunting rifles and fleets

of all terrains are extensively searching for wild bovids in

the foothills and steppes of eastern and southeastern Iraq

throughout the year, with extensive poaching occurring

mainly in winter and spring (January—June). Poaching of

wild goat in eastern and southeastern Iraq is extensive-

ly practiced in winter (seven males/November—Febru-

ary 2018) when wild goats seem to abandon the higher

grounds of the adjacent protected areas in western Iran to

retreat to lower altitudes in eastern and southeastern Iraq.

Trapping

In our recent investigation we found that trapping has

emerged as a newly documented threat on wild bovid

populations in Iraq. The solitary, nomadic, and rutting

wild goats, Asiatic mouflons, and Persian goitered ga-

zelles are ambushed and trapped by large nets fired from

net-modified rifles or taken by a long chase via motor-

cycles. The trapped animals are sold in the local animal

markets or exported to the neighboring Arabian countries

as pets. Our interviews with the local animal traders re-

vealed that the prices of the trapped animals are varying

based on sex and age. The price ranges from $300—500

for wild goat juveniles and adult female Persian goitered

gazelles, to $800—900 for adult female wild goats, and

$400-500 for adult male wild goats.

Capturing/collecting of young from the wild

Our interviews, personal communications and corre-

spondences with local hunters indicated that parturition

takes place in early April to mid July in the wild goat

populations of eastern and southeastern Iraq which seems

concurrent to those of western Turkmenistan (Korshunov

1994) and southeastern Turkey (Gundogdu 2011). At that

time, foot patrols of local trappers/collectors are search-

Bonn zoological Bulletin 69 (1): 105-110

ing for wild goat pregnant females and/or their new-

ly born not-weaned offspring in the rocky caverns and

foothill cliffs of eastern Iraq. The interviews indicate that

the kidnapped wild goat juveniles are kept to be raised

as pets or sold in the local animal markets where many

may die due to irresponsible care (Fig. 21). It is worth

mentioning that the capturing of the ungulate young by

local trappers seems to be a common illegal practice in

western and central Iraq which requires further actions

(Al-Sheikhly 201 2a).

Acknowledgments. We are grateful the Iraqi Wildlife Center

(IWC) and Iraqi Green Climate Organization (IGCO) for con-

tinuous support of the wildlife studies in Iraq. We would like

to thank Basheer Mohmmad AI-Taei (a conservationist) for his

detailed information and photographs of the wild goat hunting

and distribution in eastern and southeastern Iraq. Our grati-

tude extends to Ta’eeb Al-Barazani and Abdulallah Al-Baraz-

ani (Forestry Police of Mergasur- Kurdistan Region) for their

detailed information on the species phenology in Barzan area,

to Abdulhamed Al-Habash (Iraqi Hunters Association) for his

further comments on the ungulates hunting in Iraq, and to the

anonymous reviewers for their comments on the earlier version

of this article.

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life Center Publication, Iran

©ZFMK

FORSCHUNGS

Bonn zoological Bulletin 69 (1): 111-115

2020 - Gippoliti S. & Lupi L.

https://do1.org/10.20363/BZB-2020.69.1.111

Scientific note

urn:lsid:zoobank.org:pub:925DF201-A926-4633-B830-14B111BDEF4C

A note on the wild canids (Carnivora: Canidae) of the Horn of Africa,

with the first evidence of a new — forgotten —

species for Ethiopia Canis mengesi Noack, 1897

Spartaco Gippoliti!& Luca Lup?’

'Societa Italiana per la Storia della Fauna “Giuseppe Altobello”’, Viale Liegi 48A, I-00198 Roma, Italy

?Centro di Documentazione e Studi della Dancalia, Pontedera (Pisa), Italy

* Corresponding author: Email: spartacolobus@gmail.com

'urn:|lsid:zoobank.org:author:833DA273-590F-4E54-8A 12-42262EB88C1F

>urn:Isid:zoobank.org: author: 7CEC1C51-7531-4E1A-BOE7-42A6AE3031BA

Abstract. The first ever reported observation of a member of the genus Canis well in the interior of the Danakil area (Ethi-

opia) offers the opportunity to revise available evidence about the existence of a neglected species of small-sized ‘jackal’

in the Horn of Africa. A review of historical zoological literature led to assign this small-sized, reddish jackal to Canis

mengesi Noack, 1897, originally described from inner Somaliland. Geological and geomorphological considerations sup-

port the distinctiveness of the Red Sea coastal jackal Canis anthus riparius Hemprich & Ehrenberg, 1832, typical of the

narrow alluvial, sandy coast, while Canis mengesi is found in the volcanic rocky habitat prevailing over most northern

ISSN 2190-7307

http://www.zoologicalbulletin.de

Afar (Danakil, Ethiopia).

Key words. Canis mengesi, Canis riparius, Danakil, geomorphology, taxonomy.

Knowledge of mammals in some parts of the Horn of

Africa is still very sparse, and gaps exist even with re-

spect to species diversity among the most visible mam-

mals. Regarding canids, one of the best studied mammal

group worldwide, a short note on an unusual wolf-like

individual observed in coastal Danakil Eritrea (Tiwari &

Sillero Zubiri 2004) should have promoted more inter-

est regarding the issue of alpha diversity among canids

in the Horn of Africa, but nothing apparently was done

and this observation remained unidentified. Currently,

much scientific interest concerning the intriguing African

‘golden jackal’ group, has been attracted by new phyloge-

netic data that allied this canid closer to the Eurasian wolf

Canis [upus rather than the Eurasian golden jackal Canis

aureus (Viranta et al. 2017).

The object of this note 1s another observation of a sin-

gle individual of an unusual small-sized canid in the in-

terior of northern Afar (Danakil) region of Ethiopia, done

by one of us (L.L.) on January 1* 2018, along the road

between the Massif of Dadar and the Massif of Masca

(about 12°43’ N, 41°08’ E). A few photos allow us to

discuss some details concerning this individual while at-

tempting a taxonomic identification. This small canid was

observed along a recently asphalted road about 150 km

Received: 28.02.2020

Accepted: 02.04.2020

south of Lake Afrera, an area lacking data concerning the

presence of any member of the genus Canis (cfr. Yalden

et al. 1980). The small size of this individual canid is ev-

ident from comparison with the horizontal traffic signals

(Fig. 1).

The general reddish coloration may suggest a red fox

Vulpes vulpes — a species that 1s probably part of the Er-

itrean fauna (Gippoliti 2020a) yet unlikely to inhabit the

Danakil Region — but the blackish end of the tail, the lack

of black behind the ear, the body building and body pro-

portion (Fig. 2) led to reject this hypothesis.

As evidenced by photos, the canid was observed in

rocky habitat typical of the central and northern rocky

plateau of Afar. The Danakil depression is floored prin-

cipally by Pliocene volcanic rocks of the Afar Stratoid

series (Barberi & Santacroce 1980). The Afar Depres-

sion, between the Red Sea and the Ethiopian plateau, is

covered by Tertiary and Quaternary volcanic rocks. The

Danakil Alps run parallel to the coast, forming a strong

barrier between the interior area and the sandy and allu-

vial coastal region (Fig. 3) (Lupi 2009, 2012).

Unlike Tiwari & Sillero-Zubiri (2004), we examined

the classical zoological and taxonomic literature, a valu-

able source of data concerning morphological diversity

Corresponding editor: R. Hutterer

Published: 19.04.2020

12 Spartaco Gippoliti & Luca Lupi

Figs 1 (left) and 2 (right). Two photos of the same individual canid. Note the small size and habitat characteristics where this canid

individual was observed. Photos: Luca Lupi.

that is often overlooked by recent research (Gippoliti

2020b). We found that a canid taxon with the characters

shown in the photo was described from the Horn of Afri-

ca at the end of the 19th century. In 1897, the German zo-

ologist Theodor Noack described two new canid species

from several living specimens captured in Somaliland by

Joseph Menges, a collaborator of the famous Carl Hagen-

beck (Noack 1897). The larger species was named Canis

hagenbecki while the smaller one became Canis men-

gesi. These descriptions were based on numerous living

specimens and several skulls in the possession of Noack.

According to Noack (1897), Canis mengesi is smaller

and shorter-legged than C. hagenbecki. His diagnostic

characters, especially compared with C. hagenbecki, in-

clude the following: snout is shorter and the longer ear

has a slenderer tip. The hind quarters are kept low, so that

the gait of the animal resembles a hyena. Hair on the back

is short, with a dark spot on the middle tail, but without

or at least with only a minor black tip of the tail. Body

colour is reddish yellow or reddish grey, including the

nasal area and the rear of the ears. Forehead red grey, hair

on the back paler with more yellow hair tips, the brown

of the hair tips hardly visible if present at all. Lower lip

is brown, upper lip white, iris of the eye yellowish red

with a grey hue. Legs are yellowish red, not darker on

the forelegs, hardly paler on the inner sides. A dark collar

on the neck is absent. Breast and belly are paler than the

flanks. The species digs cavities in the soil. The vocaliza-

tion is similar to C. hagenbecki, but more whining, rather

like a young dog. Skull is slender, with an only weakly

curved profile, nasal bones somewhat longer than max-

illae, and broader in front than in the middle. Occiput as

in C. hagenbecki and C. anthus. Pterygoid process more

widely spaced from each other than in C. hagenbecki.

Upper premolars 2 and 3 with additional cusp, as low-

er premolar 4 that has 2 additional cusps. Noack failed

Bonn zoological Bulletin 69 (1): 111-115

to provide details on types, and the exact provenance of

Canis mengesi — as those of C. hagenbecki - remained

vague - Somaliland, Ktistengegenden, Inneres? (Noack,

1897: 518). Heck (1899) under the name of Canis hadra-

maticus Noack published a photo — perhaps the only one

so far published — of one of the captive Canis menge-

si Studied by Noack, showing a relatively massive head

compared to body and legs, and the white area over the

lips (Fig. 3).

Some years later Hilzheimer (1906) not only accepted

C. mengesi, but on the basis of the study of two more

skulls (ex-captive animals captured in Somaliland) in

the museum of Stuttgart, he described a new subspecies,

Canis mengesi lamperti. With 125 and 121 mm their

basilar lengths are even smaller than the type of Canis

mengesi, which they resemble except that their nasalia

do not extend as far back as the maxillary (Hilzheimer

1906). According to Hilzheimer (1906), Canis mengesi

is the smallest true jackal, which forms a group of its

own within the golden jackal group due to its color and

skull shape. Its native range is unknown but could be the

interior of northern Somalia. Maximum basilar length of

its skull is 132 mm. He described C. mengesi lamperti as

very small, as red as a fox, black in midline of back, very

long ears, no black markings and tail with dark brown tip

(Hilzheimer 1908).

The mounted skin of the holotype of Canis mengesi

lamperti (SMNS 2394) is shown here for the first time

as far as we know (Fig. 5), while its skull was shown

by Hilzheimer (1908: table II). It is a male from Joseph

Menges’ expedition to Somaliland that lived in a zoo in

Stuttgart and was donated by Nill to the museum 1n 1897

(Dieterlen et al. 2013). The meagre evidence so far avail-

able does not allow a clear assessment of the minor mor-

phological differences between the two described taxa of

mengesi and our own observation, yet we can conserva-

©ZFMK

A note on the wild canids of the Horn of Africa

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GEOLOGICAL LEGEND - LEGENDA GEOLOGICA |

Scale - Scala

1:950.000

Scale - Scala

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/\ Fluvial and lacustrine sediments,

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rocks (PR) L.S.

Lave (LR) e piroclastiti (PR) riolitiche L.S.

Axial volcanic ranges (< 1 Mya)

Catene vulcaniche assiali (< 1 Ma)

Marginal rhyolite centers (< 4 Mya)

Centri riolitici di margine (< 4 Ma) e i Spater cones

Transverse basaltic volcanism (< 4 Mya)

Vulcanismo basaltico trasversale (< 4 Ma)

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Afar stratoid series (4-1 Mya)

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Serie basaltica di Dhala (8-6 Ma) ;

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Mabla rhyolites series (14-10 Mya) | | |

Serie riolitica di Mabla (14-10 Ma) ;

Neoproterozoic basement, Mesozoic

sediments, Tertiary flood basalts (a),

peralkaline granites (b)

Basamento Neoproterozoico, sedimenti

mesozoici, plateau basaltici del

Terziatio (a), graniti peralcalini (b)

\. Sh a

113

Fig. 3. Geomorphological map of Danakil (Lupi 2012), showing our visual record of Canis mengesi (triangle), and those assigned

to Canis anthus riparius (circle).

Bonn zoological Bulletin 69 (1): 111-115

©ZFMK

114 Spartaco Gippoliti & Luca Lupi

Fig. 4. A living Canis mengesi at Berlin Zoo before his formal

description by Noack. From Heck (1899) who labeled it Canis

hadramauticus Noack. Note the white area over the lips, which

was emphasized by Noack (1897) in his description of mengesi.

tively propose that a small reddish member of the genus

Canis occurs in Danakil, Ethiopia and Somaliland and

his name is Canis mengesi Noack, 1897.

The taxonomic history of Canis mengesi is quite typ-

ical of the systematic attitude of the previous century.

Anderson (1902) studied a skin and skull of C. mengesi

(not one of the typical series, apparently) in Berlin and

maintained it as specifically distinct, a position that also

De Winton (footnote in Anderson 1902: 220) clearly ac-

cepted, changing his previous opinion “In my paper on

African Canidae, C. mengesi was doubtfully referred to

this species [C. variegatus]. Further material has enabled

me to see my mistake, and I fully agree with the view

here expressed”. Anderson (1902) provided the follow-

ing measurements taken on the mounted skin: head and

body length 510 mm, tail length 223 mm, height at shoul-

der 290 mm, ear length 75 mm anterior and 90 mm poste-

rior. Interestingly, some of these measurements are lower

than those reported for the red fox Vulpes vulpes in Egypt

(Osborn & Helmy 1980). The skin (no number but skull

n. 6073) was described by Anderson (1902: 219-220)

as follow “Greyish yellow throughout on the trunk, but

many of the hairs with long black tips; slightly rufous on

the upper surface of the muzzle and white along the upper

lip and on the side of the face before the eyes; chin and

throat white, but a brown area on the middle of the upper

lip. Side of head below the ears yellow, back of ears yel-

Bonn zoological Bulletin 69 (1): 111-115

low with black hairs intermixed. Inside of ears clothed

with white hairs. A tendency to form a dark collar. Fore

limbs bright yellowish, but with a faintly dark area down

the front to near the wrist. Outsides of hind limbs yellow.

Under parts white, with the exception of the base of the

throat in front. Tail concolorous with the body, towards

the tip broadly marked with dark blackish brown; the

black spot on its dorsal surface well defined.” Schwarz

(1926) synonymized several taxa, among them menge-

si, under the name Canis aureus riparius Hemphrich &

Ehrenberg, 1832. Glover Allen (Allen 1939), followed

Schwarz and maintained mengesi as a synonym of Thos

aureus riparius but considered Thos lamperti distinct at

the specific level although stressing the need for further

studies that never happened. Therefore Coetzee (1971)

felt justified to state that “Canis mengesi lamperti [....] 1s

regarded here as asynonym of C. a. riparius”’, apparently

without justification, but de facto relegating the taxon to

oblivion.

After reviewing the few available data and the photo-

graphic evidence here presented, it seems reasonable to

conclude that

1. Asmall-sized member of the genus Canis is found in

the interior of Ethiopian Danakil,

2. Its reddish color, size and pattern generally agree with

that of a forgotten taxon, Canis mengesi, so far his-

torically known only from the interior of Somaliland,

3. Photographic evidence offered by Tiwari & Sille-

ro-Zubiri (2004) seems to confirm that Canis mengesi

is a distinct taxon from the one occupying the coastal

plain zone of Eritrea (i.e., Canis anthus riparius),

4. This new record may indicate that C. mengesi is a

specialist of arid rocky habitats.

Apparently for the first time in decades we propose a

much richer diversity of African canids taxa than usu-

ally recognized, particularly of the genus Canis — now

that the species mesomelas and adusta are separated in

the genus Lupulella (Atickem et al. 2017; but see also

Machado & Teta 2020). The few data concerning golden

Fig. 5. Holotype of Canis mengesi lamperti, courtesy C. Leid-

enroth, State Museum of Natural History Stuttgart

©ZFMK

A note on the wild canids of the Horn of Africa 115

jackals in the Eritrean coastal region (Fig. 3), historically

assigned to the taxon riparius, are clearly limited to the

sandy alluvial coastal plain while we documented a total-

ly different canid in interior Danakil, that has been never

observed in the much better studied coastal region. We

propose therefore that the so far under-appreciated geo-

morphological diversity of the Horn of Africa is one of

the reasons to explain the presence of several lineages of

Canis (Gippoliti 2018). In agreement with Groves et al.

(2017) and Gippoliti (2019), we think that such diversi-

ty 1s better described by ranking these lineages as spe-

cies, and this is particularly the case with Canis mengesi

whose dwarf size, specialized habitat and hair color is

well outside the known variability shown by the ‘African

golden jackal/wolf’ Canis anthus Cuvier, 1820 as it is

now universally understood.

Acknowledgements. The late Colin Groves and Arnd Sch-

reiber provided valuable help in the translation of German pa-

pers and are warmly thanked for this. We wish to thank Stefan

Merker and Carsten Leidenroth, State Museum of Natural His-

tory Stuttgart, for the photo of the holotype of Canis menge-

si lamperti. Richard Weigl and Jan Robovsky helped with the

old Berlin photo. Bruce Patterson (Chicago), Rainer Hutterer

(Bonn), Nikolai Spassov (Sofia) and Boris KryStufek (Ljublja-

na) made valuable revisions of previous versions of the manu-

script.

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the Museum of Comparative Zoology 83: 3-763

Anderson J (1902) Zoology of Egypt, Mammalia. Hugh Rees

Ltd, London

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D (2017) Deep divergence among mitochondrial lineages in

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ti in Dancalia. Mammiferi. Annali Museo civico Storia Natu-

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and the magmatic evolution of East African rift system.

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891-899

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6: 291-303

Gippoliti S (2018) Far-reaching effects of “taxonomic iner-

tia”. The case of the ‘Canis anthus’ complex classification

and conservation in Northern Africa Preprint. August 2018.

https//doi.org10.13140/RG.2.2.13604.53121

Gippoliti S (2019) Mammal species delimitation matters. A re-

ply to Zachos (2018). Mammalian Biology 94: 127-131

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mals in Italian literature and museums, with some taxonomic

notes. Biogeographia-The Journal of Integrative Biogeogra-

phy 35: 27-42

Gippoliti S (2020b) Everything mammal conservation biol-

ogists always wanted to know about taxonomy (but were

afraid to ask). Journal for Nature Conservation 54: 1-6.

https://doi.org/10.1016/j.jnc.2020.125793

Groves CP, Cotterill FPD, Gippoliti S, Robovsky J, Roos C,

Taylor PJ, Zinner D (2017) Species definitions and conser-

vation: A review and case studies from African mammals.

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Hilzheimer M (1908) Beitrag zur Kenntnis der nordafrikan-

ischen Schakale nebst Bemerkungen tuber deren Verhaltnis

zu den Haushunden, insbesondere nordafrikanischen und al-

tagyptischen Hunderassen. Zoologica 53: 1-111

Lupi L (2009) Dancalia. L’esplorazione dell’ Afar, un’avventura

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Machado FA, Teta P (2020) Morphometric analysis of skull

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Schwarz E (1926) Der Schakal der Galla-Hochlander. Varia-

tionsstudien an Saugetieren, I. Senckenbergiana 8: 155-158

Tiwari JK, Sillero-Zubiri C (2004) Unidentified canid in the

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BHL

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Bonn zoological Bulletin 69 (1): 117-122

2020 - Gokulakrishnan G. et al.

https://do1.org/10.20363/BZB-2020.69.1.117

ISSN 2190-7307

http://www.zoologicalbulletin.de

Scientific note

urn:|sid:zoobank.org:pub: BCCS5 BF79-B2F4-40A2-AD92-55D3AC977FCB

Further records of a poorly-known insular endemic skink

Lipinia macrotympanum (Stoliczka, 1873)

(Squamata: Scincidae)

G. Gokulakrishnan’, C. Sivaperuman’ & S. R. Chandramouli* *

'? Zoological Survey of India, Andaman and Nicobar Regional Centre, Haddo, Port Blair

3 Department of Ecology and Environmental Sciences, Pondicherry University, Puducherry

* Corresponding author: Email: findthesnakeman@gmail.com

'urn:lsid:zoobank.org:author:8 1676BC5-F41F-4A8A-8531-FF9CBB282843

?urn:lsid:zoobank.org:author:08F28A 1 0-E80D-420C-924 1 -24F5CC199EB6

-urn:lsid:zoobank.org:author:73 BF7214-77B 1-45EA-A7FB-8CB13D15094F

Abstract. The little-known, insular endemic skink Lipinia macrotympanum (Stoliczka, 1873) was recorded recently from

two new localities in Great Nicobar Biosphere Reserve (GNBR) further south of the previously known localities. Based

on these observations, new data on morphology, natural history and distribution are presented and it is suggested to be

considered as an endangered species based on the IUCN assessment criteria.

Key words. Lipinia macrotympanum, new locality records, distribution map, Nicobar archipelago.

The skink genus Lipinia Gray, 1845 is represented by 32

species which are distributed from the Nicobar Islands

in the West to Papua New Guinea in the east (Uetz et al.

2019). Of these, the westernmost representative of the ge-

nus, Lipinia macrotympanum was described originally by

Stoliczka (1873) as Mocoa macrotympanum from “South

Andaman, on a sandy beach in Macpherson’s Straits”.

Later, Biswas & Sanyal (1977) reported a specimen of

this species erroneously identified as “Lygosoma qua-

drivittatum” (now Lipinia quadrivittata) from Campbell

Bay, Great Nicobar. Subsequently, Das (1997) reported

the rediscovery of Lipinia macrotympanum based on

his new collection of a specimen from Pulo Ulon, Little

Nicobar and the specimen reported by Biswas & Sanyal

(1977). Ever since this report, Lipinia macrotympanum

was never recorded from the Andaman and Nicobar Is-

lands. Herein, we report on two specimens of Lipinia

macrotympanum based on our field observations and col-

lected specimens. One of the individuals reported here

(ZSI/ANRC/T/3709) was illustrated by Rangasamy et al.

(2019) in their list of herpetofauna of the Andaman and

Nicobar Islands.

Received: 19.12.2019

Accepted: 08.04.2020

Faunal surveys spanning 10-15 days were conduct-

ed on islands of the Nicobar archipelago intermittent-

ly between 2015 and 2018. Two of three specimens of

L. macrotympanum recorded during these surveys were

collected, preserved and deposited in the holdings of

the Zoological Survey of India, Andaman and Nicobar

Regional Centre (ZSI ANRC). The collected specimens

were measured with a vernier caliper and a Leica stereo-

microscope to the nearest 0.1 mm. The following charac-

ters were recorded: Snout tip to vent (SVL), trunk length

from axilla to groin (AG), tail length from vent to tail tip

(TL), head length (HL), head width at jaw angle (HW),

head depth (HD), eye diameter (ED), tympanum diame-

ter (TYD), eye-nostril distance (EN), eye-snout distance

(ES), eye-tympanum distance (ETY), forelimb length

(FLL), hindlimb length (HLL), inclusive of femur length

(from groin to knee) (FEL) and tibia length (from knee to

heel) (TBL), finger lengths (F1—F5), toe lengths (T1—TS5),

midbody scale-rows (MSR), nuchals (NU), supralabials

(SL), infralabials (IL), ventrals (V), supraoculars (SO),

prefrontals (PRF), subdigital lamellae under toe IV. Sex

of the specimens was determined by examining the clo-

acal region for the presence of hemipenes. Geographic

coordinates of the areas of its occurrence were recorded

with a GPS and mapped with ARC MAP 10. Terminolo-

gies for color descriptions follow Poyarkov et al. (2019).

Corresponding editor: W. Bohme

Published: 19.04.2020

118 G. Gokulakrishnan et al.

Lipinia macrotympanum (Stoliczka, 1873)

(Figs 1—2)

Mocoa macrotympanum Stoliczka, 1873

Lygosoma macrotympanum — Boulenger (1890)

Leiolopisma macrotympanum — Smith (1935)

Lygosoma quadrivittatum (non Peters, 1867) — Biswas &

Sanyal (1977)

Lipinia macrotympanum — Greer (1974); Das (1997);

Das & Austin (2007)

Lipinia macrotympana — Das (1999) sic.

INDIA — 1 adult male (ZSI/ANRC/T/3709); Shastri

Nagar; 6.810° N, 93.892° E; 37 m a.s.l.; G. Gokulakrish-

nan leg. 11 Oct. 2015. 1 adult male (ZSI/ANRC/T/4330);

Galathea; 6.8216° N, 93.8673° E; 37 m a.s.l.; G. Goku-

lakrishnan leg. 20 Nov. 2016.

L. macrotympanum is a small species of Lipinia from the

Nicobar Islands, that can be diagnosed and characterized

by: the presence of a large and exposed tympanic mem-

brane; 7 supralabials; 6 infralabials; presence of a large,

transparent disc on the lower eyelid; a single broad pre-

frontal with a median constriction or two separated pre-

frontals (fide Das, 1997); two, nearly equal sized loreals;

a single, undivided frontoparietal; 4 supraoculars; a pair

of enlarged preanal scales; 21-23 midbody scale rows;

51-53 paravertebrals; 60-62 ventrals; 16-17 subdigi-

tal lamellae under toe IV; SVL 36.5-45 mm; tail 43.9—

50 mm; dorsal coloration of black with three yellow lon-

gitudinal stripes from snout to vent; tail red or reddish

brown (based on the collected specimens and Das, 1997).

The newly collected material, two adult males, mea-

sure 38.5-39.6 mm SVL; overall habitus slender and

elongated. Head short (HL:SVL 0.12); slightly longer

than broad (HL: HW 1.02) with a pointed snout tip in both

dorsal and lateral views. Nostrils located laterally, closer

to the snout tip than to the eyes (EN:ES 0.7). Rostral visi-

ble from above; frontonasal broader than long; prefrontal

single in ZSI/ANRC/T/3709; *8’ shaped, with a median

constriction; two small rhomboidal prefrontals, in con-

tact with each other in ZSI/ANRC/T/4330; frontal wedge

shaped; frontoparietal single; interparietal fairly elongat-

ed; parietals large; in contact with each other; three pairs

of broad nuchals present. Paravertebrals slightly broader

than the adjacent body scales. Supraoculars four; third

largest; lower eyelid with a transparent disc. Loreals two,

trapezoidal in shape and nearly of equal size. Temporals

large and smooth. Supralabials 7, 6" largest; infralabials

6. Tympanic opening large (TYD:ED 0.66) with a visi-

ble eardrum, lacking auricular lobules. Mental semicir-

cular; a single large postmental. Anterior chin-shields in

contact with each other; posterior chin-shields separated

by a single scale. Midbody scale rows 21—23:; smooth.

Limbs fairly well developed. Relative length of fingers

IV>IN>H>V>I. Thigh short (FEL:SVL 0.12); tibia as

Bonn zoological Bulletin 69 (1): 117-122

Table 1. Measurements of the examined Lipinia macrotympa-

num specimens compared with literature.

ZSVANRC/ ZSI/ANRC/ _ Das (1997)

T/ 4330 T/ 3709

Total Length 92'5 89.8 80.4-91.7

SVL 38.7 37.6 36.5-38.1

TL 53.8 52.2 43.9-53.6

AG 24 23.8 20.2-21.3

HL 48 4.7 5.8

HW 47 46 3.7-3.9

ES 2.9 Zen 2.7-2.9

EN 2 1.9 1.5-1.6

NS 1.3 1.1 —

ED 1.8 ie! 1.3-1.8

TYD 1.2 1.1 1.0-1.1

IN i) 1.4 1.3-1.7

IO 4 3.8 1.3-1.7

FLL 10.11 9.8 8.4

FEL 46 4.5 =

TBL 46 4.5 ce

Paravertebrals 51 53 =

Ventrals 60 62 62

MSR 23 21 21-23

T4 lamellae 15 16 15-17

NU 6 6 6

long as thighs (FEL:TBL 1.0); foot slightly longer. Toe

IV longest; relative length of toes TV >II>V >II>I; toe

IV with 15 smooth subdigital lamellae; claws long and

protruding. Measurements of the material studied are

presented in table 1.

Dorsal coloration black to dark brown anteriorly; fad-

ing posteriorly to light brown with a reddish brown tail

in ZSI/ANRC/T/3709. Dorsum with three yellow stripes;

the mid dorsal light stripe (MDLS) originating from the

snout and broadening as it proceeds posteriorly towards

the sacrum. The other specimen, ZSI/ANRC/T/4330 was

golden brown overall, with just the head and neck bear-

ing the dark coloration. Two paravertebral dark stripes

(PVDS) commencing from post ocular region, continu-

ing till the sacrum, beyond which it merges with the uni-

formly reddish brown coloured tail; stripes not discern-

ible posteriorly. Lateral body and limbs orange colored.

Lateral dark stripe (LDS) and ventrolateral dark stripes

(VLDS) absent. Dark temporal marking (DTM) present

in all the samples. Venter uniform creamy white. Under-

side of tail reddish. The coloration of ZSI/ANRC/T/4330

©ZFMK

New records of Lipinia macrotympanum 119

Fig. 1. Lipinia macrotympanum in \ife. A-B. ZSI/ANRC/T/4330 from Galathea. C. ZSI/ANRC/T/3709 from Shastri

Nagar.

reported herein has not been known until now. Illustra-

tion of this species published by Das (2002) conforms to

the coloration of ZSI/ANRC/T/3709.

The first individual recorded from Shastri Nagar (ZSI/

ANRC/T/3709) was found near an old building, and was

Bonn zoological Bulletin 69 (1): 117-122

seen actively moving and approaching the observers after

dusk at ca. 19:43 h. The immediate vicinity if this spot is

bordered by evergreen forests and a stream to the west

and a sandy beach to the south. The second and third in-

dividuals from Galathea were observed on the ground:

©ZFMK

120 G. Gokulakrishnan et al.

Fig. 2. Head of Lipinia macrotympanum ZS\/AN-

RC/T/3709. A. Dorsal view. B. Lateral view. C. Ventral

view.

the specimen collected (ZSI/ANRC/T/4330) was found

resting under a dry palm leaf post noon at ca. 15:18 h.

The third, uncollected individual was found foraging on

the ground, at the camp site near the tent in Feb 2016.

This region (Galathea) is surrounded by Casuarina

groves bordering a stretch of a sandy beach near the Gal-

athea River delta. The habitat of this region is generally

characterized by reduced canopy cover, low leaf-litter

and sandy soil situated close to the sea coast with strand

vegetation.

From congeners, Lipinia macrotympanum can be dis-

tinguished as follows (data for comparison modified from

Das & Austin 2007 and Poyarkov et al. 2019): presence

of an externally visible tympanic membrane (vs. hidden

in L. sekayuensis;, L. inexpectata and L. surda), dorsum

with a pattern of longitudinal stripes (vs, absent in L. sur-

Bonn zoological Bulletin 69 (1): 117-122

da and faint stripes in L. sekayuensis),; 16-17 subdigi-

tal lamellae under toe IV (vs. 19-23 in L. albodorsalis,

18-25 in L. infralineolata,; 7-10 in L. leptosoma, 19 in

L. longiceps;, 21 in L. miangensis; 20-21 in L. occiden-

talis, 24—31 in L. pulchella; 22 in L. pulchra;, 18-21 in

L. rabori; 18 in L. relicta,; 22—26 in L. rouxii; 19-21 in

L. semperi;, 18—22 in L. septentrionalis, 19-21 in L. ven-

emai, 25 in L. vittigera. Three pairs of nuchals present

in L. macrotympanum (vs. five pairs in L. cheesmanae;

2 pairs in L. inexpectata), 21-23 midbody scalerows in

L. macrotympanum (vs. 22—25 in L. albodorsalis, L. au-

riculata, 28 in L. cheesmanae, 22—26 in L. leptosoma, 24

in L. longiceps and L. miangensis, 24—28 in L. noctua;

24-25 in L. notolineata; 24—26 in L. occidentalis, 22—26

in L. pulchella; 24 in L. pulchra; 22-28 in L. rouxi, 24—26

in L. septentrionalis, 24—26 in L. venemai; 28 in L. vittig-

era and L. vassilievi;, 32 in L. vulcania; 24 in L. zamboan-

gensis, 28-32 in L. microcercus and L. trivittata.

Lipinia macrotympanum has been one of the most

poorly known skink species in the Andaman and Nicobar

archipelago, which has been recorded only three times

since its description in 1873 (Biswas & Sanyal 1977; Das

1997; Rangasamy et al., 2014). Other herpetofaunal sur-

veys (e.g., Vijayakumar 2005, Harikriahnan et al. 2008,

2014) did not record L. macrotympanum. The present ob-

servations of L. macrotympanum reported here are from

the southern extremity of Great Nicobar and are at least

35—40 km south of the closest previously known locality

from Great Nicobar (1.e., Campbell Bay fide Biswas &

Sanyal, 1977) thereby extending its distribution range

further south. Das (1997) stated that the individual re-

corded by him was also seen on the sand, moving with

great agility. L. macrotympanum being active after dusk

reported here is novel information as earlier authors have

all recorded it during the day time. The individuals re-

ported here were also seen on the ground as reported by

Das (1997). The type locality of this species, Macpher-

son’s Strait lies between the southern tip of South An-

daman and Rutland Island. There have been no reports

of this species from any of the islands in the Andaman

archipelago since its original description. All of the sub-

sequent reports (Biswas & Sanyal 1977, Das 1997, this

work) have been from the southern group of islands in

the Nicobar archipelago, 1.e., Little and Great Nicobar

Islands, situated to the south of the Sombrero Channel.

The Andaman Islands, situated in the north of the ten-de-

gree channel are biogeographically different from those

of the Nicobar Islands and their fauna show a more In-

do-Chinese faunal affinity (Das 1999). It is speculated

that the type locality of L. macrotympanum mentioned

by Stoliczka (1873) could be inaccurate and the species

may not actually occur in the Andaman Islands. The pos-

sible absence of Lipinia in the Andaman Islands 1s further

supported by the fact that it has never been recorded from

islands of the Andaman archipelago after the report by

Stoliczka (1873) although several herpetofaunal surveys

©ZFMK

New records of Lipinia macrotympanum 121

92°0'0"E 94°0'0"E 95°0'0"E 96°0'0"E

93°0'0"E

13°30'0"N

13°30'0"'N

10°30'0"N 11°30'0"N 12°30'0"N

9°30'0"N 10°30'0"N 11°30'0"'N 12°30'0"N

9°30'0"N

RIN" N

Nicobar Islands

8°30'0"N

------Sombrero Channel------

7°30'0"N

P3ANON

0 25 50 100 Kilometers

92°0'0"E 93°0'0"E 94°0'0"E 95°0'0"E 96°0'0"E

93°30'0"E 94°0'0"E

Pulo Ulon

70'0"N

7°0'0"'N

Shastri

Nagar

12 Kilometers

93°30'0"E 94°0'0"E

Fig. 3. Type locality (Macpherson’s Strait) of Lipinia macrotympanum: Literature records (red dots) and new locality

records (black dots) in Great and Little Nicobar Islands.

have been and are still being carried out in the Andaman

archipelago (e.g., Das, 1999; Harikrishnan et al., 2014:

Rangasamy et al., 2014; pers. obs.). Similarly, there have

been some intriguing records of certain species which

were mentioned in older literature from certain regions,

but have never been recorded from such localities sub-

sequently. Examples include Lycodon tiwarii from May-

abunder, North Andaman, Oligodon woodmasoni from

Andamans for both of which, confirmed current records

are only from the Nicobar Islands (Vijayakumar & Da-

vid 2006) and Hemidactylus platyurus which was once

reported from Great Nicobar (Tiwari & Biswas 1973) but

is presently known from the Andaman Islands, and not

Nicobars.

Based on the observations reported until now, we rec-

ommend to regard L. macrotympanum as an endangered

species based on the criteria B1 (Extent of occurrence

less than 5000 km?) and B2 (Area of occupancy less than

500 km?) of IUCN. Further studies are required to better

understand the ecology of this poorly known, narrowly

endemic species.

Bonn zoological Bulletin 69 (1): 117-122

Acknowledgements. We thank the Department of Environ-

ment and Forests, Andaman and Nicobar Islands for permis-

sion and for the infrastructure provided. GGK and CS thank

the Director, ZSI, Kolkata for the support and encouragement;

SRC thanks K. V. Devi Prasad and the faculty of the Dept. of

Ecology and Environmental Sciences and the Dept. of Ocean

studies and Marine Biology, Pondicherry University for the

support extended. Constructive comments by the reviewers are

appreciated.

REFERENCES

Biswas S, Sanyal DP (1977) Notes on the Reptilia collection

from the Great Nicobar Island during the Great Nicobar Ex-

pedition in 1966. Rec. Zool. Surv. India 72: 107-124

Boulenger GA (1890) The Fauna of British India, Including

Ceylon and Burma. Reptilia and Batrachia. Taylor & Francis,

London, xviii

Das I (1997) Rediscovery of Lipinia macrotympanum

(Stoliczka, 1873) from the Nicobar Islands, India. Asiatic

Herpetol. Res. 7: 23—26

Das I (1999) Biogeography of the amphibians and reptiles of

the Andaman and Nicobar Islands, India. Pp. 43-77 in: Ota

H. (ed.) Tropical Island herpetofauna. Origin, current diver-

sity and current status. Elsevier

©ZFMK

122 G. Gokulakrishnan et al.

Das I, Austin C (2007) New Species of Lipinia (Squamata:

Scincidae) from Borneo, Revealed by Molecular and Mor-

phological Data. J. Herpetol. 41: 61—71

Greer AE (1974) The generic relationships of the scincid lizard

genus Leiolopisma and its relatives. Australian J. Zool. (Sup-

plement Series) 31: 1-67

Harikriahnan S, Choudhury BC, Vasudevan K (2008) Assess-

ment and inventory of herpetofaunal diversity of Nicobar Is-

lands, India. Report: Wildlife Institute of India: 42

Harikriahnan S, Vasudevan K, Das A, Choudhury BC, Dutta

SK, Das I (2014) Macroecology of Terrestrial Herpetofauna

in Andaman & Nicobar Archipelago. Report: Wildlife Insti-

tute of India: 49

Poyarkov Jr. NA, Geissler P, GorinVA, Dunayev EA, Hartmann

T, Suwannapoom C. (2019). Counting stripes: revision of the

Lipinia vittigera complex (Reptilia, Squamata, Scincidae)

with description of two new species from Indochina. Zool.

Res. 40: 358-393

Rangasamy V, Chandra K, Ragunathan C, Venkataraman K.

(2014) Amphibians and reptiles in Andaman and Nicobar

Islands: Diversity and Distribution. Online at http://www.

upsbdb.org/pdf/Souvenir2014/ch-18.pdf

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Rangasamy V, Sivaperuman C, Gokulakrishnan G, Parthipan P

(2018) Herpetofauna of Andaman and Nicobar Islands. Pp.

37-56 in: Sivaperuman C. & Sivaperuman K. Venkataraman

(eds) Indian hotspots. Springer Nature Singapore

Smith, MA (1935) The fauna of British India, including Ceylon

and Burma. Reptilia and Amphibia, Vol.2, Sauria, Taylor and

Francis, London

Stoliczka F (1873) Note on some Andamanese and Nicobarese

reptiles, with the description of three new species of lizards.

J. Asiatic Soc. Bengal 92 (3): 162-169

Tiwari KK, Biswas S (1973) Two new reptiles from the Great

Nicobar Island. J. Zool. Soc. India. 25(1 & 2): 57-63

Uetz P, Freed P, HoSek J (eds) (2019) The Reptile Database.

Online at http:/(\www.reptile-database.org [last accessed 12

Dec. 2019]

Vijayakumar SP, David P (2006) Taxonomy, natural history and

distribution of the snakes of Nicobar Islands (India), based

on new materials and with an emphasis on endemic species.

Russ. J. Herpetol. 13 (1): 11-40

Vijayakumar SP (2005) Status and distribution of Amphibians

and Reptiles of the Nicobar Islands, India. Final Report. Ruf-

ford Foundation / Madras Crocodile Bank / Wildlife Institute

of India: 48

©ZFMK

ISSN 2190-7307

http://www.zoologicalbulletin.de

Bonn zoological Bulletin 69 (1): 123-130

2020 - Gorczyca J. et al.

https://do1.org/10.20363/BZB-2020.69.1.123

Research article

urn:|sid:zoobank.org: pub:8840C9B5-072C-4E04-B9F5-604AFD149E76

The first record of the genus Fulvius Stal, 1862

(Heteroptera: Miridae: Cylapinae)

from continental China with description of a new species

Jacek Gorezyca', Andrzej Wolsk? & Artur Taszakowski° *

!3 Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences,

SY, SY ly

University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland

? Institute of Biology, University of Opole, Oleska 22, 45-052 Opole, Poland

* Corresponding author: Email: artur.taszakowski@us.edu.pl

'urn:|sid:zoobank.org:author:6E164D8D-B7D1-48E3-B771-C36E211AB7DC

> urn:Isid:zoobank.org:author:author:845C8DAF-B265-4C4E-954E-6B8C44A EA 27B

3urn:lsid:zoobank.org:author: BB6E3 148-D9BC-4DC1-A212-E99ECS5F96E28

Abstract. A new species of the genus Fulvius Stal, 1862 (Heteroptera: Miridae: Cylapinae: Fulviini) is described based on

a couple of specimens collected in Yunnan Province in SW China. The genus is also reported from continental China for

the first time. Detailed illustrations of the tarsi, the distribution of trichobothria on the metafemur and male genitalia are

given, and an image of the dorsal habitus is presented.

Key words. Asia, biodiversity, new species, plant bugs, taxonomy, true bugs, Yunnan Province.

INTRODUCTION

Fulvius Stal, 1862 is known as one of the most speciose

genera within the subfamily Cylapinae, with more than

80 valid species worldwide (Wolski et al. 2018). Nev-

ertheless, the state of the knowledge about this genus

is probably far from being complete. Most species oc-

cur in the New World and the Afrotropical and Oriental

Regions. Only a few species are known from the Aus-

tralian Region and very few have been described from

the Palearctic Region (Gorczyca 2006). Little is known

about the biology of the congeners. While most members

of Fulvius are frequently collected using UV light traps,

some of them are saproxylic and have been found on fall-

en decaying wood or often on fungi, sucking the fungal

hyphae (Gossner & Damken 2018; Kim et al. 2019). On

the other hand, some of them are carnivorous (Yasunaga

& Miyamoto 2006; Pluot-Sigwalt & Cherot 2013).

While examining some material housed in the Depart-

ment of Entomology at the National Museum of Natural

History, Prague, Czech Republic, two specimens of the

genus Fulvius, collected in Yunnan Province of SW Chi-

na were found. These were confirmed as representing an

undescribed species of Fu/vius, which 1s described in this

paper. This discovery also reveals the first distributional

record for the genus from continental China.

Received: 06.01.2020

Accepted: 14.05.2020

MATERIAL AND METHODS

The specimens were imaged using the following equip-

ment: a Leica M205C stereo microscope with a Leica

DFC495 digital camera and Leica application suite 4.9.0

software; a Leica DM 3000 upright light microscope

with a Leica MC 190 HD digital camera and Leica Ap-

plication Suite 4.12.0 software and an Olympus upright

light microscope with a Canon EOS 750D digital cam-

era. SEM photographs were obtained using a Phenom XL

field emission scanning electron microscope at 10 and

15 kV accelerating voltages using a BackScatter Detector

(BSD). Measurements were taken with Leica applica-

tion suite 4.9.0 software and are presented in millime-

tres (mm). The total body length is defined as the length

from the apex of the clypeus to the posterior margin of

the membrane. The measured body parts were defined in

Wolski (2015). Genitalia were kept in 10% KOH solution

before dissection, and the female genitalia were stained

with chlorazol-black. The terminology of the male geni-

talic structures follows Kerzhner & Konstantinov (1999),

Konstantinov (2003) and Cassis (2008), and the termi-

nology of the female genitalia follows Davis (1955), Sa-

dowska-Woda et al. (2006) and Pluot-Sigwalt & Matocq

(2017).

Corresponding editor: M. Espeland

Published: 04.06.2020

124 Jacek Gorezyca et al.

RESULTS

Taxonomy

Fulvius yunnanicus sp. nov.

urn: lsid:zoobank.org:act: E4C62668-C84B-4407-B895-9F 54F2268ECO

Type material

Holotype (<). China, Yunnan Prov., 1.8 km W Zizhi

vill., 2.vil. 2016, 25°44.7' N, 98°33.6' E, 2005 m a.s.l.,

from large dead tree stumps, J. Hajek & J. RUzi¢ka leg.:

collection of the National Museum Praha, Czech Repub-

lic. Paratype (2). Same data as for holotype; both are

preserved in the Department of Entomology, the National

Museum, Prague, Czech Republic.

Diagnosis. The new species belongs to the anthocoroi-

des-group (see discussion below) and can be distin-

guished from other members of the group by the follow-

ing combination of characters: pronotum dark brown

with three brown longitudinal stripes spanning its whole

length; antennal segments I-II dark brown to black with

contrastingly yellow apical 1/4; legs entirely brown

(Fig. 1); endosoma with large, oval sclerotized lobe api-

cally (Fig. 4C); bursa copulatrix with ring-like sclerite

situated near base of the seminal depository; sclerotized

rings weakly developed (Fig. 5A).

Most similar to F} mateusi Sadowska-Woda & Gorczy-

ca, 2008, F. nigricornis Poppius, 1909 and F: tagalicus

Poppius, 1914 in sharing the uniformly coloured hemely-

tron. & yunnanicus can, however, be easily distinguished

from these species by having the pronotum with brown,

longitudinal patches along entire length (Fig. 1) and the

presence of the oval sclerotized lobe in the endosoma

(Fig. 4C) (see remarks below).

DESCRIPTION

Male

Colouration (Fig. 1). Dorsum, pale brown with darker,

mostly dark brown areas.

Head. Dark brown, tinged with yellow, first and sec-

ond segment vary from dark brown to nearly black,

second segment contrastingly yellow apically, third and

fourth segments dark brown; labium brown, last segment

dark brown.

Thorax. Pronotal collar. Brown. Pronotum. Dark

brown with two brown longitudinal stripes. Mesoscutum

and scutellum. Dark brown, scutellum pale at apex. Tho-

racic pleura. Proepimeron, mesepisternum and mese-

pimeron dark brown almost black. Hemelytron. Pale

brown, partly translucent, exocorium slightly tinged

with red; clavus pale brown at base, dark brown in apical

part with large dark brown and reddish patch contiguous

Bonn zoological Bulletin 69 (1): 123-130

1mm

Fig. 1. Fulvius yunnanicus sp. nov., holotype, dorsal view.

with clavus and membrane; cuneus dark brown, paler at

apex; membrane grey, venation dark grey. Large areolar

cell triangular; small areolar cell very small. Legs. Pale

brown, femora in apical part slightly tinged with red.

Abdomen. Chestnut to dark brown.

Structure, texture and vestiture. Dorsum matte, cov-

ered with fine, pale, very short closely fitting, scale-like

setae.

Head. Eyes contiguous with pronotal collar; first and

second antennal segments covered with dark, short setae

(Figs 1-2); second segment slightly thickened towards

apex; third and fourth segments very thin, covered with

pale, long, protruding setae. Labium reaches beyond

metacoxae (Fig. 2C).

©ZFMK

Fulvius yunnanicus sp. nov. 125

Fig. 2. Fulvius yunnanicus sp. nov., holotype, front part of the body. A. Dorsal view; B. Ventral view; C. Lateral view.

Thorax. Pronotum. Anterior lobe of pronotum only Legs. Relatively long (Fig. 1), covered with very short

slightly convex with thin longitudinal sulcus medially — setae, much shorter than diameter of tibiae; metafemora

(Fig. 2A). with nine trichobothria (Fig. 3C—E); tarsi two-segment-

126 Jacek Gorezyca et al.

Fig. 3. Fulvius yunnanicus sp. nov. A. Paratype, metatarsus; B.

metafemur; D—E. Details of the structure of the trichobothria.

ed, second segment not divided; claws with distinct sub-

apical tooth (Fig. 3AB). Hemelytron. Major cell triangu-

lar, minor cell very small.

Male genitalia (Fig. 4). Typical of anthocoroides

group (Gorczyca 2002; Sadowska-Woda et al. 2008:

Wolski et al. 2018, also see discussion below). Right

paramere. Apical process thin and relatively long; spine

Bonn zoological Bulletin 69 (1): 123-130

Claws in details; C. Holotype, distribution of trichobothria on the

on inner surface of paramere body indistinct. Aedeagus.

Sclerotized part of seminal duct broadened apically; en-

dosoma with strongly developed, arcuate sclerite and

large, elliptical sclerotised lobe on apical half.

©ZFMK

Fulvius yunnanicus sp. nov. 127

Fig. 4. Fulvius yunnanicus sp. nov., holotype, male genitalia. A. Right paramere; B. Left paramere; C. Lateral view of endosoma;

D. Dorsal view.

Female

Similar to male in colouration, structure, texture and ves-

titure.

Female genitalia (Fig. 5). Genital chamber (or bursa

copulatrix) rounded; lateral oviducts short, slightly broad

apically, ring-like sclerite near basal part of seminal de-

pository rounded, protruding, prominent, broadly devel-

oped; sclerotized ring situated laterally, indistinct; poste-

rior wall with wrinkled interramal sclerite; membranous

structure present between gonapophysis I.

Measurements (mm). 4/9 (holotype measurements

first)

Body. Length 4.09/4.10, width 1.36/1.36.

Head. Length of head 0.79/0.79, width 0.61/0.66, dor-

sal width of eye 0.17/0.18, width of vertex 0.27/0.28.

Antenna. Length of segment I 0.51/0.52, II 1.14/1.19,

III 0.51/0.51, [TV 0.50/ missing in 9.

Labium (unmeasurable in specimens examined).

Pronotum. Length 0.61/0.63, length of lateral margins

0.67/0.77, length of anterior margins 0.51/0.52, length of

posterior margins 1.14/1.37

Distribution. China, Yunnan Province (Fig. 6).

Bonn zoological Bulletin 69 (1): 123-130

Etymology. The specific epithet refers to the Chinese

province Yunnan where the specimens were collected.

Remarks. Gorczyca (2002), Sadowska-Woda et al.

(2008) and Wolski et al. (2018) summarized the morpho-

logical characters that define the three species groups that

are currently found in the genus Ful/vius Stal, 1862: the

anthocoroides, bifenestratus, and bisbistillatus groups.

The presented new species can easily be classified as a

member of the anthocoroides group as it has the follow-

ing characters: a) dorsum matte, covered with uniformly

distributed setae (Fig. 1; Wolski et al. 2018: figs 41-44);

b) second tarsomere not subdivided medially, subapical

tooth present (Fig. 3A—B; Wolski et al. 2018: figs 45-46);

c) the aperture of the pygophore is oriented posteriorly,

with long dorsal wall (Wolski et al. 2018: figs 47-48);

d) the parameres are similar in size, the right paramere

has a relatively thick paramere body and a thin and short

apical process; the left paramere has a relatively long

apical process with a subapical incision (Fig 4A—B; Car-

valho and Lorenzato 1978: figs 56-57, 68-69; Gorczyca

2002: figs 1-4; Pluot-Sigwalt & Chérot 2013: fig. 4B—C;

Yasunaga 2000: figs 23-24, 28-29; Yasunaga and Wolski

2017: figs 3A—B); e) endosoma with sclerites or sclero-

tized appendages; the sclerotized portion of the seminal

©ZFMK

128 Jacek Gorezyca et al.

0.1 mm

Fig. 5. Fulvius yunnanicus sp. nov., paratype, female genitalia: A-B. Genital chamber (or bursa copulatrix). A. Dorsal view; B.

Posterior wall, anterior view; C. Gonapophysis I and adjacent structures, dorsal view; D. Gonapophysis I and adjacent structures,

right lateral view. m = membranous structure adjunct to gonapophysis I; odl = lateral oviduct; sc = ring-like sclerite near basal part

of seminal depository; sd = seminal depository; sr = sclerotized ring.

duct is well developed, long and tubular (Fig. 4C—D;

Carvalho & Lorenzato 1978: fig. 55; Pluot-Sigwalt &

Chérot 2013: fig. 4A; Yasunaga 2000: fig. 30; Yasunaga

& Wolski 2017: fig. 3C) and f) a membranous structure

is present between the gonapophysis I (Fig. 5C—D; Sad-

owska-Woda et al. 2008).

Within the anthocoroides group F: yunnanicus sp. nov.

is most similar to the Oriental F? mateusi Sadowska-Wo-

da & Gorczyca, 2008, F. nigricornis Poppius, 1909

and F. tagalicus Poppius, 1914 . All these species have

uniformly coloured hemelytron (e.g., Yasunaga 2000:

fig. 19), not having any pale patch basally as it is found

for example in F’ anthocoroides (Reuter, 1875), F: dim-

idiatus (Poppius, 1909) or F) ussuriensis Kerzhner, 1973

Bonn zoological Bulletin 69 (1): 123-130

(e.g., Yasunaga 2000: figs 18, 22; Yasunaga & Wolski

2017: fig. 2C). The present new species can, however,

be easily distinguished from F) mateusi, F. nigricornis

and F) tagalicus by having the pronotum with brown,

longitudinal patches along entire length (Fig. 1) and the

presence of the oval sclerotized lobe in the endosoma

(Fig. 4C). From F) mateusi F- yunnanicus sp. nov. can be

also distinguished by the antennal segment II with con-

trastingly yellow annulation apically (Fig. 1) (antennal

segment IT is uniformly dark brown in F’ mateusi) and the

presence of the ring-like sclerite near base of the seminal

depository (Fig. 5A) which is lacking in F? mateusi (Sad-

owska-Woda & Gorczyca 2008: fig. 6).

©ZFMK

Fulvius yunnanicus sp. nov. 129

Fig. 6. Distribution of Fulvius yunnanicus sp. nov.

Acknowledgements. We express our sincere thanks to Petr

Kment (Department of Entomology, National Museum, Prague,

Czech Republic) for the loan of the material. We also thank two

anonymous reviewers for their useful comments and suggestion

on earlier versions of the manuscript.

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New Guinea (Hemiptera, Miridae). Revista Brasileira de Bi-

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Cassis G (2008) The Lattinova complex of Austromirine Plant

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Davis NT (1955) Morphology of the female organs of repro-

duction in the Miridae (Hemiptera). Annals of the Entomo-

logical Society of America 48: 132—150

Gorezyca J (2002) Notes on the genus Fulvius Stal from the

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Gorczyca J (2006) The catalogue of the subfamily Cylapinae

Kirkaldy, 1903 of the world (Hemiptera, Heteroptera, Miri-

dae). Monographs of the Upper Silesian Museum 5: 1—100

Gossner MM, Damken C (2018) Diversity and ecology of sap-

roxylic Hemiptera. Pp. 263-317 in: Ulyshen MD (ed.) Sap-

roxylic insects: diversity, ecology and conservation. Spring-

er, Heidelberg

Kerzhner IM, Konstantinov FV (1999) Structure of the aedea-

gus in Miridae (Heteroptera) and its bearing to supragener-

ic classification. Acta Societatis Zoologicae Bohemicae 63:

117-137

Kim J, Lim J, Jung S (2019) A taxonomic review of the fun-

gal-inhabiting plant bugs (Hemiptera: Heteroptera: Miridae:

Cylapinae) from the Korean Peninsula. Journal of Asia-Pa-

cific Biodiversity 12: 249-256. https://doi.org/10.1016/

jjapb.2019.01.006

Konstantinov FV (2003) Male genitalia in Miridae (Heterop-

tera) and their significance for suprageneric classification of

the family. Part 1: general review, Isometopinae and Psallopi-

nae. Belgian Journal of Entomology 5: 3-6

Pluot-Sigwalt D, Chérot F (2013) Donées biologiques et anato-

miques, régime alimentaire et taxonomie d'un nouveau Ful-

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vius afrotropical (Insecta, Heteroptera, Miridae, Cylapinae,

Fulviini). Zoosystema 35 (1): 45-68. https://doi.org/10.5252/

72013n1a5

Pluot-Sigwalt D, Matocq A (2017) An investigation of the roof

of the genital chamber in female plant-bugs with special

emphasis on the “dorsal sac” (Hemiptera: Heteroptera: Mi-

ridae). Annales de la Société entomologique de France (N.S.)

Sadowska-Woda I, Chérot F, Malm T (2008) A preliminary

phylogenetic analysis of the genus Fulvius Stal (Hemip-

tera: Miridae: Cylapinae) based on molecular data. In-

sect Systematics and Evolution 39: 407-417. https://do1.

org/10.1163/18763120878878429 |

Sadowska-Woda I, Chérot F, Gorczyca J (2006) Contribution

to the study of the female genitalia of twelve Fulvius species

(Heteroptera, Miridae, Cylapinae). Denisia 19: 617-636

Sadowska-Woda I, Gorezyca J (2008) Fulvius mateusi a new

species of Cylapinae from the Oriental Region (Hemiptera:

Miridae: Cylapinae). Genus 19 (1): 15-19

Wolski A (2015) Revision of the plant bug genus Xenocylapus

Bergroth (Hemiptera: Heteroptera: Miridae: Cylapinae), with

a description of Henryfulvius gracilis —a new cylapine genus

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and species from Ecuador. Annales de la Société entomolo-

gique de France (N.S.) 50 (3-4): 311-335. https://doi.org/

10.1080/00379271.2014.990251

Wolski A, Gorczyca J, Yasunaga T, Jindra Z, Herczek A (2018)

Taxonomic review of the bifenestratus species group of the

genus Fulvius Stal with descriptions of two new species (He-

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Yasunaga T (2000) The mirid subfamily Cylapinae (Heter-

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org/10.1163/22119434-99900044

Yasunaga T, Miyamoto S (2006) Second report on the Japanese

cylapine plant bugs (Heteroptera, Miridae, Cylapinae), with

descriptions of five new species. Pp. 721—735 in: Rabitsch W.

(ed.) Hug the bug — For love of true bugs. Festschrift zum 70.

Geburstag von Ernst Heiss. Denisia 19

Yasunaga T, Wolski A (2017) A new species and a new synon-

ymy of the plant bug genus Fu/vius from Japan (Hemiptera:

Heteroptera: Miridae: Cylapinae). Zootaxa 4232 (4): 588—

592. https://doi.org/10.11646/zootaxa.4232.4.10

©ZFMK

Bonn zoological Bulletin 69 (1): 131-140

2020 - Chandramouli S.R. et al.

https://do1.org/10.20363/BZB-2020.69.1.131

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:|sid:zoobank.org:pub:34 DFDE32-0BD3-4C49-8B25-87A82FA918A9

Status and distribution of the little-known and elusive Nicobarese worm lizard

Dibamus nicobaricum (Fitzinger in Steindachner, 1867)

(Squamata: Dibamidae)

S.R. Chandramouli'’, G. Gokulakrishnan’” & C. Sivaperuman*

' Department of Ecology and Environmental Sciences, School of Life Sciences, Pondicherry University, Puducherry

?3 Zoological Survey of India, Andaman and Nicobar Regional Centre, Haddo, Port Blair

* Corresponding author: Email: findthesnakeman@gmail.com

'urn:lsid:zoobank.org:author:73 BF7214-77B 1-45EA-A7FB-8CB13D15094F

2urn:Isid:zoobank.org:author:81676BC5-F41F-4A8A-853 1-FF9CBB282843

3urn:lsid:zoobank.org:author:08F28A 1 0-E80D-420C-924 1 -24F5CC199EB6

Abstract. Field surveys were carried out to record the elusive and little-known fossorial Nicobarese worm lizard Dibamus

nicobaricum (Fitzinger in Steindachner, 1867) on seven of the 23 islands of the Nicobar archipelago. It was recorded

from three new localities, two in Great Nicobar and the other from Teressa Island, extending the northern and southern

boundaries of its distribution significantly. One of the individuals, a subadult male recorded during this study happens

to be the smallest one ever recorded, measuring just 70 mm SVL. A predictive distribution model was developed based

on the geo-coordinates of its occurrence with a reliable prediction of 25—100% probability on islands of the central and

southern group of the Nicobar archipelago, diminishing to 12—25% on Car Nicobar, situated to the north. The Area Under

the Curve (AUC) of the model was 0.907, indicating a reliable prediction. Status of D. nicobaricum was assessed for the

first time as per the IUCN guidelines which reveal that it has to be considered as an endangered species based on its narrow

distribution range.

Key words. Nicobar worm-lizard, Dibamus nicobaricum, distribution, status, MA XENT model.

INTRODUCTION

Dibamids are one among the oldest living group of squa-

mate reptiles (Pyron et al. 2013). The genus Dibamus

Dumeéeril and Bibron, 1839 currently has 24 species (Uetz

et al. 2020) of which Dibamus nicobaricum (Fitzinger

in Steindachner, 1867) is one among the earliest known

species. The holotype was collected by G.R. Frauenfeld

from “Nicobars” during the global voyage of the Austri-

an Frigate “SMS Novara” and described originally by

Fitzinger in Steindachner (1867) as Rhinophidion nico-

baricum. In the same publication, Steindachner (1867)

reported on similarities between Rhinophidion Fitzing-

er, 1967 and Typhloscincus Peters, 1864 resulting in the

transfer of the species nicobaricum to Typhloscincus.

Later Stoliczka (1873) attributed this species to the genus

Dibamus Duméril & Bibron, 1839 where it is currently

placed. Dibamids, being fossorial and small bodied or-

ganisms, have remained extremely elusive and hence, not

many records of most species exist.

The Nicobar worm-lizard Dibamus nicobaricum has

been reported only a very few times since its original de-

scription. Stoliczka (1873) considered Dibamus nicobar-

icum to be a synonym of Zyphloscincus Martensii Peters,

Received: 11.09.2019

Accepted: 19.05.2020

1864 from Ternate Island, Indonesia (now Dibamus no-

vaeguineae). Annandale (1904), Humayun Abdulai (fide

Das 1996), Biswas and Sanyal (1977), and Das (1996)

are some of the authors who recorded this species from

Great Nicobar and Biswas and Sanyal (1980) recorded

it from Camorta in the Central group of Nicobar Islands

based on a single adult female specimen. Biswas and

Sanyal (1977) reported on morphological and sexual

variation within this species based on the examination of

three specimens. Based on an examination of the above

material and his own collection from Shompen Hut in

Great Nicobar, Das (1996) resurrected D. nicobaricum

from the synonymy of Dibamus novaeguineae to a dis-

tinct and valid species. Also, he considered the record

from Camorta to be doubtful (Das 1996: 160). Although

this species was discovered about a century and a half

ago there is an apparent lack of knowledge concerning its

biology, population structure and distribution within the

Nicobar archipelago. This deficiency of data also results

in the fact that its current status has not yet been assessed

according to IUCN criteria yet. Hence, the present study

was conducted to determine the status and distribution of

the Nicobar worm-lizard Dibamus nicobaricum.

Corresponding editor: W. Bohme

Published: 04.06.2020

132

S.R. Chandramouli et al.

Table 1. Morphology of two individuals of D. nicobaricum recorded during this study (measurements in mm).

Character

SVL 70

Tail length 1]

Body Width 2.9

Tail width 22

Head length 3.3

Head width 2.8

Head depth 2.8

Eye to nostril 2.5

Number of ventrals 218

Number of subcaudals 38

Midbody scalerows 23

Sex male

MATERIAL AND METHODS

Visual encounter survey method (following Crump and

Scott, 1994) was employed to collect data on the occur-

rence of the target species. Islands were selected in such

a way that at least one of each subgroup of islands was

represented and most of the relatively larger islands (with

geographic area > 50 km?) were included. The forests

were walked by foot and surveys were conducted for one

hour duration, wherein specific types of habitats such as

evergreen forests, semi evergreen forests, riparian for-

ests, coastal moist deciduous forests and plantations and

microhabitats such as leaf-litter, dry stream beds, but-

tresses and soil under rocks and decayed fallen logs were

carefully inspected for the presence of the target species.

One of the specimens recorded here from Teressa Island

was collected, preserved and deposited at ZSI ANRC

(Zoological Survey of India, Andaman and Nicobar Re-

gional Centre), Port Blair. Surveys were conducted both

during the day and night time. Logs were turned, leaf lit-

ter was disturbed, loose soil was dug and tree buttresses

were specifically examined in detail with a flash light to

detect the target species. Behavior of the individuals re-

corded during this study was observed in situ following

Altmann (1974). Photographic documentation was car-

ried out in the natural habitat, but upon capture. Mor-

phological characters namely, the number of scale-rows

at midbody, supralabials, infralabials, number of ven-

trals and subcaudals were examined with a magnifying

lens and the following measurements; snout-vent length

(SVL), tail length, body width, tail width, head length,

head width, head depth, eye-nostril distance were record-

ed using vernier calipers to the nearest 0.1 mm. All of the

survey locations were marked with a GPS and mapped.

Bonn zoological Bulletin 69 (1): 131-140

individual from Great Nicobar

ZSI/ ANRC (T)-7718 (Teressa)

107.6

24.5

7.4

6.6

6.1

5.5

3.5

183

male

The geo-coordinates of the survey locations were record-

ed with a Garmin 12 channel GPS and were pooled with

those based on literature records; thereby a consolidated

set of occurrence points was available to us. This set of

GPS points were used in a predictive distribution model-

ing based on maximum entropy algorithm — MA XENT v.

3.3.3 (Phillips et al. 2006). For making predictions of oc-

currence of the target species, climatic data were down-

loaded for the relevant tile from the Worldclim database

(Hijmans et al. 2005) and appropriately clipped to the

area of interest with DIVA GIS ver. 7.5. Based on these

predictions and the geo-coordinates of its occurrence, the

possible extent of occurrence and the exact area of occu-

pancy of D. nicobaricum was determined (derived from

Geocat: http://geocat.kew.org/). These were then used as

variables in the status assessment as per the IUCN norms

version 3.1 (IUCN 2012).

RESULTS

Three individuals were recorded from new localities

during this study; one from Govind Nagar, another from

Galathea Bay in Great Nicobar and the third one from

Kalasi in Teressa Island. Dibamus nicobaricum 1s record-

ed from Teressa Island in the central Nicobar Islands for

the first time and this also forms the northernmost record

of this species. Likewise, the one recorded from Galathea

forms the southernmost record. One of the specimens

from Govind Nagar (Fig. 1A) recorded during this study

is the smallest one ever recorded, measuring just 81 mm,

with 70 mm SVL. This specimen is described below in

detail.

©ZFMK

Status of Dibamus nicobaricum 133

fine

be eres f 2 J ; PERSE ee ==

Fig. 1. Dibamus nicobaricum recorded during this study in life: A— C: Govind Nagar, D - Galathea, Great Nicobar.

134

(a) Morphology (Figs 1-2)

Body vermiform; head blunt; neck and eyes indistinct:

nostrils located towards the snout tip, more ventral than

dorsal or lateral in position; rostral large, roughly as broad

as long, occupying '4 of the head length. Frontonasal

much broader than long; relatively smaller than frontal.

Frontal shield pentagonal with the vertex pointing poste-

riorly, slightly wider and fairly longer than the frontona-

sal. Ocular shield horizontally elongate, situated between

the edges of frontal and frontonasal shields; eyes locat-

ed underneath the ocular scales but visible. Postocular

single and fairly large. Two distinct supralabials visible

on either sides; anterior one much elongated and wedge

shaped; posterior relatively shorter and bordering ocular

and postocular shields. Mental shield small, bordered

by one infralabial (the first) on each side. Body scales

smooth, glossy and fairly imbricate. Forelimbs complete-

ly absent; two small skin-flaps situated on either sides of

the vent (immediately above), indicating the rudiments

of hind-limbs. Measurements and pholidosis of the spec-

imens examined are presented in Table 1. Dorsal body

unpatterned; uniform reddish brown in colour. Ventral

region more pinkish and slightly lighter than the dorsal.

S.R. Chandramouli et al.

(b) Distribution (Fig. 3)

Dibamus nicobaricum was recorded from three new lo-

calities during the present study, two of which are from

Great Nicobar, where it is already known and a first re-

cord from Teressa Island. An adult male was recorded

from Kalasi in Teressa Island, under the soil at about

5 cm depth in a coconut plantation (under exploitation)

and a juvenile male was recorded from under a log in

riparian habitat along the banks of a seasonal stream near

Govind Nagar, Great Nicobar (Fig. 4). Both these were

in dense evergreen forests under thick canopy cover. The

third individual was recorded from under a log in a lit-

toral forest in Galathea Bay, Great Nicobar, forming the

southernmost record for this species.

The MAXENT model predicted the distribution of

D. nicobaricum in Great and Little Nicobar islands with

occurrence probabilities ranging from 1 to 0.25 in Great

and Little Nicobar islands and islands of the Central

group, which diminishes to 0.12—0.25 in Car Nicobar,

the northernmost island of the Nicobar archipelago. AUC

(area under the receiver operating characteristic curve)

value was 0.908 with significant contributions by the

following variables: precipitation of the wettest month

Table 2. Percentage contribution of bioclimatic and physiographic variables to the model.

Variable

% contribution

Permutation importance

_biol3_29 a

_biol6 29 a

_biol7_29 a

_bi06 29 a

_bio7_29 a

_bio2 29 a

_biol 29 a

LibiglO+292a.

_biol8 29 a

_biolS5 29 a

_biol4 29 a

_bio9 29 a

_bio& 29 a

bios=29%.a

_bio4 29 a

_bio3 29 a

. DIGI2: 29a

_bioll 29 a

_biolO_ 29 a

_alt_29 a

Bonn zoological Bulletin 69 (1): 131-140

45.8 0)

42.5

720

47 0

41 1537

WES,

SO. OF Om: OS (OS. F OS * Os OS Oa SO

©ZFMK

Status of Dibamus nicobaricum 35

agement =

Fig. 2. Dibamus nicobaricum. A. Holotype of D. nicobaricum NMW 23461 (courtesy: Gernot Vogel). B. ZSI/ ANRC (T)-7718 col-

lected from Teressa, central Nicobars. C. Ventral view of an individual from Great Nicobar, in life. D. Ventral view of tail, showing

hindlimb rudiments (arrows).

136 S.R. Chandramouli et al.

92°30'0"E 93°0'0"E 93°30'0"E 94°0'0"E

Z Z

S >

i=) —)

a x

Zz. Z.

= =

rs a a

S oO

Teressa © ‘

Camorta

Zz. | Zz.

> x. >

> >

i: Katehall ancowry i

Z. z

= _S

7 ”

™ , ™

Little

Nicobar

Z Z

— —

> Great >

tm |

ome mc, Sut ct etl en) ed Som |

ie 18 30 40 Kilometers Nicobar

92°30'0"E 93°0'0"E 93°30'0"E 94°0'0"E

Fig. 3. Distribution records of Dibamus nicobaricum in the Nicobar archipelago. New records from this study marked in red.

Status of Dibamus nicobaricum 37

Fig. 4. Habitat of Dibamus nicobaricum near Govind Nagar in Great Nicobar.

(45.8%), precipitation of wettest quarter (42.5%), precip-

itation of the driest month (4.7%), minimum temperature

of coldest month (4.1%) and annual temperature range

(2.9%). The other factors pertaining to climate and al-

titude did not have any influence on the prediction (Ta-

ble 2, Figs 5—7).

Behavioural observations were made on the recorded in-

dividuals of Dibamus nicobaricum to observe its pattern

of activity in situ. The period of complete exposure of the

organism was very meager when compared to the dura-

tion spent underground. Whenever the animal ventured

under the soil surface, 1t always reached the bottom of

the container, burrowing through the soil nearly 2-3 cm

deep and resting underground. It voluntarily ventures

out above the soil surface very rarely (during day time).

This elusive behavior, its relatively small body size and

cryptic colouration could chiefly be the reasons behind

the very few records of this species till now. Majority of

the local people were not familiar with Dibamus nico-

baricum and could not recognize it based on the pictures

shown.

Bonn zoological Bulletin 69 (1): 131-140

(d) Status assessment of Dibamus nicobaricum

Based on the projected distribution maps and the number

of individuals observed and reported in literature until

now, it would be appropriate to regard Dibamus nico-

baricum as an ‘Endangered’ species as per the norms of

the IUCN criteria B1 (Extent of occurrence 3865 km”,

which is less than 5000 km?) and B2 (Area of occupancy

estimated to be 36.0 km’, which is less than 500 km”).

However, data on population of D. nicobaricum and its

fluctuation over a period of time are extremely difficult

to establish owing to its rarity, relatively small body size,

fossorial behaviour and elusive nature.

DISCUSSION

Dibamus nicobaricum has been recorded only a few

times since its original description in 1867. The present

study adds to the information on natural history, distri-

bution and behavior of Dibamus nicobaricum. Although

Dibamus nicobaricum was revalidated as a distinct

species by Das (1996), Honda et al. (2001) questioned

the validity of the Nicobarese species based on the fact

©ZFMK

138 S.R. Chandramouli et al.

0.00 - 0.12

0.12 - 0.25

0.25 - 0.38

0.38 - 0.50

0.50 - 1.00

kilometers

Fig. 5. Predicted distribution of Dibamus nicobaricum based on

occurrence points. Warmer colours denote higher occurrence

probability.

that Das (1996) failed to study the holotype housed at

the Natural History Museum of Vienna (NMW 23461)

and considered it to be a synonym of Dibamus leucurus

(Bleeker, 1860). In addition, they pointed at certain mor-

phological inconsistencies between the material reported

by Das (1996) as Dibamus nicobaricum and the holotype

that they have examined. Later, Das and Yakoob (2003)

argued based on data from the original description of the

species by Fitzinger (1867) and reinstated the specific

status of Dibamus nicobaricum. Originally described

as a member of the genus Rhinophidion, which is to be

treated as a neuter because of its termination “on” the

specific epithet nicobaricum was appropriate which is

also in neuter because of its termination “wm” and the

binomial was grammatically correct according to the

Art. 31.2 of the ICZN (1999). When Steindachner (1867)

referred this species to the genus Zyphloscincus, he er-

roneously amended the specific epithet to ‘nicobaricus’ .

Stoliczka (1873), who transferred nicobaricus to the ge-

nus Dibamus from Typhloscincus also retained the spe-

cific epithet with the masculine termination “us”. How-

ever, Das (1996) reinstated the correct specific epithet

by mentioning this species in the combination Dibamus

nicobaricum with a masculine generic epithet and a neu-

tral specific epithet, as per the original description. Lat-

er, Das (1999) changed it back to the name combination

Dibamus nicobaricus (sic.) with a masculine generic as

well as specific epithet. Likewise, the taxon authorship of

D. nicobaricum has sometimes been attributed to Stein-

dachner (1867) (e.g., Uetz et al. 2020). However, the cor-

Bonn zoological Bulletin 69 (1): 131-140

rect representation should be Fitzinger in Steindachner,

1867, because Steindachner (1867: 53) himself credited

the description of Rhinophidion nicobaricum to Fitzinger

by mentioning it as “Fitzinger in lit”.

Though Das (1996) included the Camorta locality in

the distribution of the species, he was skeptical about its

validity and expressed doubt on its authenticity assum-

ing that the locality could be in error and emphasized

the need for its verification. During the present study,

Dibamus nicobaricum has been recorded from Teressa

Island, located further northwest (~ 40 km) of Camor-

ta, which endorses the earlier record from Camorta by

Biswas and Sanyal (1980), thereby extending the north-

ern boundary of its distribution range significantly. Like-

wise, the new record from Galathea Bay in the southern

extremity of Great Nicobar Island extends its known

distribution range further southwards by at least 30 km.

Its confirmed presence in Camorta, Katchall and Teressa

Islands in the central group of the Nicobar archipelago

make its occurrence on other islands of this group such as

Nancowry, Tillanchong and Bompaka highly probable.

Also, there is a high probability of its occurrence in the

intervening Little Nicobar Island. Records of D. nicobar-

icum have been relatively rare since its description and

information on abundance of the species is hard to obtain

due to its elusive and fossorial lifestyle. Hence, this spe-

cies has been considered data deficient by the IUCN until

now. Based on the projected distribution maps and the

number of individuals observed and reported 1n literature

and the present study, it would be appropriate to regard

Dibamus nicobaricum as an ‘Endangered’ species as per

the norms of the IUCN criteria B1 (Extent of occurrence

less than 5000 km?) and B2 (Area of occupancy less than

500 km?). Several aspects of this species, such as breed-

ing biology, feeding ecology and population estimates

still remain unknown. Further studies on such specific

aspects would provide us more insights about the endan-

gered and narrowly endemic Dibamus nicobaricum.

Acknowledgements. SRC thanks the Department of Environ-

ment and Forests of Andaman and Nicobar Islands for permis-

sion, K.V. Devi Prasad and the faculty of the Department of

Ecology and Environmental Sciences and the Department of

Ocean Studies and Marine Biology, Pondicherry University

for the support and hospitality. This paper is an outcome of a

grant (No: 160514249) from the Mohamed bin Zayed Species

conservation Fund. Gernot Vogel kindly provided data and pho-

tographs of the holotype of Dibamus nicobaricum housed at

the NMW, Vienna. We thank the Director of Zoological Survey

of India, for his encouragement and support to undertake the

survey in Andaman and Nicobar Islands. SRC is grateful to R.

Whitaker for recommending this study.

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Fig. 6. Jackknife test of variable importance to the model.

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Bonn zoological Bulletin 69 (1): 141-155

2020 - Steenis, J. van et al.

https://do1.org/10.20363/BZB-2020.69.1.141

ISSN 2190-7307

http://www.zoologicalbulletin.de

Research article

urn:lsid:zoobank.org:pub:787328A 5-4082-4677-858C-867962B56395

First records of Chrysotoxum volaticum Séguy, 1961 from Europe

and Platycheirus marokkanus Kassebeer, 1998 from Spain

(Diptera: Syrphidae) together with additional records

of Spanish Chrysotoxum Meigen, 1803

Jeroen van Steenis'*, Menno P. van Zuijen2, Antonio Ricarte’, M. Angeles Marcos-Garcia‘, Dieter Doczkal,

Axel Ssymank® & Ximo Mengual’

‘Naturalis Biodiversity Center, Leiden. Hof der Toekomst 48, NL-3823 HX Amersfoort, The Netherlands

? Kolkakkerweg 21-2, NL-6708 RK Wageningen, The Netherlands

4 Centro Iberoamericano de la Biodiversidad (CIBIO), University of Alicante, San Vicente del Raspeig 03690, Alicante, Spain

*Klingelackerweg 10, 76571 Gaggenau, Germany

° Falkenweg 6, 53343 Wachtberg, Germany

’Zoologisches Forschungsmuseum Alexander Koenig, Leibniz-Institut fiir Biodiversitat der Tiere, Adenauerallee 160,

D-53113 Bonn, Germany

* Corresponding author: Email: jvansteenis@syrphidaeintrees.com

'urn:Isid:zoobank.org:author:C7FOD0O1C-B182-4B93-AF73-E4 154367B535

2urn:Isid:zoobank.org:author:C82093D8-EE58-47DD-B13A-4F47BDF73911

3urn:Isid:zoobank.org:author:3 C2 FCE66-9DDF-4E8A-BDO0D-96BB01C238D8

4urn:Isid:zoobank.org:author: EBDD4FE8-EBA6-4E40-A EC3-9B4EED6E7C98

Surn:|sid:zoobank.org:author:79800F7A-AA21-4948-A D64-619BDSFCBB98

6urn:lsid:zoobank.org:author:58B9D453-586C-4B08-BAD6-BCC606E3D654

7urn:Isid:zoobank.org:author:A5093 10D-B567-4830-B8A4-BCB139BB8768

Abstract. The first European records of Chrysotoxum volaticum Séguy, 1961 from Spain and France, and Platycheirus

marokkanus Kassebeer, 1998 from Spain are provided. These are further examples of North African species also present

in the Iberian Peninsula. Diagnostic characters are given to separate C. volaticum and the similar Chrysotoxum bicinctum

(Linnaeus, 1758), and additional records of other Chrysotoxum Meigen, 1803 hoverflies from Spain are also reported. We

also provide DNA barcodes for C. volaticum and discuss the utility of DNA barcoding to identify species in the genus

Chrysotoxum.

Key words. Ibero-Maghreb fauna, new species records, France, Spain, diagnosis, DNA barcoding.

INTRODUCTION

Syrphidae is a species rich family of Diptera which has

received much attention during the last decades. Adults

of this family are often wasp and bee mimic flower vis-

itors, while larvae have very different feeding modes

(Rotheray & Gilbert 1999, 2011). Adults of many spe-

cies are important pollinators (Ssymank & Kearns 2009;

Inouye et al. 2015), predatory larvae are important for

pest control (Bugg et al. 2008, Pineda & Marcos-Garcia,

2008; Amoros-Jiménez et al. 2012) and saprophagous

larvae in the decomposition of organic material (Lardé

1989; Rotheray et al. 2009; Martinez-Falcon et al. 2012).

The large amount of knowledge we now have about this

family in Europe and the interest syrphids provoke in

many academic and applied fields has led the internation-

al organisation IUCN to develop a European red list for

Received: 05.04.2020

Accepted: 22.05.2020

Syrphidae (IUCN 2018). The data here reported will help

the preparation of a red list from Spain.

MATERIAL AND METHODS

Morphological terminology follows Thompson (1999).

The examined material originates from different col-

lecting events in Spain and France in the last decades.

The species were identified using original descriptions

(Séguy 1961; Kassebeer 1998) and other literature (Niel-

sen 1999; de Courcy Williams et al. 2011; Nedeljkovic

et al. 2013; Speight et al. 2013; Young et al. 2016). Many

Spanish specimens were collected in the ‘Sierra de Al-

caraz’, in the province of Albacete, a low mountainous

area with open Pine forests with Mediterranean maquis

(Van Steenis et al. 2017). The information provided under

Corresponding editor: R. Peters

Published: 04.06.2020

142 Jeroen van Steenis et al.

‘Examined material’ is given in the order of region or

province, area and locality with an indication of the alti-

tude, collecting date, in which a range is indicated with

“_» the collector, without adding “leg.” in the material

studied section, and in some cases a specimen identifying

number, rather than the precise label information.

The figures were made by the first author by stacking

multiple photos in Zerene Stacker ver. 1.04 and then fur-

ther edited with GNU Image Manipulation Program ver.

2.8.22. Each individual photo was taken with Cognisys

StackShot at fixed intervals with a Canon EOS D6 SLR

camera, a Canon MP-E 5x macro-zoom with a Yongn-

uo YN14EX ring flash attached. The colour plates were

made with the aid of a Zeiss camera lucida on a Zeiss-ste-

reomicroscope SV11 by Axel Ssymank.

Abbreviations for depositories / collections

AET = private collection of André van Eck, Tilburg,

the Netherlands

ASW_ = private collection of Axel Ssymank

CEUA = Coleccion Entomologica de la Universidad

de Alicante, CIBIO Institute, Alicante, Spain

CPP. = private collection of Chris Palmer,

Portsmouth, United Kingdom

DDG _~ = private collection of Dieter Doczkal,

Gaggenau, Germany

JSA = private collection of Jeroen van Steenis

MNCN = Museo Nacional de Ciencias Naturales,

Madrid, Spain

MNHN = Muséum National d’ Histoire Naturelle,

Paris, France

MRL = private collection of Menno Reemer, Leiden,

the Netherlands

MZW_ = private collection of Menno van Zuijen

NBC = Naturalis Biodiversity Center, Leiden,

the Netherlands

NHM-~ = The Natural History Museum, London,

SBH = private collection of Sander Bot, Haren,

the Netherlands

The 5’ region of the cytochrome c oxidase subunit I (COT)

gene, the so called DNA barcode (Hebert et al. 2003a,

2003b) was obtained from three specimens of Chrysotox-

um volaticum Séguy, 1961. Meso- and metalegs from dry,

pinned specimens were used for DNA extraction. The

extraction protocol follows Mengual et al. (2018) and the

specimens were preserved and labelled as DNA voucher

specimens for the purpose of morphological studies and

deposited at the CEUA. DNA primers and PCR amplifi-

cation protocols follow Rozo-Lopez & Mengual (2015).

Bonn zoological Bulletin 69 (1): 141-155

RESULTS

Both Chrysotoxum volaticum and Platycheirus marok-

kanus have been mentioned to occur in Europe (Ssy-

mank & Doczkal 2007; Van Steenis & Van Steenis 2014),

but only records of P. marokkanus have been documented

so far (Van Eck 2016).

Since Séguy’s original description, Chrysotoxum vola-

ticum has been reported only from Morocco by Claussen

(1989) and Claussen & Hauser (1990). The original de-

scription of C. volaticum is not very informative and this

species is missing from most identification keys. Thus,

we provide here a table (Table 1) of diagnostic characters

and a key to distinguish it from the similar Chrysotoxum

bicinctum (Linnaeus, 1758).

Chrysotoxum bicinctum (Linnaeus, 1758)

Distribution. Widespread throughout Europe, possibly

very rare in the Iberian Peninsula. In Spain, records of

this species are confirmed just from the provinces of As-

turias, Cantabria and Lérida.

Material examined. Many records in the authors’ col-

lections throughout Europe. Spain: 14 (CEUA), Astur-

ias, Santillan, 6-VII-1986, M.A. Marcos Garcia (26b),

[det. as C. bicinctum form A by A. Ssymank in 2009];

12 (CPP), Cantabria, Potes, Las Ilces, 43°06’41” N,

4°45°27” W, 754 m, 26-VI-2017, C.J. Palmer; 19

(CPP), Girona, Setcases, 26-VIII-1996, C.J. Palmer:

1° “yellow” (SBH), Lleida, Bordes de Graus, camping,

42°40°07” N 1°14°14” E, 1321 m, 4-VII-2019, S. Bot; 19

(SBH), Lleida, near Tavascan, 42°40’59” N, 1°13’59” W,

1400 m, 29-VII-2013, S. Bot; 14 (NBC), Lleida, Vall

d’Aran, VIII-[19]45; 14 (CEUA), Santander, Vada, 22-

VI-1987, M.A. Marcos Garcia (34).

The two CEUA males were already published as C. bi-

cinctum in Marcos-Garcia (1990) and are here confirmed

to belong to this species.

Remarks. This species is similar to Chrysotoxum volat-

icum and was, until recently, confused with this species

in Europe (Ssymank & Doczkal 2007). Note that there

is a form of C. bicinctum resembling C. volaticum in the

more extensively dark coloured wing (Fig. 3F). These

specimens are common in the UK and Scandinavia and

are generally darker (Figs 2C, 2D), with dark legs, dark

abdomen and dark-brown to entirely black (as in Figs 4A,

4C) mouth edge and hypostomal bridge. In the Pyrenees,

intermediate forms are also found with a combination of

characters in-between C. bicinctum and C. volaticum in-

dicating possible hybridization.

There is one female (Spain, Pyrenees, coll. SBH) with

black mouth edge and hypostomal bridge as in C. vola-

ticum and a short wing macula, a black frons with small

©ZFMK

First records of Chrysotoxum volaticum from Europe and Platycheirus marokkanus from Spain

pollinose maculae and narrow fascia on tergum IV as

in C. bicinctum. Two other females (coll. SBH, Spain

Lérida and France, Pyrenees) have a yellow hypostomal

bridge, a black frons and a short wing macula as in C. bi-

cinctum, but large pollinose maculae on the frons and

a wide yellow fascia on tergum IV as in C. volaticum.

These all could be females of C. bicinctum in which the

last two are “yellow” forms in which the pollinose macu-

lae on the frons are larger. There are three males (France,

Pyrenees, coll. SBH), sympatric with one of the “yellow”

females, which seem to be more straightforward iden-

tified as Chrysotoxum volaticum, although the frontal

pollinosity, the frontal colour and the colouration of the

scutellum seem to be more like in C. bicinctum.

143

Chrysotoxum volaticum Séguy, 1961

Distribution. Originally described from Algeria and

Morocco (Séguy, 1961). Recently recorded from Moroc-

co (Claussen, 1989; Claussen & Hauser, 1990). Dirickx

(1994) also reported this species in the Mediterranean

region of Morocco.

New to Europe and found in France, Portugal and

Spain.

Material examined. Type series: 2 3, 3 9, “Moyen At-

las, Ifrane (Morocco), VI-[1]949”, “Museum Paris 1949

L. Chopard”; 1 3 “Setif, Algérie, coll. Théry”, “Museum

Paris, Algérie, Setif A. Théry 1902” (MNHN). France:

2 2 (MRL), Cevennes, Causse Blandas, 10 km SW Le

Vigan, 43°54’56” N, 3°28°51” E, 800 m, 20-VHI-2014,

M. Reemer; 1 2 (JSA), Languedoc-Roussillon, Prades,

Table 1. Differentiating characters between Chrysotoxum volaticum and C. bicinctum.

Colouration of wing

Chrysotoxum bicinctum

Dark macula on wing margin shorter

Chrysotoxum volaticum

Dark brown to black on anterior margin, reaching

Scutellum in dorsal view

Frons, colour around

the lunulae on frontal

prominence

Pollinosity on frons

Ratio: length of eye

contiguity/ ocellar triangle

(males only)

Tergum III

Tergum IV

Genae and hypostomal bridge

never reaching wing apex and usually

ending as a broad blunt spot above

the bow of vein R4+5, usually apical

border of dark wing macula clearly

demarcated. In dark specimens radial

cell R1 also darkened and outer apical

border diffuse

Almost completely black, with a

narrow yellow posterior margin.

In bright specimen two narrow yellow

or obscured small maculae may be

present basally, in males sometimes

fused to a narrow basal yellow line

Complete frons dark brown to black;

lunulae itself mostly dark brown to

black, rarely obscurely yellow or in

some specimen yellow

Males: narrow pollinose fascia white

Females: pollinose maculae smaller,

leaving about '/s—'/ of the frons free in

the middle

Eye contiguity often distinctly longer

than ocellar triangle, Ratio ca. 1.1—1.3

Black usually with very narrow yellow

fascia or well developed yellow pair of

maculae, however dark specimen have a

completely dark terum III

Yellow fascia narrow, usually

0.2—0.4 of length of tergum IV, in light

specimens wider

Genae below eyes with a black vitta,

but hypostomal bridge clearly yellow,

in dark specimens genae black and

the wing apex, Radial cell R1 completely darkened

and dark patch extending distinctly beyond the tip

of this cell, dark spot in cell R2+3 reaching costa

for up to about % of its length within this cell,

wing patch apically and on posterior margin clearly

demarcated, sometimes reaching backwards to join

R4+5 apically

Scutellum largely yellow with scarcely visible

narrow black fascia basally and a black median fascia

of varying extent:

Females usually with broad median black fascia of ca.

0.50.7 x of length of scutellum

Frons laterally and posteriorly of lunulae yellow.

However, the yellow part may be largely obscured

with only laterally some dark-yellow colour

Males: narrow pollinose fascia yellowish

Females: pollinose maculae large, almost touching,

narrow non-pollinose line in between usually less than

'/s of width of frons

Almost the same length,

Ratio 0.9-1.1

Black with a very narrow yellow posterior margin,

rarely also with small yellow maculae

Yellow fascia broad, usually 0.4—0.75 of length of

tergum IV,

Genae below eyes and hypostomal bridge usually

completely black or with dark brownish patches

on the sides; a few individuals may have an almost

hypostomal bridge dark-brown to black

Bonn zoological Bulletin 69 (1): 141-155

yellow mouth edge

©ZFMK

144 Jeroen van Steenis et al.

Fig. 1. Adult habitus. A. Lateral view. B—D. Dorsal view. A. Chrysotoxum bicinctum, 2°, Sweden. B. C. bicinctum, 3, Sweden.

C. C. festivum, 4, Spain. D. C. volaticum, 3, Sierra de Alcaraz. Scale bars: 2.5 mm.

Les Sauterelles, 42°34’15” N 2°24’49” E, 785 m, 12-

VIUI-2014, J. van Steenis; 19 (JSA), Vernet les Bains,

Col de Mantet, 42°28’50” N 2°18°53” E, 1765 m, 17-

VIII-2014, J. van Steenis; 3 3 (SBH), Pyrenees, Vallée

d’Eyne, 42°28’05” N, 2°05’17” E, 1650 m, 23-VIH-2013,

S. Bot; 1 6 (NBC), Pyrenees Orientales, Font Rocheu,

11-VII-1965, J. v.d Vecht; 1 9 (NBC), Pyrenees Oriental-

es, Fillols, 10-VII-1965, J. v.d. Vecht; 1 2 (NBC), Vau-

cluse, Carpentras VI-1953, P.M.F. Verhoeff; 12 9 (NBC),

Vaucluse, Carpentras, 1—3-VIII-1953, P.M.F. Verhoeff:

Morocco: 2 2 (NBC), Toubkal Massif, Oukaimeden,

2500-2800 m, 2—8-VII-1977, v. Oorschot, Houkes &

Oosterbroek; 1 2 (NBC), Arhbalou, 43 km S. Marra-

kech, route $513, 1000 m, 3—14-VII-1977, v. Oorschot,

Houkes & Oosterbroek; Portugal: | 2 (NBC), Doure,

Resende, 16—19-VII-1953, P.M.F. Verhoeff; 1 9 (AET),

Braga, Gilmonde, Barcelos, 41°29’02” N 8°46’00” W,

22-V-2012, R. Andrade; Spain: 1 3 (JSA), Albacete,

Sierra de Alcaraz, Batan del Puerto, 38°34’ N 2°21’ W,

1200 m, 21-VI-2003, J. van Steenis; 2 6, 1 9 (JSA),

3 2 (MZW), Sierra de Alcaraz, Puerto de las Crucetillas,

38°31’ N 2°26’ W, 1400 m, 21-VI-2003, J. van Steenis &

M.-P. van Zuijen; 1 6, 1 2 (MZW), Sierra de Alcaraz,

Puerto de las Crucetillas, 38°32’ N, 2°24’ W, 1100 m, 21-

Bonn zoological Bulletin 69 (1): 141-155

VI-2003, M.P. van Zuijen; 1 4, 1 2 (JSA), 12 (MZW),

Sierra de Alcaraz, Puerto de las Crucetillas, 38°32’ N,

2°23’ W, 1000-1200 m, 22-VI-2003, J. van Steenis &

M.P. van Zuiyen; 1 2 (JSA), Sierra de Alcaraz, Cafiada

del Provencio, 38°31’ N 2°20’ W, 1000 m, 22-VI-2003, J.

van Steenis; 1 4 (NBC), Andalucia, Prado Llano, 23-VII-

1980; 1 9 (NBC), Andalucia, Prado Llano, 24-VII-1980;

12 (NBC), Vadillo Castril, Sierra de Cazorla, 3-VIII-

1980; 5 4 (MRL), Andalucia, Sierra Nevada, 2 km N of

Trevelez, 25-VI-2003, M. Reemer; 1 4 (MRL), Andalu-

cia, Sierra Nevada, Trevélez, 37°00’47” N, 3°15°47” W,

1600 m, 10-VI-2019, M. Reemer; 1 9 (CEUA), Avila,

Becedas, 6-VII-1977, M.A. Marcos-Garcia; 2 5 (ASW),

3 3, 1 2 (DDG), Castilla la Mancha, Sierra de Alcaraz,

Ridpar, 38°30°17” N, 2°27°36” W, ca. 775 m, 14-VI-

2003, A. Ssymank & D. Doczkal; 4 3, 1 2 (ASW),

53, 12 (DDG), Sierra de Alcaraz, Espinares de Leon,

38°32715” N, 2924718” W, ca. 1380 m, 14-VI-2003, A.

Ssymank & D. Doczkal; 3 9 (CEUA), Ciudad Real,

PN. Cabafieros, respectively 20-V-2005, 5-VII-2005,

24-VIII-2005, A. Ricarte; 3 4 (NBC), Gerona, Ribas de

Freser, 900 m, 25-VII-1970, V.S. v.d. Goot; 1 4 (NBC),

Gerona, Ribas de Freser, 900 m, 26-VII-1970, V.S. v.d.

Goot; 2 4 (NBC), Gerona, Mollo, 1300 m, 17-VII-1970,

©ZFMK

First records of Chrysotoxum volaticum from Europe and Platycheirus marokkanus from Spain 145

Fig. 2. Adult habitus, dorsal view, all from Sierra de Alcaraz. A. Chrysotoxum cisalpinum, °. B. C. gracile, 2°. C. C. octomacula-

tum, 2. D. C. octomaculatum, 2, dark form. Scale bars: 2.5 mm.

VS. v.d. Goot; 2 6 (NBC), Gerona, Ribas, Zariquiey; 1 9

(NBC), La Rioja, dal v Najerilla, S. of Najera, ca 10 km

S. of Anguiano, 22-VH-—10-VII-1988, PJ. v. Helsdin-

gen; 2 9 (NBC), Gerona, Ribas de Freser, 900 m, 21-

VI-1970, V.S. v.d. Goot; 1 9 (NBC), Gerona, Ribas de

Freser, 900 m, 25-VI-1970, V.S. v.d. Goot; 1 9 (NBC),

Gerona, Mollo, 1300 m, 19-VH-1970, VS. v.d. Goot; 1 2

(NBC), Gerona, Sant Ilari de Sacala, VIII-1969, Serra:

1 3 (NBC), Granada, Capileira, 22-VII-1969, H. Over-

beek; 1 9 (NBC), Montseny, St Pere de Vilamajor, Sagar-

ra; 2 2 (NBC), Guadalajara, Tierzo bei Mo[illegible]na,

1100 m, 11-VII-1977, W. Schacht; 1 3 (NBC), Guada-

lajara, Tierzo bei M[illegible], 1100 m, 11-VII-1977, W.

Schacht; 2 4 (NBC), Huesca, Torla, 1036 m, 8—26-VII-

1974, J. Wolschrijn; 1 9 (MNCN), Huesca, San Juan de

la Pefia, 1220 m, Exp. Inst. de Entomologia, 4-VIII-1943,

Chrysotoxum bicinctum (L, 1758) Peris Torres det. 1945;

Bonn zoological Bulletin 69 (1): 141-155

1 3 (MNCN) Jaén, Sierras de Segura, El Pardal, VI-

1903, Escalera; 1 4 (CEUA), Leon, Valdetejas, 1200 m,

13-VII-1977, M.A. Marcos-Garcia; 1 2 (NBC), Lerida,

Alamacellas, Zariquiey; 14 (MNCN), Madrid, Escorial,

Coleccion Lauffer, Chrysotoxum bicinctum L, det Strobl;

Escorial, VHI-1905, Mercet, Chrysotoxum bicinctum L,

Gil Collado det; 1 9 (CEUA), Salamanca, Béyar, 5-VII-

1978, Carmen Calvo; 3 3 (CEUA), Fresnedoso, 3-VII-

1978, Gonzalo Llorente; 1<' (CEUA), Palomares-Béjar,

10-VII-1978, Gonzalo Llorente; 1 4 (CEUA), Porteros,

14-VI-1981, M. Portillo, Th. villosa; 1 4 (CEUA), Valle-

josa de Riofrio, 15-VI-1979, Gonzalo Llorente; 1 9

(NBC), Nuria, 1800-2000 m, 22-VII-1970, VS. v.d.

Goot; 1 29 (MNCN), Segovia, San Ildefonso, VI-1906,

Escalera; | 9 (CEUA), Valencia, Chelva, 7—21-VI-1994,

C. Pérez-Bafion; 1 9 (CEUA), Requena, 22-VI-1994, C.

Pérez-Bafion; 1 4, Utiel, 7-VI-1994, C. Pérez-Bafion;

©ZFMK

146 Jeroen van Steenis et al.

Fig. 3. Habitus and wing. A. Chrysotoxum volaticum 3. B. C. volaticum 2 with wing. C. Wing of C. volaticum 3. D. C. bicinctum,

typical form & with wing. E. Wing of C. bicinctum, typical form 3. F. Wing of C. bicinctum form’ A’ from Brandenburg, Germany.

First records of Chrysotoxum volaticum from Europe and Platycheirus marokkanus from Spain 147

Fig. 4. Details of head and scutellum. A. Chrysotoxum volaticum @, head in lateral view. B. C. volaticum 4, head ventral view.

C. C. volaticum ° head ventral view. D. C. bicinctum, typical form @, head in lateral view. E. C. bicinctum 3 head ventral view.

F. C. bicinctum 8 head ventral view. G-H. C. bicinctum, typical form & scutellum, dorsal and lateral view. I. C. bicinctum form

"AN J scutellum, dorsal view. J, L, N. C. volaticum & scutellum in dorsal and lateral view, normal colouration. K, M. C. volaticum

1 ¢ (NBC), Sierra Alta, 1600-1800 m, 26-VII-1965,

VS. v.d. Goot; 1 9 (CEUA), Santander, Vada, 22-VI-

1987, M.A. Marcos Garcia (34); 1 3 (NBC), Tarrago-

na, Prades, 900 m, 1—10-VII-1967, H. & T. v. Oorschot,

J. & M. Lourens; 1 3 (NBC), Teruel, Sra de Albarracin,

Noguera, 1600 m, 12-VII-1977, W. Schacht; 1 4 (NBC),

Teruel, Sierra de Albarracin, Noguera, 1600 m, 3—6-VIII-

1980, W. Schacht; 1 9 (NBC), Teruel, Bronemales; 1 9

(NBC), Teruel, Aguas Amarguas, 1620 m, 21-VII-1965,

VS. v.d. Goot; 3 2 (NBC), 24-VII-1965; 2 2 (NBC), 29-

VI-1965; 1 9 (NBC), Teruel, Sierra Alta, 1600-1800 m,

26-VII-1965, V.S. v.d. Goot; 3 2 (NBC), Teruel, Pajar-

es, 1000 m, 20-VII-1972, VS. v.d. Goot; 1 2 (NBC),

Bonn zoological Bulletin 69 (1): 141-155

Teruel, Puerto de Pajares, 1350-1700 m, 21-VII-1972,

VS. v.d. Goot; 3 2 (NBC), 22-VII-1972; 1 2 (NBC),

Teruel, Santa Croche, 1150 m, 5-VIII-1965, V.S. v.d.

Goot; 1 9 (NBC), Teruel, Santa Croche, 1150 m, 5-VIII-

1965, V.S. v.d. Goot; 1 2 (NBC), Teruel, Sierra de Al-

barracin, Nogueta, 1600 m, 3—6-VIII-1980, W. Schacht;

2 9 (CEUA), Jaén, PN. Cazorla, Coto Rios, Llanos

de Arance, 38°03’12.1” N, 02°50°10.6” E, 641 m, 13-

VI-2019, A. Ricarte (ZFMK-DIP-00067297, ZFMK-

DIP-00067298); 1 3 (CEUA), Jaén, Coto Rios, meadow

in riverbank opposite Fuente de la Pascuala camping site,

38°03’ 13” N, 2°50’09” E, 641 m, 29-V-2018, E. Galante

(ZFMK-DIP-00067299).

©ZFMK

148 Jeroen van Steenis et al.

Fig. 5. Head; A. Dorsal view. B—D. Lateral view. A. Chrysotoxum cisalpinum, 3, Sierra de Alcaraz. B. C. festivum, 2, Spain.

C. C. volaticum, 2, Sierra de Alcaraz. Scale bars: 1.0 mm.

Remarks. This species is similar to Chrysotoxum bicinc-

tum, differing by the characters mentioned in Table 1.