Bull. nat. Hist. Mus. Lond. (Zool.) 65(2): 73-122 Issued 25 November 1999

Systematics and phylogeny of Zausodes

C.B. Wilson, 1932 (Copepoda, Harpacticoida,

Harpacticidae), including three new species

from the northern Gulf of Mexico

LORI BOUCK

Department of Oceanography, Florida State University, Tallahassee, FL 32306-4320, USA a NOW 19 09 .

DAVID THISTLE’ busy te eee |

Department of Oceanography, Florida State University, Tallahassee, FL 32306-4320, USA a ee Pr . tt ISR ARY ;

RONY HUYS inlet hapa toh

Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD

CONTENTS

NNER OULU ULON MES meee ag cote rte tee cent cet dade e ace oe ORME TPS NR escola n ete Eaten a cieeak ges adasa dant fash taccwsensnn tay ecesvaraths aetncadeatarcteRecaiace

Materials and Methods ..........

SIWGLGUTAE LULES ceecee Beco ence ECPer EP ERRCEC OPEC COEP ee CEPECEEEEEE

Family Harpacticidae Dana, 1846 ................

Genus Zausodes C.B. Wilson, 1932 ........:0ccc0 a

AGUS ODES GKCRIGO LUSK Gs Ea VOISOM LO Sicoterszaese ts nes dese so aveocsash Siege ae teduapeaserhr AMets cua deadecad cee cca Sedasaucereesentaantecrenacecussereccascee is

LATS OLE SUSE POET IUT) Sy Me UIA NGS hr wees op ap BR We Sac So nage anna cn tee cadns tects wat he maenes eon canes cdbuetedes sareus eiscaceenanaedh cevedecntemscasteeeees 81

GSTINISH NEOZCESO ESTO ENNIO. © csscce ce cnatdcane exer ee ces tarse tata owen az cone cecuenatevte ce tase rane nese hacaeiea tua sapewen eon cis gonenves Ace cvUnscactunnetec rates 81

NeOzanSodesarcalaius (Geddes M9 GGa) COMI MOVs: <.is..c<.cccrtcseasadesncnescesanssasqcrstessccusstabasoenatsncduccstcucevdvacausteeraesessbavet des 84

INCOZQUSOGES MINISERIES AKO Disa L954) (COMID NTO) apts acnsacsanacessoncsdesnanessnsasonaseouceenaucrancsnsnossdencssansccvctdcpdstepesctssatusieeonsee 89

Neozausodes paranaguaensts (JakObi; 1954)\ COM: TOV. ..c:kckassccssceacctceccestsctecvescousasacscostucvesevaceorssesacucecowsavens seroaeeaeceses 89

INCOZAUSOHES SIGMUTEEL (LAKODI, AUS 54 COMI OIL Wareire a. aissuns agateeeneae tctlawe aa te daSenassdatediadau denvaes dete tudes davpedtenancan eeeadeekecnerenete 9]

INGQdaUSOdeNSOXTUS, (Team 2 51965) COMM: NOV, axa casnsncsasacsncensccateetet cc case dicdels ds sadvesssvexarttvets stesuey daenevsenasstuctvoaMMyatactecs:cerstersas 91

INCOZAUSGAGS SRULENDETRETUSP: NOV. ssascacsasxecencxancennevarsacsuvedsvacdaeecevias te dsVouadave boneddead uieotedar<ied¥adaiassoaconttuneevacieessessesatyan cz 9]

Gems Mifcronedid) Semenov, Seek cce Nectar ees BELEN Ge cs asceseveswd cacepenystie the vetitaos vastus owesVouey cbnues oupds genussatesaavieviceperssess caoreti eden 96

WUMCKO PCIE COOKOTUMUSD NOV. xanwens saansss sacancntveaeeavesenaechaetteanuee abewasNowe dee sx adder cu avaoereusiuion eussfaqewsdevescezededeteu= acura evedgsescexds 96

WVIVCY ODE AIGA ESTE RE GAS DSTO WG o. areae cesta Grete ategt a ae ok cscs ca gan egy patra cd gus seen tad anda teseaenencastscaxcvcsaneenteeascasundevessnaceasseacene 107

GenUSATCHIAUSOGES)| BEM. TOV... ccscsucsasaseseceasceranceacssennssannneacdonnasaaveuses caxasase dasentus cagedatnsexcaveseatuacaneastwansicacddexsesaadaanstesseoesstese 113

AVC RUZEUSOGES! DIGTIGHICES (LLO#, 19179) | COMMS TION dace «nosa-ncecce-cvsreste=-27 cuseseeagaace: ste WacencsnecacadesaehcssnsencessarsiecesensGeceancerset 113

PRG Si yates Sette st eee cms ce vc cen entene es Mecr es Revc esas cuncses acaxe ie Safastias essa an sind CoRedt eel che acne udaus van euaeadsaavadeat (saeneres \Vavuauesivasunperiacdcoie vane 113

SHE CULO MUU OM COMOND preset sea tence en cca NC gare e aerate hater nace sSe Sx <WaeeRae Pana tes eat ou encenets sunk ve ceeere net cusenedoeScerevedosaaduecrteses 113

Monpholapicallk ChavaGlenrs ho vcrc.ter nceacstysencehaaessarcstucdeardeccssens veassananatdoneavctmsses taasvscvsinecNont ecucusseracedasouseuucvsshsucevcetoaevesevereneesicesee 116

PSD eatreduimn ted eg eATA Gs AV ALY SUS cos paz successes cee ea eccs eas supteu seee tvs saeaesesee cect ses. sadaciasoreta such vasquaeact4eanauh sucegonssackeNicdsaanatisdwessesveseseas sceocoseieedes )

FRE SUREESY ACU ALS CUES ST OM yeast nce ctu anes ep taka sen Cate eae Eat nde ek oak suas eteatetacteesastentatnestarucaresvesensnt scosaceetatceorsartaeetesvsuceverves 119

Status of Zausodes cinctus Krishnaswamy, 1954 121

Acknowledgements 122

TREE REMC ES erace sae wesw cre teen ree eraser eta enc See sas inne Saceasrviesaseersecavestssseosts aazdasasws scenes cisAvsasicodsesdd«aeocdceviescstostedeedsiesesavstsivenvaessvtveecaccves 122

SYNOPSIS. Re-examination of copepod material, collected from the northern Gulf of Mexico and previously identified as

Zausodes arenicolus C.B. Wilson, 1932 (Harpacticoida, Harpacticidae), resulted in the discovery of three new species of the

Zausodes complex. Phylogenetic analysis identified four distinct lineages within this complex which are attributed generic status.

Zausodes C.B. Wilson, 1932 is redefined to include only Z. septimus Lang and the type species Z. arenicolus which is completely

redescribed. A new genus Mucropedia is proposed to accommodate two new species from the Gulf of Mexico, M. kirstenae and

M. cookorum. Z. biarticulatus It6, 1979 from the Japanese Bonin Islands is transferred to Archizausodes gen. nov. and regarded

as the most primitive member of the Zausodes complex. All other species are grouped in Neozausodes gen. nov., including N.

shulenbergeri sp. nov. from the Gulf of Mexico and N. areolatus (Geddes, 1968a) comb. nov. which is completely redescribed

on the basis of type material. Z. cinctus Krishnaswamy, 1954 is ranked species incertae sedis in the family Harpacticidae. The

sister group relationship between Perissocope Brady, 1910 and the Zausodes complex is discussed. Lang’s (1944, 1948)

subfamilial division of the Harpacticidae is abandoned.

*Author for correspondence

INTRODUCTION

Species of Zausodes C.B. Wilson are typical inhabitants of sandy

substrata in shallow subtidal localities, however, some records

indicate that their horizontal zonation extends into the infralittoral of

sandy beaches (Wilson, 1932; Mielke, 1990, 1997). Although the

genus was originally proposed for the type species Z. arenicolus

from the Woods Hole area (Wilson, 1932), most species that have

been added since are subtropical in distribution. The genus currently

comprises nine species but only two of them, Z. arenicolus and Z.

septimus Lang, 1965, have been recorded again since their original

description (Bell & Woodin, 1984; Coull, 1971a—b; Foy & Thistle,

1991; Mielke, 1990, 1997). The taxonomy and phylogenetic posi-

tion of the genus within the family Harpacticidae are not well

understood for a variety of reasons. First, species of Zausodes are

amongst the smallest Harpacticidae and males often do not exceed

0.4 mm in size. Second, Wilson’s (1932) generic diagnosis contains

a number of significant inconsistencies which originate from his

imperfect description of Z. arenicolus. Lang (1965) clarified some

of the erroneous statements but did not present a complete

redescription. Third, several subsequent descriptions are grossly

inadequate and severely hamper both species identification and

phylogenetic reconstruction of relationships. This 1s particularly the

case for the species described by Jakobi (1954) and Krishnaswamy

(1954). Finally, the current subfamilial classification of the

Harpacticidae introduced by Lang (1948) is inadequate. The genus

Zausodes was placed in the Zausodiinae together with Zaus Goodsir

and Zausopsis Lang, however recent discoveries of new taxa (Ito,

1979; Watkins, 1987) have provided strong indications for a close

relationship between Zausodes and Perissocope Brady, a genus

currently assigned to the Harpacticinae.

While examining a collection of harpacticoids from the northern

Gulf of Mexico, previously identified by D.Thistle and co-workers

as Z. arenicolus (Foy & Thistle, 1991; Ravenel & Thistle, 1981;

Thistle, 1980; Thistle et al., 1995), we found several other species of

Zausodes which could not be assigned to the type species. Although

Z. arenicolus was present among the specimens, as confirmed by

comparison with Wilson’s type material, three species new to sci-

ence were found. Since one of these was very similar to Z. areolatus

Geddes, the type locality of which is in the relatively nearby

Caribbean (Geddes, 1968a), the type material of the latter was

obtained for comparison.

This paper describes the three new species from the Gulf of

Mexico, provides complete redescriptions for both Z. arenicolus and

Z. areolatus and analyses the phylogenetic relationships between

the species. The genus Zausodes is redefined in the light of these

findings.

MATERIALS AND METHODS

Samples were taken by SCUBA divers with a 15.5 cm? corer. The

top 3 cm of each core were preserved in sodium-borate-buffered

formalin. In the laboratory, harpacticoids were concentrated from

each sample with a modified Barnett (1968) extraction technique

combined with a 0.062-mm mesh sieve. After rose bengal staining,

harpacticoids were sorted under a dissecting microscope and mounted

in glycerol on slides.

Specimens were dissected in lactic acid, and the dissected parts

were placed in Hoyer’s mounting medium (Pfannkuche & Thiel,

1988) on H-S mounts (Shirayama et al., 1993) or Cobb slide frames

L. BOUCK, D. THISTLE AND R. HUYS

(Westheide & Purschke, 1988). Drawings were prepared with a

camera lucida ona Zeiss Standard 16 compound microscope equipped

with differential interference contrast. Habitus views were drawn at

800x; other illustrations were drawn at 2000x. Body size was

measured along a line halfway between the dorsal and ventral

margins in lateral view at 256x with the aid of a camera lucida.

Terminology follows Huys & Boxshall (1991). Abbreviations used

in the text and figures are: ae = aesthetasc; P1—P6 = first to sixth

thoracopods; exp(enp)—1(2,3) to denote the proximal (middle, distal)

segment of a ramus.

Phylogenetic relationships between taxa were analyzed using the

phylogenetic computer package PAUP 3.1 prepared by David L.

Swofford of the Laboratory of Molecular Systematics, Smithsonian

Institution (Swofford, 1993; Swofford & Begle, 1993). Since evolu-

tion within the Copepoda is assumed to proceed typically by

oligomerization (Huys & Boxshall, 1991), all characters were set

irreversible using the CAMIN-SOKAL option. This option sup-

presses character reversals at the expense of introducing extra

convergences and thereby increasing the tree-length. The options

employed in the analysis were BRANCH AND BOUND, which

guaranteed to find all most parsimonious trees, and the MINF

optimization, which assigns character states so that the f-value is

minimized.

SYSTEMATICS

For practical reasons the systematics section of this paper is ar-

ranged according to the conclusions arrived at in the phylogeny

section below. Species are allocated to genera following the topol-

ogy of the most parsimonious cladogram obtained by the phylogenetic

analysis (Fig. 33A).

Family Harpacticidae Dana, 1846

Genus Zausodes C.B. Wilson, 1932

In its revised concept (see below) the genus is restricted here to the

type species and Z. septimus. Lang (1965) had already recognized

the close relationship between these species, pointing out their

similarity in the 9P5. Z. arenicolus displays two characters which

are not found in any of the species of the former Zausodes complex:

(1) the 3-segmented P4 endopod, and (2) the presence of a

mucroniform process on enp-2 of the male P2. The former is an

evolutionary labile character, frequently showing intermediate states

in other species (Lang, 1965), whilst the latter is regarded here as a

plesiomorphy retained within the former Zausodes complex only in

Z. arenicolus, but being present in many other harpacticid genera

such as Perissocope, Harpacticus Milne-Edwards and Tigriopus

Norman (Huys et al., 1996). It is assumed that in all other species of

the former Zausodes complex this process was secondarily lost.

DIAGNOsIS. Harpacticidae. Antennule 9 8-segmented, with pin-

nate or plumose setae on segments 1—6; without strong, modified

spines on segments 3-5 or enlarged pectinate or pinnate spines on

segment 6. Antennulec’without modified spines on segment 3.

Antennary exopod 1-segmented, with 2 apical setae. Maxilla with 4

spines/setae on praecoxal endite. P2—-P3 endopods 3-segmented, P4

endopod 2- or 3-segmented. P2 9 enp-3 with 2 inner setae. P3 9 enp-

2 without inner seta. P4 exp-3 with 3 outer spines in both sexes. P4

enp-3 (or enp-2 when 2-segmented) with 1 inner seta in both sexes.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

P2Cenp-2 with or without apophysis, inner seta not modified; enp-

3 with | apical seta (inner one lost), outer spine not fused to segment.

P3c'enp-2 outer distal corner not attenuated.

Swimming leg setal formula:

exopod endopod

2 0.1.223 0.1.221 [9]

0.1.211 [Co]

P3 0.1.323 1.0.221

P4 ONES 23 1.0.121 or 1.121

P5 exopod elongate-oval in both sexes. P5 endopodal

lobe 9 expressed; 3rd and 4th inner setae much shorter than others

(or | seta lost in Z. septimus).

Sexual dimorphism in rostrum, antennule, P2 endopod, P5, P6,

genital segmentation and size.

TYPE SPECIES. Zausodes arenicolus C.B. Wilson, 1932 (by

monotypy).

OTHER SPECIES. Z. septimus Lang, 1965.

Zausodes arenicolus C.B. Wilson, 1932

TYPE LOCALITY. Katama Bay, Martha’s Vineyard, Woods Hole

(Massachusetts); beach sand washings.

MATERIAL EXAMINED.

National Museum of Natural History (Smithsonian Institution),

Washington, D.C.: Woods Hole region; type series consisting of one

vial containing > 50 specimens (USNM 63877); 1 9 and | o’dissected

for examination. According to the USNM catalogue files the

holotypec’has gone missing since at least 1983 when the harpacticoid

collections were inventoried. It is assumed that in reality the holotype

was never segregated by C.B. Wilson although the empty vial,

which supposedly contained the specimen, received a separate

registration number (no. 63423).

The Natural History Museum, London: syntypes (49 2,40'c") in

alcohol; from type locality; coll. C.B. Wilson, 15 August 1927;

BMNH 1948.9.10.37.

Gulf of Mexico: 29°51'N, 84°31'W (about 50 m north of day mark

- #2), St. George Sound, Florida, 5 m depth, unvegetated medium

sand (median grain size = 0.254 mm); a seagrass meadow occurs

about 150 m to the north; see Foy & Thistle (1991) for additional

description. Deposited at the Natural History Museum, London are

992 Qand 3c¢'Cin ethanol (BMNH 1999.176—-187) and 22 Qand

20 Con slides (BMNH 1999.188-191). Deposited at the

Smithsonian, Washington, D.C. are 9 9 9 and2c’cC'in ethanol (USNM

288445446) and 1 9 and 2c’ C'dissected on slides (USNM 288444).

REDESCRIPTION. All illustrations and text are based on specimens

from the Gulf of Mexico. Illustrations were compared to type

material obtained from the Smithsonian in order to verify the species

identification.

FEMALE. Body length: measured from anterior margin of rostrum

to posterior margin of caudal rami: 433 um (x = 0.499, n = 4);

without rostrum and caudal rami: 394 um (x = 0.456, n = 4). Body

(Figs 1A—B, 2C—D) dorsoventrally flattened. Greatest width 200um

(x =0.202, n=4), measured near posterior margin of cephalothorax.

Nauplius eye distinct; reddish brown in fresh, unstained specimens;

invisible in cleared specimens. Integument with surface ornamenta-

tion/sculpturing consisting of irregular pattern of fine striations (not

illustrated). Sensillae present dorsally and dorsolaterally on

cephalothorax and body somites except penultimate one (not all

shown). Ventrolateral margin of cephalic shield with sensillae.

Epimera of thoracic somites thickly chitinized laterally. All somites

but anal with fine spinular rows dorsally and dorsolaterally; penul-

timate somite with ventral spinular row; anal somite with spinular

rows dorsally, ventrally, and laterally on the posterior margin.

Lateral margins of free thoracic somites with 3 sensillae. Ventral

posterolateral corners of urosomites 3—5 and lateral margins of

urosomites 1—4 with spinules. Genital double-somite with continu-

ous chitinous internal rib ventrolaterally and ventrally (but not

dorsally). Anal somite cleft medially; anus located terminally,

triradiate, bordered by incised frill that is partially exposed in dorsal

aspect; with two ventral pores near posterior margin; anal opercu-

lum rounded, smooth; pseudoperculum present, weakly developed.

Caudal rami (Figs 1!A—B, 2C—D) approximately as long as wide,

with 7 setae: setae I-III bare, setae [V—V bipinnate, seta VI bipinnate,

dorsal seta (VII) carried on a biarticulate socle. Gelatinous string

(Figs 1A—B) extending posteriorly from each caudal ramus present

in some specimens.

Rostrum (Fig. 1C) prominent, bell-shaped in dorsal view, with

membranous fringe, defined at base; with two short sensillae

anteriorly and one sensilla on each mediolateral margin; with mid-

dorsal pore.

Antennule (Fig. 2B) 8-segmented; segments 2 and 3 longest; first

segment widest with several spinular rows; fourth segment with an

aesthetasc (50 um long); eighth segment with acrothek consisting of

3 elements (probably 2 setae and | aesthetasc, however, we were

unable to distinguish which elements were setae and which was an

aesthetasc); with armature formula 1-[1], 2-[9 + 1 pinnate], 3—[7 +

2 pinnate], 4-[3 + 1 pinnate + (1 + ae)], 5—[1 + 1 pinnate], 6—[2 + 2

pinnate], 7—[4], 8—-[4 + acrothek].

Antenna (Fig. 2A). Coxa short and unornamented; allobasis with

several spinular rows, abexopodal spinulose seta, and membranous

insert marking original segment boundary between basis and first

endopodal segment; free endopod 1-segmented; lateral armature

consisting of a spine, 1 short seta and 1 long seta; distal armature

comprising | seta, | pinnate, curved spine, and 4 geniculate spines,

longest one of which bearing spinules proximal to geniculation and

fused at base to a slender seta; with spinular rows and hyaline

surface frill as indicated in Fig. 2A; exopod 1-segmented with 2

distal, unequal setae.

Labrum well developed, medially incised.

Mandible (Fig. 3A). Gnathobase with seta at dorsal corner; coxa

with proximal row of spinules; palp biramous, comprising basis and

l-segmented exopod and endopod; basis produced transversely,

with proximal spinular row and 4 bipinnate setae; endopod longer

than exopod, with | bare and 1 pinnate lateral seta and 6 apical setae;

exopod with | pinnate and 2 bare lateral setae, 3 distal setae, and

spinules subdistally and along outer margin.

Maxillule (Fig. 3C). Praecoxa with spinular row along outer edge

and with arthrite bearing 8 spines around distal margin, 2 anterior

surface setae, and posterior spinular row; coxal endite with 4 setae

and a spinular row; basal endite with 6 setae; endopod with 1 bare

and 2 pinnate setae distally; exopod with | bare inner seta, | pinnate

outer seta, 2 distal setae, and a spinular row.

Maxilla (Fig. 3B). Syncoxa with spinular row along outer margin

and 3 endites; praecoxal endite with 2 bare and 2 bipinnate setae;

coxal endites each with 2 bare setae and | pinnate spine; allobasis

with claw and 3 bare setae; endopod 1-segmented with 4 bare setae.

Maxilliped (Fig. 3D). Syncoxa with a bipinnate seta and numer-

ous spinular rows as indicated; basis with a spinular row and seta

along palmar margin, with spinules along outer distal margin and on

anterior face; endopod represented by acutely recurved claw with

spinules along inner margin and proximal accessory seta.

16 L. BOUCK, D. THISTLE AND R. HUYS

Fig. 1 Zausodes arenicolus C.B. Wilson, 1932 (@ ). A, Habitus, lateral view; B, habitus, dorsal view; C, rostrum. Scale bars = 20 Lm.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

thy,

yet 4

ate hy

oO UU eM)

cate panareaet rn TTT CO e ag

a ae! canvas apgn nett OM ret HU ETE ATE Ty vere tttie Vantrin aye

” aint f :

ast ia Lat tec iirenet

Stuer lt ort tat /o Fomvbal ntl Lu

SNe ee wen tn War eeeierier tem iy

peenin, Dt ayy

fete

ar anne pty

einen Bra

we queen! TUNE oe cet mtr

ve ninargltl

vee vw

| a | \

int

a tr nung

one, CT PETIT A, sate cp ttre

VANE gy

Uren cone, Tron cere

TCU veirvene t ;

ton att

Seem TCORET TORSO Ea a Lan

pee eT

ON Epa oem any

Beek

8 Ng

fy iXS

\ we

Fig. 2 Zausodes arenicolus C.B. Wilson, 1932 (¢ ). A, Antenna; B, antennule; C, urosome (excluding PS-bearing somite), dorsal view; D, urosome

(excluding P5-bearing somite), ventral view; Scale bars = 20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

= nee : eS re

Hin ee TR

TERS

icolus C.B. Wilson, 1932 (@ ). A, P2; B, P3. Scale bars = 20 um.

Fig.4 Zausodes aren

L. BOUCK, D. THISTLE AND R. HUYS

SSAA

Geno SSS

PDDARADan —e/

Rodos >~ 3S

gree sae

Fig.5 Zausodes arenicolus C.B. Wilson, 1932 (9). A, P5 exopod, posterior view; B, P4; C, P1 (arrow indicating rudimentary seta); D, P5, anterior view.

Scale bars

20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

PI (Fig. 5C). Rami prehensile; coxa with spinular rows along

inner, outer, and distal margins and on anterior face, with pore at

inner distal corner; basis with bipinnate seta near mid-point of outer

margin and bipinnate spine at inner distal corner; spinular rows

present along inner and outer margins and around articulation with

endopod; with pore near outer proximal corner. Exopod 3-seg-

mented, 1.5 times as long as endopod (excluding apical elements);

exp-! with distal pinnate seta and spinular rows along outer margin;

exp-2 elongate, 2.6 times as long as exp-1, with short, slender inner

seta distally (arrowed) and outer margin spinular row extending to

insertion of subdistal pinnate seta; exp-3 vestigial, largely incorpo-

rated into exp-2, with 2 geniculate spines and 2 claws. Endopod

2-segmented; enp-1 elongate, with outer spinular row; enp-2 0.2

times as long as enp-1, with outer spinular row and bearing genicu-

late spine, claw, and short, slender inrer seta distally.

P2-P4 (Figs 4A-B, 5B) with 3-segmented rami. Coxae with

spinular rows at outer distal corner of P2—P3 and posteriorly near

outer edge of P4. Bases with outer bipinnate spine (P2) or naked seta

(P3—P4), and spinules plus a pore at outer distal corner. Endopods

distinctly shorter than exopods. Spinular rows present on posterior

surface of P2—P4 exp-3, P4 exp-1 and -2, P2—P4 enp-3. Outer distal

spine of P2—P4 exp-3 and P2 enp-3 tripinnate. Pores present as

illustrated (Figs 4A—B, 5B). Seta and spine formula of P2—P4 as in

Table 1.

P5 (Figs SA,D) biramous, not fused medially. Baseoendopod with

numerous anterior surface and marginal spinular rows; endopodal

lobe triangular, with 2 sparsely plumose and 2 short bare setae along

inner margin and | distally pinnate seta apically; outer basal seta

slender and arising from cylindrical process. Exopod 1.9 times as

long as wide (excluding distal spines) with numerous anterior,

posterior and marginal spinular rows, with | inner, 1 apical and 3

outer bipinnate spines, apical one with flagellate tip; posterior

surface with proximal pore near outer margin.

Genital double somite (Figs 2C—D) wider than long. Genital field

located far anteriorly. Copulatory pore large, midventral; leading via

short copulatory duct to single median seminal receptacle. Gonopores

paired, closed off by opercula derived from vestigial sixth legs

bearing 2 naked setae.

MALE. Body length: measured from anterior margin of rostrum to

posterior margin of caudal rami: 366 um (xX = 0.379 um, n = 4);

without rostrum and caudal rami: 294 um (xX = 338 um, n= 4). Body

width 147 um (X= 149 um, n=4). Not all sensillae shown in habitus

views (Figs 6A—B). Sexual dimorphism in body size, rostrum,

antennule, P2 endopod, PS, P6, and urosome segmentation (Figs

7A-B).

Rostrum (Fig. 6A) trapezoid, defined at base.

Antennule (Figs 6C—D) 6-segmented, chirocer; segment 5 bear-

ing aesthetasc, not conspicuously swollen; segments 3 and 5 longest;

with geniculation between segments 5 and 6; first segment with

several spinular rows along anterior margin; with armature formula

1—[1], 2-[1], 3-[9], 4-[10], 5—[6 + (1 + ae)], 6-[6 + acrothek].

P2 (Fig. 7E) as in 9 except for endopod. Enp-1 with outer row of

spinules. Enp-2 with outer distal corner produced into spinous

apophysis, extending to distal margin of enp-3; outer margin

spinulose; inner margin with subdistal bipinnate seta. Enp-3 with

spinulose outer margin, short outer pinnate spine, long bipinnate

spine distally and 2 pinnate inner setae; with spinules on posterior

face and at bases of distal inner and apical elements.

P5 (Figs 7C—D) biramous. Baseoendopods fused medially form-

ing transversely elongate plate; endopodal lobe slightly developed,

with | outer, distally pinnate seta and | inner, bipinnate seta; outer

basal seta slender and arising from cylindrical process; with spinules

around articulation with exopods. Exopod as inQexcept for an

additional small, bipinnate seta along the outer margin, and fewer

spinular rows.

P6 (Fig. 7B) symmetrical; with distal seta and spinules along

outer margin; located more laterally than in.

NOTES.

Wilson (1932) noted sexual dimorphism in the first pair of swim-

ming legs and the exopods of P3—P4 and further claimed that none

of the other rami was genuinely modified in the male. Lang (1965)

re-examined type specimens of Z. arenicolus and concluded that

neither P1 nor P3—P4 displayed sexual dimorphism and that Wilson

had overlooked the modification of the male P2 endopod.

Coull’s (1971b) numerous records from the North Carolina shelf,

Bell & Woodin’s (1984) record from Virginia, Bell’s records from

Tampa Bay (e.g. Bell et al., 1989), and this paper suggest that Z.

arenicolus assumes a continuous distribution along the American

east coast from Massachusetts, around the Florida peninsula, and

into the northern Gulf of Mexico.

Zausodes septimus Lang, 1965

TYPE LOCALITY. California, Monterey Bay, off Hopkins Marine

Station, about 7 m depth.

NOTES.

The few disjunct records of this species suggest a wide distribution

both in the Caribbean and along the Pacific seaboard of the U.S. and

Latin America. Mielke (1990) found Z. septimus along both Pacific

and Caribbean coasts of Panama and subsequently recorded the

species also from Punta Morales in Costa Rica (Mielke, 1997). Coull

(197 1a) identified Z. septimus from sediment samples taken on St.

Thomas (U.S. Virgin Islands).

Mielke’s (1990) specimens from Panama (particularly from the

Caribbean side; Isla Nalunega) are remarkably smaller than those

from the type locality in California but otherwise agree in most

aspects with Lang’s (1965) description. Significant discrepancies

are found in (1) the shape of the rostrum which is squarish and

truncate in the Californian material but elongate bell-shaped and

pointed in Mielke’s material, (2) the proportional lengths of the

antennulary segments in the Q (particularly segments 3-4 are dis-

tinctly shorter in the Panama females), (3) the length of P1 endopod

which is markedly shorter in Lang’s specimens, and (4) the shape

and length of outer and apical spines of P2—P4 exp-3 which are

stouter and shorter in the Panama population. A further study based

on material from a wider range of localities is required to confirm

whether these differences originate from intraspecific variability as

Mielke (1990, 1997) advocates, or reflect the existence of two

closely related species.

Z. septimus can be differentiated from Z. arenicolus by the

segmentation of the P4 endopod and by the shape of the P5

baseoendopod and the relative position of its setae. Males of both

species can be distinguished by their P2 endopod (i.e. enp-2 with

mucroniform process in Z. arenicolus).

Genus Neozausodes gen. nov.

Lang (1965) remarked on the close similarity between Z. sextus and

the three Brazilian species Z. limigenus, Z. stammeri and Z.

paranaguaensis. Geddes (1968a) regarded Z. areolatus as morpho-

logically closest to Z. sextus. As aresult of the phylogenetic analysis

these 5 species together with N. shulenbergeri sp. nov. are grouped

here in a new genus.

82 L. BOUCK, D. THISTLE AND R. HUYS

Fig. 6 Zausodes arenicolus C.B. Wilson, 1932 (o’). A, Habitus, dorsal view; B, habitus, lateral view; C, antennule, fifth and sixth segments, anterior

view; D, antennule, dorsal view. Scale bars = 20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

aoe eee

4) rere re

en a ee

area

Lawes

EI GEE

Sea

Fig. 7 Zausodes arenicolus C.B. Wilson, 1932 (co). A, Urosome, dorsal view; B, urosome, ventral view; C, P5 exopod, posterior view; D, P5, anterior

20 um.

view; E, P2 endopod. Scale bars

DIAGNOSIS. Harpacticidae. Antennule 9 6- or 7-segmented, with-

out pinnate or plumose setae on segments 1—6; with strong, modified

spines on segments 3—5 and enlarged pectinate or pinnate spines on

segment 6. Antennulec' with modified spine on segment 3. Antennary

exopod 1-segmented, with 2 apical setae. Maxilla with 3 spines/

setae on praecoxal endite. P2 endopod 3-segmented (2- incof N.

areolatus), P3 endopod 2- or 3-segmented, P4 endopod 2-seg-

mented. P2 9enp-3 with 1—2 inner setae. P3 9enp-2 without inner

seta. P4 exp-3 with 3 outer spines in both sexes. P4 enp-2 with 1

inner seta in both sexes. P2c’enp-2 without apophysis, inner seta

(proximal one in 2-segmented endopod of N. areolatus) not modi-

fied; enp-3 (-2 in N. areolatus) with 1 apical seta (inner one lost),

outer spine not fused to segment. P3c’enp-2 outer distal corner not

attenuated.

Swimming leg setal formula:

exopod endopod

ip) 0.1.223 0.1.221 or 0.1.121 [@]

0.1.211 [C'sextus]

0.311 [C’areolatus]

0.1.111 [CO C other species]

P3 0.1.323 1.0.221 or 1.221

P4 0.1.323 1.121

P5 exopod round in both sexes. P5 endopodal lobe 9 expressed;

all setae well developed.

Sexual dimorphism in rostrum, antennule, P2 endopod, P5, P6,

genital segmentation and size.

TYPE SPECIES. Zausodes areolatus Geddes, 1968a= Neozausodes

areolatus (Geddes, 1968a) comb. nov.

OTHER SPECIES. Z. limigenus Jakobi, 1954 =N. limigenus (Jakobi,

1954) comb. nov.; Z. paranaguaensis Jakobi, 1954 = N.

paranaguaensis (Jakobi, 1954) comb. noy.; Z. stammeri Jakobi,

1954=N. stammeri (Jakobi, 1954); Z. sextus Lang, 1965 =N. sextus

(Lang, 1965) comb. nov.; N. shulenbergeri sp. nov.

ETYMOLOGY. The generic name is derived from the Greek prefix

neos, Meaning new, and alludes to the advanced position of this

genus within the Zausodes-group. Gender: masculine.

Neozausodes areolatus (Geddes, 1968a) comb. nov.

TYPE LOCALITY. Bahamas, Eleuthera, SW of Glass Window;

25°26'03"N, 76°36'10"W; 5 m depth, sand bottom.

MATERIAL EXAMINED.

American Museum of Natural History: holotype 9 dissected and

mounted on 3 slides (AMNH 12944); paratypes are 1 9 and

1 Mdissected on 3 slides each, and 8 9 9 in alcohol, collected from

type locality (AMNH 12945). Note that the holotype registration

number was inadvertently misprinted in Geddes (1968a) as 12949.

Zoological Museum of the University of Bergen: paratypes (20° C’,

39 2) from Exuma Cays, Great Guana Cay, between White Point

and Black Point, 24°04'25"N, 76°23'45"W; 3-4 m depth, sand

bottom (ZMUB 49315).

REDESCRIPTION. All female illustrations are from the holotype

except Figs 8B—C, which are from paratypes. Male habitus and P5

illustrations are from a Bergen Museum paratype; other male illus-

trations are from an AMNH paratype.

FEMALE. Body length measurements from AMNH paratypes:

measured from anterior margin of rostrum to posterior margin of

caudal rami: X = 606 Um (n = 3); without rostrum and caudal rami:

L. BOUCK, D. THISTLE AND R. HUYS

xX = 561 um (n = 3). Body (Figs 8B—C, 9B-C) dorsoventrally

flattened. Body width: x =314 um (n=3). Integumental surface (e.g.

Al, rostrum, urosome) with areolated ornamentation/sculpturing

(not illustrated). Sensillae present dorsally and dorsolaterally on

urosomites 2— 4 and anal somite. Urosomites 2—5 with fine denticle

rows dorsally and dorsolaterally; antepenultimate and penultimate

somites with ventral spinular rows; anal somite with spinular rows

dorsally, ventrally, and laterally on the posterior margin. Ventral

posterolateral corners of urosomites 4—5 and lateral margins of

urosomites 2—4 with spinules. Anal somite cleft medially; anus

located terminally, triradiate, bordered by incised frill that is par-

tially exposed in dorsal and ventral aspects; with two ventral pores

near posterior margin; anal operculum and reduced pseudoperculum

present. Caudal rami (Figs 8B—C, 9B-—C) wider than long, with 7

setae: setae I-III bare, setae IV—V bipinnate, seta VI bipinnate,

dorsal seta (VI) carried on a biarticulate socle. No gelatinous string

was apparent.

Rostrum (Fig. 9A) prominent, lateral margins roughly parallel,

defined at base; with two short sensillae anteriorly and two sensillae

subdistally; with middorsal pore.

Antennule (Fig. 8A) 6-segmented; segments | and 2 longest; first

segment widest with spinules; fourth segment with an aesthetasc

(50 pm long), a surface indentation running from the anterior mar-

gin towards, but not reaching, the posterior margin, and an

uninterrupted cuticle extending the length of the posterior margin;

with setal formula 1-[1], 2-[10], 3-[8 + 2 unipinnate], 4-[4 + 2

unipinnate + (1 + ae)], 5—[6 + 2 pinnate], 6—[5 + acrothek]. The setal

formula was based on the holotype, but setae missing in the holotype

specimen that were found in the paratypic slides were added to the

formula. Added setae include 1 seta from segment 2, 1 unipinnate

seta from segment 3, and | seta from segment 5. The setation in the

illustration is a composite, showing all setae.

Antenna (Fig. 9D). Coxa short and unornamented; allobasis with

spinular row, abexopodal seta, and membranous insert marking

original segment boundary between basis and first endopod seg-

ment; free endopod 1-segmented; lateral armature consisting of a

pinnate spine and | pinnate, | short bare, and 1 long bare seta; distal

armature comprising | seta, 1 unipinnate, curved spine, and 4

geniculate spines, longest one of which bearing spinules proximal to

geniculation and fused at base to a slender seta; with spinular rows

and hyaline surface frill as indicated in Fig. 9D; exopod 1-seg-

mented with 2 distal, unequal setae and a spinular row. The short,

bare, lateral seta of the endopod was found on the paratype but could

not be discerned on the holotype.

Mandible (Fig. 10A). Gnathobase with pinnate seta at dorsal

corner; coxa with proximal row of spinules; palp biramous, com-

prising basis and 1-segmented exopod and endopod; basis produced

transversely, with proximal spinular row and 3 bipinnate setae (one

of which broken off in the holotype but observed in the paratype);

endopod longer than exopod, with | bare and | pinnate lateral seta

and 6 apical setae; exopod with 3 lateral and 4 distal setae and

subdistal spinules.

Maxillule (Fig. 10C). Praecoxa with spinular row along outer

edge and with arthrite bearing 8 spines around distal margin, 2

anterior surface setae, and posterior spinular row; coxal endite with

5 setae; basal endite with 6 setae; endopod with 3 pinnate setae

distally and a lateral spinular row; exopod with 1 pinnate inner seta,

1 bare and 2 pinnate distal setae.

Maxilla (Figs 1OE-F). Syncoxa with 3 endites; praecoxal endite

with 3 bipinnate setae; coxal endites each with 1 bare seta and 2

pinnate setae; allobasis with claw and 3 bare setae; endopod 1-

segmented with 1 distally pinnate and 3 bare setae.

Maxilliped (Fig. 10D). Syncoxa with a pinnate seta and numerous

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

Fig. 8 Neozausodes areolatus (Geddes, 1968a) comb. noy. (¢). A, Antennule; B, habitus, dorsal view (somewhat distorted); C, habitus, lateral view.

Scale bars = 50 tm.

L. BOUCK, D. THISTLE AND R. HUYS

yvvvyv! yw e

yw wy

vuv ¥

Vy vy V

vv vVVV

WN Vy Www yy WwyVy

Pry

vv vvvv VV ni WW VVVwwyyy vy

Vvv

VV VW vw Vv

WV Vy Www VV WVVAWVAMANY VW WW VY Winn SS ww

yi) vw Wy

Vwvy Te

ral Wvvvww WV WW Wyy Vy WNWYVWYWy YAW

Vy if

NY oy

PRA

TRTLIRTOAR RRL

arent INU === ae

S> /8

NMA iy,

AAA

aanitnith

Soh SAMA aay

AP, WLP Sip,

ZX van

aN gn

ZN 4X

AN Ewe EE

—a

Fig.9 Neozausodes areolatus (Geddes, 1968a) comb. nov. (9). A, Rostrum; B, last 3 urosomites and caudal rami, dorsal view; C, same, ventral view; D,

antenna. Scale bars = 20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

SF 4

S-~

Fig. 10 Neozausodes areolatus (Geddes, 1968a) comb. nov. (2). A, Mandible; B, P1; C, maxillule; D, maxilliped; E, maxilla; F, maxillary endites. Scale

bars = 20 um.

L. BOUCK, D. THISTLE AND R. HUYS

v. (2). A, P2; B, P3; C, P4; D, P5. Scale bars = 20 um.

olatus (Geddes, 1968a) comb. no

sodes are

Fig. 11 Neozau

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

spinular rows as indicated in Fig. 10D; basis with a spinular row and

seta along palmar margin, with spinules along outer distal margin;

endopod represented by acutely recurved claw, spinulose along the

distal inner margin, with proximal accessory seta.

Pl (Fig. 10B) Rami prehensile; coxa with spinular rows along

inner and outer margins; basis with pinnate seta subdistally at outer

margin and spine near articulation with endopod; spinular rows

present along inner and outer margins and on anterior face. Exopod

3-segmented, 1.3 times as long as endopod (excluding apical ele-

ments); exp-! with distal pinnate seta and spinular rows along outer

margin; exp-2 elongate, 2.1 times as long as exp-1, with short,

slender inner seta distally and outer margin spinular row extending

to insertion of subdistal pinnate seta; exp-3 vestigial, largely incor-

porated into exp-2, with 2 geniculate spines and 2 claws. Endopod

2-segmented; enp-1 elongate, with outer spinular row; enp-2 0.3

times as long as enp-1, with outer spinular row and bearing genicu-

late spine, claw, and short, slender inner seta distally.

P2—P4 (Figs 11A—C) with 3-segmented exopods; endopod 3-

segmented in P2 and 2-segmented in P3—P4 with the distal segment

comprised of two fused segments; indentations mark the plane of

fusion. Coxae with spinular rows at outer distal corner and posteriorly

near outer margin of P2. Bases with outer bipinnate spine (P2) or

naked seta (P3—P4), spinules, and a pore (P2—P3) near outer distal

corner. Endopods distinctly shorter than exopods. Spinular rows

present on posterior surface of P2—P4 terminal endopodal segments.

Spinular rows present on posterior surfaces of P4 exp-1, -2, and -3 in

the paratype. Pores present as illustrated (Figs 11A—C). Seta and

spine formula of P2—P4 as in Table 1.

P5 (Fig. 11D) biramous, not fused medially. Baseoendopod with

numerous anterior surface and marginal spinular rows; endopodal

lobe triangular, with 3 bipinnate and 2 pinnate setae; outer basal seta

slender and arising from cylindrical process. Exopod 1.2 times as

long as wide (excluding distal spines) with numerous anterior,

posterior and marginal spinular rows, with | inner, 1 apical and 3

outer bipinnate spines with flagellate tips. A posterior margin row of

spinules on the baseoendopod was left out of the illustration to

increase clarity.

MALE. Body length (from Bergen museum paratypes) measured

from anterior margin of rostrum to posterior margin of caudal rami:

X = 506 um (n = 2); without rostrum and caudal rami: x = 454 um (n

= 2). Body width: x = 264 um (n = 2). Not all sensillae shown in

habitus views (Figs 12A—B). Sexual dimorphism in body size,

rostrum, antennule, P2 endopod, P5, and urosome segmentation

(Figs 12A—B). The P6 could not be observed.

Rostrum (Fig. 12B) oval, twice as wide as long; with two sensillae

anteriorly and one sensilla on each mediolateral margin; with mid-

dorsal pore.

Antennule (Figs 12E—F) 6-segmented, chirocer; segment 5 not

conspicuously swollen; segments 3 and 5 longest; with geniculation

between segments 5 and 6. First segment with several spinular rows

along anterior margin; segment 5 with aesthetasc (55 um long) and

anterior distal corner produced into blunt apophysis; with setal

formula 1-[1], 2-[1], 3-[9], 4-[9], 5—[8 + (1 + ae) + 4 modified], 6—

[6 + acrothek].

P2 (Fig. 12D) as in Q except for endopod. Endopod 2-segmented

with the distal segment derived by fusion of two segments. Enp-1

with outer row of spinules. Enp-2 with pronounced indentations

marking the plane of fusion and continuous cuticle between fused

segments; with spinulose outer margin; inner margin with 3 pinnate

setae; distal margin with short distally pinnate spine and long

bipinnate spine; posterior face with spinules. Pore present as illus-

trated (Fig. 12D).

P5 (Fig. 12C) baseoendopods fused medially forming trans-

versely elongate plate (one half of plate illustrated); each side with

2 setae, slender outer basal seta arising from cylindrical process, and

spinules around articulation with exopod. Exopod as in 9 except for

an additional small, bipinnate seta along the outer margin, and fewer

spinular rows.

NOTES.

The holotype urosome is damaged showing a break between

urosomites 3 and 4. The distal portion of the urosome is reillustrated

here to provide additional information for the anal somite and caudal

rami.

Inspection of the holotype and paratypes revealed that what

Geddes (1968a) illustrated as discrete segments 4 and 5 of the

female antennule is in reality a single segment. This segment has a

surface suture, which Geddes illustrated as a functional articulation

between two segments, running subdistally from the anterior to-

wards the posterior margin. However, the surface suture is incomplete

and does not reach the posterior margin. Also, the continuity of the

cuticle along the posterior margin further supports the interpretation

of a single compound segment rather than two distinct segments.

The male P2 endopod also has a fusion not described by Geddes

(1968a). The two distal segments are fused into a single segment

indicated by a continuous cuticle running through the plane of

fusion. The membranous insert indicating the line of fusion (Fig.

12D) and the outer corner projection on what Geddes illustrated as

the second segment may have been the source of his misinterpreta-

tion of the endopod segmentation.

This redescription has revealed additional setae, not found in

Geddes’ description, on the following appendages in the female:

antennule (segments 2—6), antenna (allobasis and endopod), mandi-

ble (exopod and endopod), maxillule (coxal and basal endites),

maxilla (syncoxal endites and endopod), maxilliped (endopodal

claw), Pl and P4 (basis), and caudal rami. Additional setae were also

found on the male antennule (segments 2-6).

Neozausodes limigenus (Jakobi, 1954) comb. nov.

TYPE LOCALITY. Brazil, Parana State; Baia de Paranagua, Ilha do

Mel, Mar de Dentro.

NOTES.

Jakobi’s (1954) deficient description is very brief and contains

several internal inconsistencies (Lang, 1965). According to the

author the male is unknown but in the description of Z.

paranaguaensis he states that there is no sexual dimorphism in the

swimming legs. He further claims that the armature formula of P2—

P4 is identical in Z. limigenus and Z. stammeri, however, according

to his table on p. 223 the outer spine of P4 enp-2 is missing in the

former. This character, which was not figured by Jakobi, is unique

within the former Zausodes complex and requires confirmation. The

species is placed in Neozausodes on account of the 7-

segmented 9 antennule, the presence of large uniserrate spines on

the penultimate segment of this appendage, and the round P5

exopod.

Neozausodes paranaguaensis (Jakobi, 1954) comb. nov.

TYPELOCALITY. Brazil, Parana State; Baia de Paranagua, Ilha do

Mel, Mar de Dentro.

NOTE.

According to Jakobi (1954) males of this species possess a small

inner seta on P3—P4 exp-1. Since the author did not illustrate but

only tabulated this character, and none of the other species of the

L. BOUCK, D. THISTLE AND R. HUYS

Fig. 12 Neozausodes areolatus (Geddes, 1968a) comb. nov. (’). A, Habitus, lateral view; B, habitus, dorsal view; C, P5; D, P2 endopod; E, antennule,

segment 5, anterior view; F, antennule, dorsal view. Scale bars = 20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

former Zausodes complex displays such kind of sexual dimorphism,

we regard this observation as extremely doubtful. The first exopod

segment of legs 24 often has an inner tuft or row of long setules

which can easily be misinterpreted as a small seta. The species is

placed in Neozausodes on the same grounds as for the previous one.

Neozausodes stammeri (Jakobi, 1954) comb. nov.

TYPELOCALITY. Brazil, Parana State; Baia de Paranagua, Ilha do

Mel, Mar de Dentro.

NOTE.

This is the most completely described of Jakobi’s (1954) species.

There is, however, no doubt that this species requires redescription

before it can be unambiguously identified. Given the limited detail

in the illustrations, the differences between N. limigenus and N.

stammeri are not impressive, raising the suspicion that both are

conspecific.

Neozausodes sextus (Lang, 1965) comb. nov.

TYPE LOCALITY. California, Monterey Bay, off Hopkins Marine

Station; sand at about 7 m depth.

Neozausodes shulenbergeri sp. nov.

SYNONYMY. Zausodes cf. arenicolus sensu Ravenel & Thistle

(1981) [ecology]. Zausodes arenicolus sensu Varon & Thistle (1988)

[ecology].

TYPE LOCALITY. Gulf of Mexico: 29°51'N, 84°31'W (about 50 m

north of day mark #2), St. George Sound, Florida, 5 m depth,

unvegetated medium sand (median grain size = 0.254 mm); a

seagrass meadow occurs about 150 m to the north; see Foy & Thistle

(1991) for additional description.

MATERIAL EXAMINED.

The Natural History Museum: holotypeQin alcohol (BMNH

1999.192); allotypic paratypec'in alcohol (BMNH 1999.193); other

paratypes are | 9 in ethanol (BMNH 1999.194) and2 9 9 and2c’c’on

slides (BMNH 1999.195—198).

National Museum of Natural History (Smithsonian Institution,

Washington, D.C.): additional paratypes represented by 2 9 9 and

1c'in alcohol (USNM 288448449) and 29 2 and 2c'c'on slides

(USNM 288447).

DESCRIPTION. All illustrations are from paratypes except Figs

13C—D which are from the holotype.

FEMALE. Body length: measured from anterior margin of rostrum

to posterior margin of caudal rami: 443 um (x = 451 um, n = 4);

without rostrum and caudal rami: 411 um (x = 419 um, n= 4). Body

(Figs 13C—D, 16A,C) dorsoventrally flattened. Greatest width:

193 um (x = 196 um, n = 4) near posterior margin of cephalosome.

Naupliar eye distinct; reddish brown in fresh, unstained specimens;

invisible in cleared specimens. Integument with surface ornamenta-

tion/sculpturing consisting of irregular pattern of fine striations and

cephalothorax pitted (not illustrated). Sensillae present dorsally and

dorsolaterally on cephalothorax and body somites except penulti-

mate one (not all shown). Ventrolateral margin of cephalic shield

with sensillae. Epimera of thoracic somites thickly chitinized later-

ally. Third thoracic somite and urosomites 1—5 with fine spinular

rows dorsally and dorsolaterally; penultimate and antepenultimate

somites with ventral spinular row (Fig. 16C); anal somite with

spinular rows dorsally, ventrally, and laterally on the posterior

margin (Fig. 16A,C). Lateral margins of free thoracic somites with

2 sensillae. Ventral posterolateral corners of urosomites 2—5 and

lateral margins of urosomites 14 with spinules. Genital double-

somite with continuous chitinous internal rib ventrolaterally and

ventrally (but not dorsally). Anal somite cleft medially; anus located

terminally, triradiate, bordered by incised frill that is partially ex-

posed in dorsal aspect; with ventral pore near posterior margin; anal

operculum and pseudoperculum present. Caudal rami (Figs 13C—D,

16A,C) approximately as long as wide, with 7 setae: setae I-III bare,

setae [V—V bipinnate, seta VI bipinnate, dorsal seta (VII) carried on

a biarticulate socle. Gelatinous string (Figs 16A,C) extending

posteriorly from each caudal ramus present in some specimens.

Rostrum (Fig. 13A) prominent, bell-shaped, defined at base; with

two short sensillae anteriorly and one sensilla on each mediolateral

margin; with middorsal pore.

Antennule (Figs 14A—B) 7-segmented; segments | and 2 longest;

first segment widest with several spinular rows; segment 4 with

aesthetasc (35 um long); segment 7 with acrothek consisting of 3

elements (probably 2 setae and | aesthetasc, however, we were

unable to distinguish which elements were setae and which was an

aesthetasc); with setal formula 1—[1], 2-[10], 3-[7 + 2 unipinnate],

4-[3 + | unipinnate + (1 + ae)], S—[1 + 1 unipinnate], 6—-[6 + 2

pinnate], 7—[5 + acrothek].

Antenna (Fig. 13B). Coxa short and unornamented; allobasis with

spinular row, abexopodal spinulose seta, and cuticular thinning

marking original segmentation of basis and first endopodal segment;

free endopod 1-segmented; lateral armature consisting of a pinnate

spine, | long and | short seta; distal armature comprising | seta, 1

pinnate curved spine, and 4 geniculate spines, longest one of which

bearing spinules proximal to geniculation and fused at base to a

slender seta; with spinular rows and hyaline surface frill as indicated

in Fig. 13B; exopod |-segmented with 1 lateral short seta and | distal

bipinnate seta.

Labrum well developed, not medially incised.

Mandible (Fig. 14E). Gnathobase with pinnate seta at dorsal

corner; coxa with proximal row of spinules; palp biramous, com-

prising basis and 1-segmented exopod and endopod; basis produced

transversely, with proximal spinular row and 4 bipinnate setae;

endopod longer than exopod, with | bare and | pinnate lateral setae

and 6 apical setae; exopod with | pinnate and 2 bare lateral setae, 1

pinnate and 2 bare distal setae, and subdistal spinular row.

Maxillule (Fig. 14D). Praecoxa with spinular row along outer

edge and with arthrite bearing 8 spines around distal margin, 2

anterior surface setae, and posterior spinular row; coxal endite with

4 setae and a spinular row; basal endite with 6 setae; endopod with

1 bare and 2 pinnate setae distally; exopod with | pinnate inner seta,

2 pinnate and 1 bare distal setae.

Maxilla (Fig. 14C). Syncoxa with spinular row along outer mar-

gin and 3 endites; praecoxal endite with 3 pinnate setae; coxal

endites each with 2 bare setae and | pinnate seta; allobasis with claw

and 3 bare setae; endopod 1-segmented with 4 bare setae.

Maxilliped (Fig. 14F). Syncoxa with a bipinnate seta and numer-

ous spinular rows as indicated in Fig. 14F; basis with a spinular row

and seta along palmar margin, with spinules along outer distal

margin and on anterior face; endopod represented by acutely recurved

claw with spinules along inner margin and proximal accessory seta.

P1 (Fig. 15C). Rami prehensile; coxa with spinular rows along

outer margin and anterior face, with pore near inner distal corner;

basis with bipinnate seta subdistally at outer margin and bipinnate

spine at inner distal corner; spinular rows present along inner and

outer margins, anterior face, and around articulation with endopod;

with pore near outer seta. Exopod 3-segmented, 1.2 times as long as

endopod (excluding apical elements); exp-1 with subdistal pinnate

seta and spinular rows along outer margin; exp-2 elongate, 2.1 times

92 L. BOUCK, D. THISTLE AND R. HUYS

Fig. 13 Neozausodes shulenbergeri sp. nov. (¢.). A, Rostrum; B, antenna; C, habitus, dorsal view; D, habitus, lateral view. Scale bars = 20 um.

| Fig. 14 oN

SYSTEMATICS AND PHYLOGENY OF ZAUSODES 23)

eozausodes shulenbergeri sp. nov. (2 ). A, Antennule (disarticulated); B, antennule (armature omitted); C, maxilla; D, maxillule; E, mandible; F,

maxilliped. Scale bars = 10 tm.

L. BOUCK, D. THISTLE AND R. HUYS

v. (9). A, P2:; B, P3; C, P1; D, P5. Scale bars = 20 um.

sodes shulenbergeri sp. no

Fig. 15 Neozau

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

SASS

ee oe

. ys ) =

MSs </ x]

RN Soy aes :

1 a rat >

AA OT ae dP

Sane hese PX Fy tol eC Der

ee ae ceciecer ene Bea

= . bei ae as, ‘5a

si a 4? feces pan

= R We as

’ Aaa LE as

NA A: eV AS ohh Sige

WRF as rie te

. BS Ly

” ‘

’ ' i

h =

LAM AMA

SSS STeS

~-———S

SERN,

—~

CLT LE

Fig. 16 Neozausodes shulenbergeri sp. nov. (2). A, Urosome (excluding P5-bearing somite), dorsal view; B, P4; C, urosome (excluding P5-bearing

somite), ventral view. Scale bars = 20 um.

as long as exp-1, with short, slender inner seta distally and outer

margin spinular rows extending to insertion of subdistal pinnate

seta; exp-3 vestigial, largely incorporated into exp-2, with 2 genicu-

late spines and 2 claws. Endopod 2-segmented; enp-1 elongate, with

outer spinular rows extending to anterior face; enp-2 0.3 times as

long as enp-1, with spinular row and bearing geniculate spine, claw,

and short, slender inner seta distally.

P2-P4 (Figs 15A-B, 16B) with 3-segmented exopods and

endopods 3-segmented in P2 and P3 and 2-segmented in P4 with the

distal segment comprised of two fused segments; indentation at

outer lateral margin marks the plane of fusion. Coxae with spinular

rows at outer distal corner (P2—P4) and posteriorly near outer edge

of P2 and P4. Bases with outer bipinnate spine (P2) or naked seta

(P3—P4), and spinules plus a pore at outer distal corner. Endopods

distinctly shorter than exopods. Spinular rows present on posterior

surface of P3—P4 exp-3, P4 exp-1 and -2, P2—P4 terminal endopodal

segments. Outer distal spine of P2—P4 exp-3 tripinnate. Pores present

as illustrated (Figs 15A—B, 16B). Seta and spine formula of P2—P4

as in Table 1.

P5 (Fig. 15D) biramous, not fused medially. Baseoendopod with

numerous anterior surface and marginal spinular rows; endopodal

lobe triangular, with 5 bipinnate setae, outermost seta with flagellate

tip; outer basal seta slender and arising from cylindrical process.

Exopod 1.1 times as long as wide (excluding distal spines) with

numerous anterior, posterior and marginal spinular rows, with 1

inner, | apical and 3 outer bipinnate spines, apical, inner, and distal

outer ones with flagellate tips; posterior surface with pore.

Genital double somite (Figs 16A,C) wider than long. Genital field

located far anteriorly. Copulatory pore large, midventral; leading via

short copulatory duct to single median seminal receptacle. Gonopores

paired, closed off by opercula derived from vestigial sixth legs

bearing 3 naked setae.

MALE. Body length: measured from anterior margin of rostrum to

posterior margin of caudal rami: 411 um (x =398 um, n=4); without

rostrum and caudal rami: 367 lum (x = 362 um, n= 4). Body width:

189 um (x= 187 um, n=4). Not all sensillae shown in habitus views

(Figs 17A—B). Sexual dimorphism in body size, rostrum (Fig. 17D),

antennule, P2 endopod and exp-3, P3 enp-3 and exp-3, P5, P6, and

urosome segmentation (Figs 18B—C).

Antennule (Fig. 18A) 6-segmented, chirocer ae-bearing segment

not conspicuously swollen; segments 3 and 5 longest; with

geniculation between segments 5 and 6. First segment with several

spinular rows along anterior margin; fifth segment with an aesthetasc

(40 um long), 3 modified elements, and anterior distal corner

produced into blunt apophysis; with armature formula 1—[1], 2-[1],

3-[8 + 1 unipinnate], 4-[9], 5—[9 + (1 + ae) + 3 modified], 6—[5 +

acrothek].

P2 (Fig. 17C) as in 9 except for endopod and exp-3. Enp-1 with 2

outer rows of spinules. Enp-2 with outer distal corner produced into

apophysis, extending one half the length of enp-3; outer margin

spinulose; inner margin with subdistal bipinnate seta. Enp-3 with

spinulose outer margin, short distally pinnate outer spine, long

bipinnate spine distally, and | bipinnate inner seta; with spinules at

base of distal bipinnate spine. Exp-3 without posterior spinules

found in 9. Pores present as illustrated (Fig. 17C).

P3 enp-3 and exp-3 without posterior spinules found in 9.

P5 (Fig. 18D) biramous. Baseoendopods fused medially forming

transversely elongate plate; endopodal lobe slightly developed, with 1

outer, pinnate seta and | inner, bipinnate seta; outer basal seta slender,

arising from cylindrical process; with spinules around articulation

with exopods. Exopod as in 9 except for an additional bipinnate seta

along the outer margin, fewer spinular rows, and more pores.

L. BOUCK, D. THISTLE AND R. HUYS

P6 (Fig. 18C) symmetrical; with distal seta; located more laterally

than in the 9.

ETYMOLOGY. Named for Dr. Eric Shulenberger, an administrator

of scientific research who believed in the importance of taxonomy

enough to fund some.

NOTES.

N. shulenbergeri sp. nov. and the three Brazilian species (Jakobi,

1954) share the presence of only 1 inner seta on P2 enp-3. Species

within this group are closely related and identification is best

achieved by paying particular attention to the P1 endopod and the PS

in both sexes. The sexually dimorphic spinule rows on the posterior

face of P2 exp-3 and P3 exp-3 and enp-3 are unique for this species

but might well have been overlooked in some other congeners.

Genus Mucropedia gen. nov.

DIAGNOSIS. Harpacticidae. Antennule 2 8-segmented, without pin-

nate or plumose setae on segments 1—6; without strong, modified

spines on segments 3—5 or enlarged pectinate or pinnate spines on

segment 6. Antennulec’without modified spines on segment 3.

Antennary exopod 2-segmented, with armature formula [2, 2].

Maxilla with 4 spines/setae on praecoxal endite. P2—P3 endopods 3-

segmented, P4 endopod 2- or 3-segmented. P2 9 enp-3 with 2 inner

setae. P3 Qenp-2 without inner seta. P4 exp-3 with 2 outer spines

in 9 and 3 outer spines inc’. P4 enp-3 (or enp-2 when 2-segmented)

with 2 inner setae in both sexes. P2c’enp-2 without distinct apophy-

sis, inner seta modified into stout spine; enp-3 with 1 apical seta

(inner one lost), outer spine fused to segment. P3c’enp-2 outer distal

corner attenuated.

Swimming leg setal formula:

exopod endopod

P2 0.1.223 0.1.221 [9]

0.1.211 [C7]

P3 0.1.323 1.0.221

P4 ORES 22123 1.0.221 or 1.221

0.1.323 [C’]

P5 exopod elongate-oval in both sexes. P5 endopodal lobe 9 not

developed; distalmost inner seta rudimentary.

Sexual dimorphism in rostrum, antennule, P2 endopod, P3

endopod, P4 exopod, P5, P6, genital segmentation and size.

TYPE SPECIES. Mucropedia cookorum gen. et sp. nov.

OTHER SPECIES. M. kirstenae sp. nov.

ETYMOLOGY. The generic name is derived from the Latin mucro,

meaning sharp point, and pes, meaning foot, and refers to the

apophysis present on P3 enp-2 in the male. Gender: feminine.

Mucropedia cookorum sp. nov.

TYPELOCALITY. Gulf of Mexico: 29°40.63'N, 84°22.80'W, north-

ern Gulf of Mexico, 18 m depth, unvegetated medium sand; see

Thistle et al. (1995) for additional description.

MATERIAL EXAMINED.

The Natural History Museum: holotype Qin alcohol (BMNH

1999.199); allotypic paratypec'in alcohol (BMNH 1999.200); other

paratypes are 29 9 and 1c'in ethanol (BMNH 1999.201—203) and

2? Qand 2c¢'con slides (BMNH 1999.204—207).

oo ae

Vv. (O"). A, Habitus, dorsal view; B, habitus, lateral view; C, P2 endopod; D, rostrum. Scale bars = 10 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

Fig.17 Neozausodes shulenbergeri sp. no

98 L. BOUCK, D. THISTLE AND R. HUYS

DOOD Aa

yous

S19 o9-097 speeeneurt!

\Tlee ep p-p-p-

pan Pp -p-o-

al La)

OM,

5 fuwsy

ert a

Vnrrpyypit

° vovervopree er erty Qortererey pes y yyy pr pp |

S. proe gygorp FP TF POM PPD POL FD oe Dw oO Og

properereEPVPPITPT © Srey yey peppy yy py

1), eos LT “Wt

i it e tnt ime x

; 1

vay Ys

4s \

pa ASS N

Gs aN AN

44 aN N

s KN x

4 aN N

3 RY Ax

A 4X ,

a 4%

; )

L7T

——

Vel

(

AA on

Fig. 18 Neozausodes shulenbergeri sp. nov. (O’). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding PS-

bearing somite), ventral view; D, P5. Scale bars = 20 um.

—

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

National Museum of Natural History (Smithsonian Institution,

Washington, D.C): additional paratypes represented by 3 9 2 and

2¢'Cin alcohol (USNM 288452-453) and 1 Qand Icon slides

(USNM 2888450-451).

DESCRIPTION. All illustrations are from paratypes except 19A—B

which are from the holotype.

FEMALE. Body length: measured from anterior margin of rostrum

to posterior margin of caudal rami: 288 um (X = 283 um, n = 4);

without rostrum and caudal rami: 257 um (xX = 246 um, n= 4). Body

(Figs 19A—B, 20B-C) dorsoventrally flattened. Greatest width:

144 um (x = 158 um, n = 4) near posterior margin of cephalosome.

Sensillae present on cephalothorax, pedigerous somites and first,

third, fourth, and sixth urosomites (not all shown). Ventrolateral

margin of cephalic shield with sensillae. Epimera of thoracic somites

thickly chitinized laterally. Free thoracic somites and urosomites 1—

5 with fine spinular rows dorsally and dorsolaterally; urosomite 5

with ventral spinular row; anal somite with spinular rows ventrally

and laterally on the posterior margin. Lateral margins of first and

second free thoracic somites with 3 sensillae; third free thoracic

somite with 2 sensillae. Ventral posterolateral corners of urosomites

3-5 and lateral margins of urosomites 1-4 with spinules. Genital

double-somite with continuous chitinous internal rib ventrolaterally

and ventrally (but not dorsally). Anal somite cleft medially; anus

located terminally, triradiate, bordered by incised frill that is ex-

posed in dorsal and ventral aspects; with two ventral pores near

posterior margin; anal operculum and pronounced pseudoperculum

present. Caudal rami (Figs 19A—B, 20B-C) slightly wider than long,

with 7 setae: setae I-III bare, setae 1V—V bipinnate, seta VI bipinnate,

dorsal seta (VII) carried on a biarticulate socle. Gelatinous string

extending posteriorly from each caudal ramus present in some

specimens.

Rostrum (Fig. 19C) prominent, lateral margins roughly parallel to

each other, defined at base; with two short sensillae anteriorly and

one sensilla near each mediolateral margin; with middorsal pore.

Antennule (Fig. 20A) 8-segmented; segments | and 2 longest;

first segment widest with spinules; fourth segment with an aesthetasc

(50 um long); apical acrothek probably consisting of 2 setae and |

aesthetasc, however, we were unable to distinguish which elements

were setae and which was an aesthetasc; with setal formula 1—-[1], 2—

{10}, 3-[9], 4-[4 + (1 + ae)], 5—[2], 6—[4], 7-[4], 8-[4 + acrothek].

Antenna (Fig. 21A). Coxa short and unornamented; allobasis

with spinular row, abexopodal seta, and surface suture marking

original segment boundary between basis and first endopod seg-

ment; free endopod 1-segmented; lateral armature consisting of |

long and 3 short setae; distal armature comprising 1 seta, 1 curved

spine, and 4 geniculate spines, one of which bearing spinules

proximal to geniculation and fused at base to a slender seta; with

spinules and hyaline surface frill as indicated in Fig. 21 A; exopod 2-

segmented, exp-1 with | lateral seta and | bipinnate distal seta and

exp-2 with 2 distal setae.

Labrum well developed, not medially incised.

Mandible (Fig. 21B).Gnathobase with pinnate seta at dorsal corner;

coxa with proximal row of spinules; palp biramous, comprising basis

and 1-segmented exopod and endopod; basis produced transversely,

with proximal spinular row and 4 bipinnate setae; endopod with 2

lateral setae and 6 apical setae; exopod with 3 lateral setae, 3 distal

setae, and spinular rows subdistally and along outer margin.

Maxillule (Fig. 21C). Praecoxa with spinular row along outer

edge and with arthrite bearing 8 spines around distal margin, 2

anterior surface setae, and posterior spinular row; coxal endite with

5 setae; basal endite with 6 setae; endopod with 3 distal setae;

exopod with | inner seta and 3 distal setae.

Maxilla (Fig. 21E). Syncoxa with 3 endites; praecoxal endite with

4 setae; coxal endites each with 2 bare setae and | pinnate seta;

allobasis with claw, 1 pinnate and 2 bare setae; endopod 1-seg-

mented with 5 bare setae.

Maxilliped (Fig. 21D). Syncoxa with a bipinnate seta and numer-

ous spinular rows as indicated in Fig. 21D; basis with a row of fine

spinules and seta at distal palmar margin; endopod represented by

acutely recurved claw with a proximal accessory seta.

Pl (Fig. 22C). Rami prehensile; coxa with spinular row along

outer margin and pore at inner distal corner; basis with bipinnate seta

proximal to mid-point of outer margin and spine at inner distal

corner; spinular rows present along inner and outer margins, and

around articulation with endopod; with pore near outer seta. Exopod

3-segmented, 1.1 times as long as endopod (excluding apical ele-

ments); exp-! with subdistal bipinnate seta and spinular rows along

outer margin; exp-2 elongate, 1.9 times as long as exp-1, with

slender inner seta distally and outer margin spinular row extending

to insertion of subdistal pinnate seta; exp-3 vestigial, largely incor-

porated into exp-2, with 2 geniculate spines and 2 claws. Endopod

2-segmented; enp-| elongate with subdistal pore; enp-2 0.3 times as

long as enp-1, bearing geniculate spine, claw, and short, slender

inner seta distally, with distal fan of fine spinules.

P2—P4 (Figs 22A—B, 23C) with 3-segmented exopods and 3- (P2—

P3) or 2-segmented (P4) endopods. Coxae with spinular rows at

outer distal corner of P2 and P4. Bases with outer bipinnate spine

(P2) or bare seta (P3—P4), and spinules plus a pore at outer distal

corner. Endopods distinctly shorter than exopods. Spinular rows

present on posterior surface of P3 enp-3 and P4 exp-2—3 and enp-2.

Pores present as illustrated (Figs 22A—B, 23C). Seta and spine

formula of P2—P4 as in Table 1.

P5 (Figs 23A-B) not fused medially. Baseoendopod with anterior

surface and marginal spinular rows; with | short, bare and 4 long,

bipinnate inner setae; outer basal seta slender and arising from

cylindrical process. Exopod 1.9 times as long as wide (excluding

distal spines) with numerous anterior, posterior, and marginal spinular

rows; with | inner, | apical and 3 outer pinnate spines; posterior

surface with pore.

Genital double-somite (Figs 20B—C) wider than long. Genital

field located far anteriorly. Copulatory pore large, midventral; lead-

ing via short copulatory duct to single median seminal receptacle.

Gonopores paired, closed off by opercula derived from vestigial

sixth legs bearing 3 naked setae.

MALE. Body length: measured from anterior margin of rostrum to

posterior margin of caudal rami: 225 um (x = 235 um, n=4); without

rostrum and caudal rami: 194 um (x = 202 um, n = 4). Body width:

119 um (x = 126 um, n=4). Not all sensillae shown in habitus views

(Figs 24A—B). Sexual dimorphism in body size, rostrum (Fig. 24C),

antennule, P2 endopod, P3 enp-2, P4 exp-3, P5, P6, and urosome

segmentation (Figs 25B-C).

Antennule (Fig. 25A) 6-segmented, chirocer; aesthetasc-bearing

segment not conspicuously swollen; segment 3 longest; with

geniculation between segments 5 and 6. First segment with several

spinular rows along anterior margin; segment 5 with aesthetasc

(30 um long); with armature formula 1—[1], 2-[1], 3-[9], 4-[9], 5—[8

+ (1+ ae)], 6-[4 +acrothek].

P2 (Fig. 22D) as in 9 except for endopod. Enp-1 with outer row of

spinules. Enp-2 with outer distal corner extending to approximately

one third the length of enp-3; outer margin spinulose; inner margin

with subdistal stout pinnate seta. Enp-3 with spinulose outer margin,

distal spinous apophysis, and 3 inner setae.

P3 (Fig. 22E) enp-2 with outer distal corner produced into apo-

physis.

100 L. BOUCK, D. THISTLE AND R. HUYS

Fig. 19 Mucropedia cookorum sp. nov. (). A, habitus, dorsal view; B, habitus, lateral view; C, rostrum. Scale bars = 20 um.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES 101

Fig. 20 | Mucropedia cookorum sp. noy. (@). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing

somite), ventral view. Scale bars = 20 um.

102 L. BOUCK, D. THISTLE AND R. HUYS

ae = Bs ——

<<< ———s

a cia — ee

nn NO ee

ae = eet ERK S SSS SS

aa)

WML MOL KhALZA

: ee VE:

wo 2 = P

* wits

= ae —

106 L. BOUCK, D. THISTLE AND R. HUYS

vA Waa © VV VV OW Wwwywyvv vy SW

VvV

VVVYVVVYYVV VV VYNVVVYV VV] y y VV VVVWyy

vvVV pYVV —~

Ry VVIV. NYE YIN (a) VV V VV vv

Vv OVV VY YY YY VY Viv VV VV VYVoy

Vv Vy

VV VV VYNYYY © WY VVVvvwvy

(fo)

VV Vy VYYV Vy

owvvvv | MING y YW

vvvvv

vvv VV eas

Vv vvVwN fo) Vv Vw yy

VvvVVYYV¥ YY VN WW yy

Fig. 25 Mucropedia cookorum sp. nov. (c’). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing

somite), ventral view. Scale bars = 20 tm.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

P4 (Fig. 23F) exp-3 with 3 outer bipinnate spines.

P5 (Figs 25D-E) baseoendopods fused medially forming trans-

versely elongate plate; each side with 2 bipinnate setae, slender

outer basal seta arising from cylindrical process, and spinules

around articulation with exopod. Exopod 1.2 times as long as wide

(excluding setae), with an additional pinnate seta along the outer

margin not found in, and with fewer spinular rows.

P6 (Fig. 25C) symmetrical; with distal seta; located more laterally

than in.

ETYMOLOGY. Named in memory of Roy Cook and in honour of

Jessie Cook, the first author’s grandparents.

Mucropedia kirstenae sp. nov.

TYPELOCALITY. Gulf of Mexico: 29°40.63'N, 84°22.80'W, north-

ern Gulf of Mexico, 18 m depth, unvegetated medium sand; see

Thistle et al. (1995) for additional description.

MATERIAL EXAMINED.

The Natural History Museum: holotype Qin alcohol (BMNH

1999.208); allotypic paratypec’in alcohol (BMNH 1999.209); other

paratypes are 1 Qand Ic'in ethanol (BMNH 1999.210-211) and

2? Gand 2c’c’on slides (BMNH 1999.212-215).

National Museum of Natural History (Smithsonian Institution,

Washington, D.C.): additional paratypes represented by 29 9 and

2¢0'Cin alcohol (USNM 288456-457) and | Qand Icon slides

(USNM 288454-455).

DESCRIPTION. All illustrations are from paratypes except Figs

26A-B, which are from the holotype.

FEMALE. Body length: measured from anterior margin of rostrum

to posterior margin of caudal rami: 340 um (x = 320 um, n = 4);

without rostrum and caudal rami: 295 um (x = 276 um, n= 4). Body

(Figs 26A—B, 27B-C) dorsoventrally flattened. Greatest width:

153 um (x = 156 um, n = 4) near posterior margin of cephalosome.

Sensillae present on cephalothorax, pedigerous somites, and third,

fourth, and sixth urosomites (not all shown). Ventrolateral margin of

cephalic shield with sensillae. Epimera of pedigerous somites thickly

chitinized laterally. Free thoracic somites and urosomites 1—S with

fine spinular rows dorsally and dorsolaterally; penultimate somite

with ventral spinular row; anal somite with spinular rows ventrally

and laterally on the posterior margin. Lateral margins of first and

second pedigerous somites with 3 sensillae; third one with 2 sensillae.

Ventral posterolateral corners of urosomites 3—S and lateral margins

of urosomites 1—4 with spinules. Genital double-somite with con-

tinuous chitinous internal rib ventrolaterally and ventrally (but not

dorsally). Anal somite cleft medially; anus located terminally,

triradiate, bordered by incised frill that is exposed in dorsal and

ventral aspects; with two ventral pores near posterior margin; anal

operculum and pronounced pseudoperculum present. Caudal rami

(Figs 26A-B, 27B-C) approximately wider than long, with 7 setae:

setae I-III bare, setae IV—V bipinnate, seta VI bipinnate, dorsal seta

(VII) carried on a biarticulate socle. Gelatinous string extending

posteriorly from each caudal ramus not observed in specimens.

Rostrum (Fig. 26C) prominent, lateral margins roughly parallel to

each other, defined at base; with two short sensillae anteriorly and

one sensilla near each mediolateral margin; with middorsal pore.

Antennule (Fig. 27A) 8-segmented; segments 1 and 2 longest;

first segment widest with spinules; segment 4 with aesthetasc (60

um long); setal formula: 1-[1], 2-[10], 3-[9], 4-[4 + (1 + ae)], 5—[2],

6—[4], 7-[4], 8-[5 + acrothek]; apical acrothek consisting of 2 setae

and 1 aesthetasc.

Antenna (Fig. 28A). Coxa short and unornamented; allobasis

107

with spinular row, abexopodal seta, and incomplete surface suture

marking original segment boundary between basis and first endopod

segment; free endopod 1-segmented; lateral armature consisting of

1 long and 3 short setae; distal armature comprising | seta, | spine,

and 4 geniculate spines, one of which bearing spinules proximal to

geniculation and fused at base to a slender seta; with hyaline surface

frill as indicated in Fig. 28A; exopod 2-segmented, exp-1 with 1

lateral seta and | bipinnate distal seta and exp-2 with 2 distal setae.

Labrum well developed, not medially incised.

Mandible (Fig. 28B). Gnathobase with pinnate seta at dorsal corner;

coxa with proximal row of spinules; palp biramous, comprising basis

and 1-segmented exopod and endopod; basis produced transversely,

with proximal spinular row and 4 bipinnate setae; endopod with 2

lateral setae and 6 apical setae; exopod with 3 lateral setae, 3 distal

setae, and spinular rows subdistally and along outer margin.

Maxillule (Fig. 28C). Praecoxa with spinular row along outer

edge and with arthrite bearing 8 spines around distal margin, 2

anterior surface setae, and posterior spinular row; coxal endite with

5 setae; basal endite with 6 setae; endopod with 3 distal setae;

exopod with | inner seta and 3 distal setae.

Maxilla (Fig. 28E). Syncoxa with 3 endites; praecoxal endite with

1 pinnate and 3 bare setae; proximal coxal endite with | bare seta and

2 pinnate setae; distal coxal endite with 2 bare setae and 1 pinnate

seta; allobasis with claw, | pinnate and 2 bare setae; endopod 1-

segmented with 5 bare setae.

Maxilliped (Fig. 28D). Syncoxa with a bipinnate seta and numer-

ous spinular rows as indicated in Fig. 28D; basis with a row of fine

spinules and seta along palmar margin; endopod represented by

acutely recurved claw with a proximal accessory seta.

P| (Fig. 29E). Rami prehensile; coxa with spinular row along

outer margin and pore at inner distal corner; basis with bipinnate seta

near mid-point of outer margin and spine at inner distal corner;

spinular rows present along inner and outer margins, and around

articulation with endopod; with pore near outer seta. Exopod 3-

segmented, 0.9 times as long as endopod (excluding apical elements);

exp-1 with subdistal bipinnate seta and spinular rows along outer

margin; exp-2 elongate, 2.3 times as long as exp-1, with slender

inner seta distally and outer margin spinular row extending to

insertion of subdistal pinnate seta; exp-3 vestigial, largely incorpo-

rated into exp-2, with 2 geniculate spines and 2 claws. Endopod

2-segmented; enp-1 elongate with subdistal pore; enp-2 0.3 times as

long as enp-1, bearing geniculate spine, claw, and short, slender

inner seta distally, with distal fan of fine spinules.

P2—P4 (Figs 29B-C, 30A) with 3-segmented rami. Coxae with

spinular rows at outer distal corner of P2 and P4 and pore at inner

distal corner of P3 and P4. Bases with outer bipinnate spine (P2) or

bare seta (P3—P4), and spinules plus a pore at outer distal corner.

Endopods distinctly shorter than exopods. Spinular rows present on

posterior surface of P2 enp-3, P3 enp-3 and P4 exp-2-3 and enp-3.

Pores present as illustrated (Figs 29B—-C, 30A). Seta and spine

formula of P2—P4 as in Table 1.

P5 (Figs 30B-C) not fused medially. Baseoendopod with anterior

surface and marginal spinular rows; with 4 long, bipinnate and 1

short, bare inner setae; outer basal seta slender and arising from

cylindrical process. Exopod 1.9 times as long as wide (excluding

distal spines) with numerous anterior, posterior and marginal spinular

rows, with | inner, 1 apical and 3 outer pinnate spines; posterior

surface with pore.

Genital double somite (Figs 27B—C) wider than long. Genital

field located far anteriorly. Copulatory pore large, midventral; lead-

ing via short copulatory duct to single median seminal receptacle.

Gonopores paired, closed off by opercula derived from vestigial

sixth legs bearing 3 naked setae.

L. BOUCK, D. THISTLE AND R. HUYS |

108

Ley HAL

7S oe ‘

rhs . Re #

ne ’ . 4

1 . ae

5 .

_ .

x MS

i . P

in iat =

“ae

v. (Q). A, Habitus, lateral view; B, habitus, dorsal view; C, rostrum. Scale bars = 20 um.

sp. no

Mucropedia kirstenae

Fig. 26

SYSTEMATICS AND PHYLOGENY OF ZAUSODES 109

Fig. 27 Mucropedia kirstenae sp. nov. (?). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing

somite), ventral view. Scale bars = 20 tum.

jie

2) ae es

SF EZ

< Se <<>>

wae [Le

il Meee 3

—S

RS O ce

IWS:

L. BOUCK, D. THISTLE AND R. HUYS

ily

view; D,o’P4 exopod, third segment; E,o’P5 exopod,

view; C, 9 P5, anterior

v. A, 2 P4; B, 9 P5 exopod, posterior

i=)

ira)

aS)

<= 2

fe A

Vv 'E

SS A

~ oO

3 oat

Nie

S 3

S 8

ie}

‘e

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

MALE. Body length: measured from anterior margin of rostrum to

posterior margin of caudal rami: 253 um (xX = 249 um, n=4); without

rostrum and caudal rami: 220 um (xX = 217 um, n= 4). Body width:

131 um (x= 134 um, n= 4). Not all sensillae shown in habitus views

(Figs 31A—B). Sexual dimorphism in body size, rostrum (Fig. 31C),

antennule, P2 endopod, P3 endopod, P4 exp-3, P5, P6, and urosome

segmentation (Figs 32B-C).

Antennule (Fig. 32A) 6-segmented, chirocer; aesthetasc-bearing

segment not conspicuously swollen; segment 3 longest; with

geniculation between segments 5 and 6. First segment with several

spinular rows along anterior margin; segment 5 with aesthetasc

(50 um long); with armature formula 1—[1], 2-[1], 3-[9], 4-[9], 5—

[8 + (1 + ae)], 6-[7].

P2 (Fig. 29A) as in 9 except for endopod. Enp-1 with outer row of

spinules and anterior pore. Enp-2 with outer distal corner extending

approximately one third the length of enp-3; outer margin spinulose;

inner margin with subdistal thick pinnate seta. Enp-3 with spinulose

outer margin, distal spinous apophysis, and 3 inner setae.

P3 (Fig. 29D) enp-2 with outer distal corner produced into

apophysis; enp-3 without pore and posterior spinules found in 9 .

P4 (Fig. 30D) exp-3 with 3 outer bipinnate spines.

P5 (Figs 30E-F) baseoendopods fused medially forming trans-

versely elongate plate; each side with 2 bipinnate setae, slender

outer basal seta arising from cylindrical process, and spinules

around articulation with exopod. Exopod 1.1 times as long as wide

(excluding setae), with an additional pinnate seta along the outer

margin not found in 2, and with fewer spinular rows.

P6 (Fig. 32C) symmetrical; with distal seta; located more laterally

than in.

ETYMOLOGY. Named for Kirsten Lambshead.

NOTES.

M. kirstenae can be readily distinguished from M. cookorum by the

segmentation of the P4 endopod (3-segmented in M. kirstenae, 2-

segmented in M. cookorum). Both species are extremely close

otherwise and additional differences should be sought at the level of

setal lengths and segmental proportions. It is the consistent nature of

these differences rather than their magnitude that convinced us of

the distinctiveness and co-occurrence of two species. The existence

of sibling species is a well known phenomenon in the family

Harpacticidae and makes accurate identification onerous. Soyer et

al. (1987) demonstrated the presence of sibling species of the genus

Tigriopus on the Kerguelen and Crozet Islands. Huys et al. (1996)

recently pointed out that Harpacticus obscurus T. Scott, H.

giesbrechti Klie and H. littoralis Sars are extremely difficult to

separate and identification is often based on setal lengths and

ornamentation, pore patterns and position of spinule rows.

Genus Archizausodes gen. nov.

DIAGNOSIS. Harpacticidae. Antennule 9 8-segmented, without pin-

nate or plumose setae on segments 1-6; without strong, modified

spines on segments 3-5 or enlarged pectinate or pinnate spines on

segment 6. Antennulec’without modified spines on segment 3.

Antennary exopod 2-segmented, with armature formula [2, 2].

Maxilla with 4 spines/setae on praecoxal endite. P2—P3 endopods 3-

segmented, P4 endopod 2-segmented. P2 9 enp-3 with 2 inner setae.

P3 Qenp-2 with inner seta. P4 exp-3 with 3 outer spines in both

sexes. P4 enp-2 with 2 inner setae in both sexes. P2’enp-2 without

distinct apophysis, inner seta not modified; enp-3 with 1 apical seta

(inner one lost), outer spine fused to segment. P3 c’enp-2 outer distal

corner not attenuated.

113

Swimming leg setal formula:

exopod endopod

en 0.1.223 0.1.221 [9]

0.1.211 [o]

P3 0.1.323 Itel7721

P4 0.1.323 1.221

P5 exopod elongate-oval in both sexes. P5 endopodal lobe 2 not

developed; distal 3 inner setae rudimentary.

Sexual dimorphism in rostrum, antennule, P2 endopod, P5, P6,

genital segmentation and size.

TYPE SPECIES. Zausodes biarticulatus It6, 1979 = Archizausodes

biarticulatus (It6, 1979) comb. nov.

OTHER SPECIES. None.

ETYMOLOGY. The generic name is derived from the Greek prefix

archi-, meaning first, and alludes to the primitive position of the

genus. Gender: masculine.

Archizausodes biarticulatus (1t6, 1979) comb. nov.

TYPELOCALITY. Chichi-jima Island, Bonin Islands; shallow water

off Miyanohama; coarse sand with broken shells and corals.

NOTES.

Additional autapomorphies for this genus include the elongate

proximal exopod segment of P1, the transversely prolonged basis of

P4, and the reduction of particular setae on the exopod and

baseoendopod of 9 PS. A. biarticulatus shows some similarities with

Z. cinctus (see below).

PHYLOGENY

Selection of outgroup

Lang (1944, 1948) divided the Harpacticidae in two subfamilies,

Harpacticellinae and Zausodiinae, the names of which were later

corrected by Vervoort (1964) as Harpacticinae and Zausodinae,

respectively. The Zausodinae was proposed to accommodate Zaus,

Zausodes and Zausopsis, all of which have a strongly dorso-

ventrally depressed, more or less shield-shaped body with

completely developed pleurotergites on the pedigerous somites.

The Harpacticinae included Harpacticus, Tigriopus, Harpactic-

ella and Perissocope which according to Lang (1944, 1948) have

a body which is ‘normal, elongate and not shield-shaped’. Two

more genera, Discoharpacticus Noodt and Paratigriopus It6

have been added to the latter subfamily since (Noodt, 1954; It6,

1969).

Lang (1948: 355) remarked that Zausodes showed a certain

resemblance with Perissocope in the reduced swimming leg arma-

ture but nevertheless assigned more weight to the body form,

favouring a relationship with Zaus and Zausopsis. Since Zausodes

has a short Pl exp-1, a well developed maxilliped and 2 setae on

theco’P5 baseoendopod he was of the opinion that the genus had

diverged early in the evolution of the Zausodinae. On the other hand

he expressed some doubts as to the relationships of Perissocope

since males were as yet unknown.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

RENN Oo ‘Vv,

seek Way,

UNV vues oy® is

VV vv vv vy

vv vyvy Y vv vey wey 13)

wee eee vv

apt See ae oe

Siete

VV YY YY

eee woaues yay fo)

vv Ye

Vey

Vee

Fig. 32 Mucropedia kirstenae sp. nov. (C’). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view;

somite), ventral view. Scale bars = 20 tum.

unt *

3g) Basa

carat

C, urosome (excluding P5-bearing

115

116

A first indication of the artificiality of Lang’s subdivision was

given by It6 (1979) who noted the similarity between the shape of

the Pl exopod of Z. biarticulatus and that of the genus Perissocope.

It6 did not assign his species to Perissocope because it lacked the

proximally-born inner seta on P1 enp-1 distinctive of this genus.

Watkins (1987) remarked that Zausodes and Perissocope are more

closely related morphologically, ecologically and zoogeographically

than either is to any other genus of the Harpacticidae. He suggested

that the similar body shape between Zausodes and the other

Zausodinae was a product of convergent evolution, particularly as

the various body somites contribute differently to the overall tear-

drop shape, and similar convergences are found in Harpacticus

compressus Frost, Discoharpacticus mirabilis Noodt and

Perissocope biarticulatus Watkins.

Preliminary phylogenetic analysis (Huys, unpubl.) supports a

robust sistergroup relationship between Perissocope and Zausodes

sensu lato on the basis of the following synapomorphies:

1. strong sexual dimorphism in the shape of the rostrum;

2. antennule 2 with fused segments 7 and 8 (representing ancestral

segments XXIV and XXV) forming compound double segment

(see below: character 1);

3. armature of Pl exp-3 consisting of 2—3 simple (unhinged) and 2

geniculate (hinged) claws (see below: character 8); confirmed by

re-examination of the type material of P. adiastaltus Wells (BNHM

1967.7.11.5-6);

4. sexual dimorphism of P2 involving the loss of the inner distal

seta of enp-3 in the male; this seta is generally reduced in length

in other harpacticid genera such as Harpacticus, Tigriopus and

Paratigriopus but is completely absent in Zausodes sensu lato

and Perissocope.

With the recent description of P. biarticulatus by Watkins (1987)

the absence of the inner seta on P2—P4 exp-1 can no longer be

regarded as a synapomorphy linking Perissocope and Zausodes.

The adhesive mucus strings produced by the caudal rami and the

associated glands were first described for Z. sextus and Z. septimus

by Lang (1965) and subsequently also reported for species of

Perissocope by Watkins (1987). This character is not unique to these

two genera since a similar mucus apparatus has also been recorded

in other representatives of the Harpacticidae (Watkins, 1987) and

even outside this family (Huys, 1990).

Although the Zaus-Zausopsis clade is undoubtedly monophyletic,

recognizing it as a distinct subfamily Zausodinae would relegate the

Harpacticinae to a taxon of paraphyletic status. We recommend

therefore to abandon Lang’s (1944, 1948) subfamilial classification

until a comprehensive phylogenetic analysis of the family is com-

pleted.

Morphological characters

(1) Segmentation 9 antennule

The female antennule is primitively 9-segmented in the Harpacticidae

with segments 7 and 8 representing ancestral segments XXIV and

XXV, respectively. The homology of these segments is established

by their posterior setae (Huys & Boxshall, 1991). This ancestral

condition is found in the genera Harpacticus, Zaus, Discoharp-

acticus, Tigriopus and Paratigriopus. Within the former Zausodes

complex the number of antennulary segments ranges between 6 and

8. The 8-segmented state is derived by fusion of segments 7 and 8,

forming a double segment in Z. arenicolus, Z. septimus, A.

biarticulatus and the two species of Mucropedia. The origin of this

compound segment is unequivocally established by the presence of

L. BOUCK, D. THISTLE AND R. HUYS

2 posterior setae. Comparison of ontogenetic studies of harpacticid

genera possessing 9-segmented antennules such as Tigriopus (It6,

1970) and Harpacticus (It6, 1971, 1976; It6 & Fukuchi, 1978)

indicates that the double segment is not the result of a failure in the

separation of segments 7 and 8 at an earlier stage in ontogeny since

both these segments are already expressed at copepodid I. The

double segment is also found in all other Zausodes species (Table 1)

in which the antennule is only 7- or 6-segmented. It is regarded here

as a synapomorphy linking Perissocope and the Zausodes complex.

A further derived state is found in the 3 Brazilian species (Jakobi,

1954), N. sextus, N. schulenbergeri and N. areolatus in which a

triple segment is formed by incorporation of segment 6 into the

double segment, producing a 7-segmented (or 6-segmented in N.

areolatus) antennule. This condition has independently evolved in

the genus Perissocope (Wells, 1968). Our study has revealed a 6-

segmented antennule in N. areolatus which represents an

autapomorphy for this species. It has originated through fusion of

segment 5 to the aesthetasc-bearing segment 4.

(2) Proximal elements 2 antennule

The armature elements on the 9 antennule are typically setiform in

the great majority of the genera in the Harpacticidae. In some

species of Zausodes sensu lato particular elements on the proximal

segments are modified into stout, rigid spines which typically bear a

subapical flagellum (Figs 8A; 14A). The position and number of

these spines is identical in all species for which they have been

recorded, i.e. two on segment 3 and one on segments 4 and 5 each.

Two spines are found on segment 4 in N. areolatus as a result of

secondary segmental fusion.

(3) Distal elements 9 antennule

Some species of Zausodes sensu lato possess two large, conspicuous

spines on segment 6 (or the homologous portion of segment 5 in the

6-segmented antennule of N. areolatus). These spines are typically

unilaterally pinnate or pectinate (Figs 8A; 14A) and easy to discern

without dissection. They are not found on the male antennules.

(4) Setal ornamentation @ antennule

Species of Perissocope and Zausodes sensu lato typically have

antennulary setae which lack any form of ornamentation. Outgroup

comparison with other harpacticid genera such as Zaus (It6, 1980)

and Harpacticus (e.g. It6, 1976) suggests that this is the ancestral

condition. In the type species Z. arenicolus (Fig. 2B) and Z. septimus

(Lang, 1965; Mielke, 1990) the four proximal segments of

the 9 antennule bear pinnate setae, the plumosity being much more

expressed in the latter. This modification is regarded here as

apomorphic.

(5) Segmentation antennary exopod

Within the Harpacticidae the antennary exopod is 3-segmented only

in Tigriopus and some species of Perissocope. Comparison of

setation patterns indicates that the 2-segmented condition is derived

by fusion of the middle and distal exopod segments. This segmenta-

tion is found in most harpacticid genera such as Harpacticus, Zaus,

Zausopsis and Harpacticella, and in three species of the former

Zausodes complex (biarticulatus, kirstenae, cookorum). All other

Zausodes species show the further derived 1-segmented state (Table

1), being the most reduced condition within the family.

(6) Armature antennary exopod

The maximum setation is found in Harpacticus, Zaus and Zausopsis

which possess 2 lateral setae on exp-1 and 2 lateral plus 2 apical

SYSTEMATICS AND PHYLOGENY OF ZAUSODES 117

Table 1 Segmentation of 2 antennule (A1) and antennary exopod (A2), armature formula of antennary exopod and swimming legs P2—P4 in Perissocope

(2 species) and 12 species of the Zausodes complex. The swimming leg armature formulae of Z. cinctus Krishnaswamy and P. adiastaltus Wells have

been corrected (see text).

Segmentation Armature

Al A2 A2 P2 P3 P4

arenicolus 8 1 2 0.1.223 0.1.221 01-323 1.0.221 0.1.323 1.0.121

areolatus 6 1 2 0.1.223 0.1.221 0.1.323 1.221 0.1.323 1.121

biarticulatus 8 z (2+2) O5223 0.1.221 0.1.323 1.1.221 0.1.323 1.221

cinctus 7 1 2 0.1.223 0.1.221 0.1.323 1.1.221 Osie323 eit

cookorum Bey «8 2 (2+2) 0.1.223 0.1.221 0.1.323 1.0.221 0.1.322 1.221

[Co] 0.1.323

kirstenae Le] 4:8 2 (2+2) 0.1.223 0.1.221 0.1.323 1.0.221 0.1.322 1.0.221

[Co] 0323

limigenus 7 ] 2 0.1.223 0.1.121 Onr323 1.0.221 0.1.323 17

paranaguaensis 7 l 2 0.1.223 0.1.120 OM323 1.0.221 0.1.323 1.121

septimus 8 p} 0.1.223 0.1.221 0.1.323 1.0.221 0.1.323 1.121

Sextus 7 ] 2 0.1.223 0.1.221 0.1.323 1.0.221 0.1.323 1.121

shulenbergeri 7 1 2 0.1.223 0.1.121 0.1.323 1.0.221 0.1.323 st

stammeri 7 1 2 0.1.223 0.1.121 0.1.323 1.0.221 Os1ES23 1.121

Perissocope

adiastaltus 7 3 (24+0+3) 0.1.223* 0.1.221 0.1.323 1.1.321 0.1.323 20

biarticulatus 8 3 (1+0+3) 1223 0.1.221 325 ES 2 iE 322 L221

* Wells (1968) figured P2 exp-3 with formula 323; this is clearly based on an aberrant specimen since no extant harpacticoid has more than 7 elements on

this segment (Huys & Boxshall, 1991; also confirmed by re-examination of other type material).

setae on exp-2. Comparison with the 3-segmented exopod in

Tigriopus suggests that the proximal lateral seta on exp-2 in these

genera originates from the incorporated middle segment and there-

fore the ancestral setal formula must have been [2,1,3]. In Perissocope

the lateral seta on exp-2 is lost resulting in a [2,0,3] formula in P.

adiastaltus Wells or [1,0,3] in P. biarticulatus Watkins. Further setal

reduction has occurred in the Zausodes complex where only 2 setae

are retained on the distal segment in the most primitive species

(biarticulatus, kirstenae, cookorum), or secondarily, the exopod

became an unsegmented bisetose ramus (all other species).

(7) Armature praecoxal endite maxilla

Some species of Perissocope have 5 elements on the praecoxal

endite of the maxilla (Huys ef al., 1996; Fig. 106F) which is the

highest number recorded in any member of the Harpacticidae. This

number is reduced to four (state 1) or three setae (state 2) in the

Zausodes complex. It6 (1979) recorded variability in the maxilla of

Z. biarticulatus and regarded the 3-setae condition as the typical

one. The ‘atypical’ maxilla illustrated in his Fig. 3-1 shows 4

elements arranged in the same pattern as found in Z. arenicolus (Fig.

3B) and Z. septimus (Mielke, 1990: Abb. 3A). On the basis of this

similarity we have scored state 1 for Z. biarticulatus. Lang (1965)

showed only 2 setae on this endite but we suspect that the third one

was overlooked and have given this species a score 2 accordingly

(Table 3).

(8) Armature P1 exp-3

The distal exopod segment of P1 is small or vestigial in the

Harpacticidae and typically embedded in the distal margin of the

middle elongate segment. Huys et al. (1996) described the basic

armature of this segment as four unhinged claws, 1 hinged claw and

a seta, but careful re-examination of a range of genera revealed that

the seta in reality belongs to the middle exopod segment. This seta is

often small (e.g. Fig. 5C) and sited at the distal inner corner of enp-

2. Huys et al.’s misconception stems from observations of

Harpacticus and Zaus in which the distal segment is largely incorpo-

rated in the middle one. In other genera such as Harpacticella and

Tigriopus the distal segment is well delimited showing the real

origin of the inner seta (It6, 1970, 1977; It6 & Kikuchi, 1977). Both

Perissocope and the Zausodes complex deviate from the normal

armature pattern by the presence of two hinged (geniculate) claws

(see above). The modification of one of the simple claws into a

second geniculate one is a synapomorphy for these taxa. Species of

the Zausodes complex have lost one of the simple claws, retaining

only four elements on exp-3 (2 geniculate and 2 simple claws).

(9) Armature P1 enp-1

Harpacticidae typically possess a well developed inner seta on the

proximal endopod segment of P1. The exceptions to this rule are the

species belonging to the Zausodes complex which have secondarily

lost this seta.

(10) Armature P2 enp-3

Most Harpacticidae have 2 inner setae on the distal endopod seg-

ment of P2. Some species within the Zausodes complex possess

only | seta on this segment (Fig. 15A; Table 1). This reduction has

evolved convergently in other genera such as Harpacticus (e.g. H.

compsonyx) and Tigriopus.

(11) Armature P3 enp-2

The inner seta on the middle endopod segment of P3 is present in

most harpacticid genera, including Perissocope. Within the Zausodes

complex, however, this seta is commonly lost and is retained only in

Z. biarticulatus (and the imperfectly described Z. cinctus — see

below).

(12) Armature P3 enp-3

Species of Perissocope and most other genera of the family possess

3 inner setae on the distal endopod segment of P3. Various reduc-

tions occur in the more advanced genera Tigriopus, Paratigriopus

and Discoharpacticus. All species of the Zausodes complex invari-

ably have 2 inner setae on this segment.

(13) Armature P4 exp-3

Sexual dimorphism in the number of armature elements on the P4

exopod is extremely rare within the Harpacticoida. In some species

118

L. BOUCK, D. THISTLE AND R. HUYS

Table 2 Characters used in phylogenetic analysis. Apomorphic character states are referred to in square brackets. Characters 5—7 are multistate characters.

Antennule 9 8-segmented [7-segmented, segments 6 and 7 fused]

Antennule 9 with only setiform elements on segments 3, 4 and 5 [segment 3 with 2 and segments 4—5 with 1 strong, modified spine]

Antennule 2 segment 6 (or homologous portion in 6- or 7-segmented antennule) without enlarged spines [with 2 enlarged pectinate or pinnate spines]

Antennary exopod 3-segmented [state 1: 2-segmented; state 2: 1-segmented]

4 Antennule @ with all elements naked (except for pinnate spines referred to in character 3) [with pinnate or plumose setae on segments 1-6]

Antennary exopod with total of 5 setae (2 on exp-1, 3 on exp-3; exopod 3-segmented) [state 1: 2 on exp-1, 2 on exp-2 and exopod 2-segmented;

state 2: total of 2 setae on single segment]

7 Maxilla with 5 setae on praecoxal endite [state 1: 4 setae; state 2: 3 setae]

8 Pl exp-3 with 2 geniculate (hinged) and 3 simple claws [with 2 geniculate and 2 simple claws]

9 Pl enp-1 with long inner seta [without]

10 P2enp-3 with 2 inner setae [with | inner seta]

11 P3 enp-2 with inner seta [without]

12 P3enp-3 with 3 inner setae [with 2 inner setae]

13. P4exp-3 with 3 outer spines in 2 [with 2 outer spines in 9 , 3 inc’]

14. P4endopod 3-segmented [2-segmented; enp-2 and -3 fused]

15 P4 enp-2 (or homologous portion in 2-segmented endopod) with inner seta [without inner seta]

16 4 enp-3 (or homologous portion in 2-segmented endopod) with 2 inner setae [with 1 inner seta]

17 PS exopod oval or elongate in both sexes [round]

18 P5 Qendopodal lobe expressed [completely lost]

19 P5Qendopodal lobe inner seta not distinctly shorter than other endopodal elements [rudimentary]

20 P59 endopodal lobe 3rd and 4th setae well developed [much shorter than others]

21 Antennulec’segment 3 without transformed elements [with modified spine]

22 2 enp-2C'with apophysis [secondarily lost]

23. P2enp-2C’inner element setiform, not sexually dimorphic [modified into stout spine, distinctly shorter than in 9 ]

24 P2enp-3 outer spine articulating with segment [fused to segment]

25 P3enp-2Couter distal corner not attenuated [attenuated]

Table 3. Character data matrix. Characters listed in Table 2 are scored using the multistate system: 0 = ancestral (plesiomorphic) state, 1 = derived

(apomorphic) state, 2 = further derived state, ? = missing data, indicating that the character state is either unknown or unconfirmed.

lon)

Character 1 2 3 7 8 9 Oil

arenicolus

areolatus

biarticulatus

cookorum

kirstenae

limigenus

paranaguaensis

septimus

sextus

shulenbergeri

stammeri

PERISSOCOPE

cinctus

mROrrerorroocooro

COoOrrHrornrHooore

SCOrPrPrOonrHrHoocore

SoveOoney VTOOOSoOF

NONNNNNNKEEPHEND

NONNNNNNK KK NY LY

BS) (Sy 2S) SO) [Os SF SS SSS

Sey SSS SSS pe

SCSOrrHEoonrHnoceceo

SCOP rePHe eee enone

of the Thompsonulidae (Huys & Gee, 1990) and Tetragonicipitidae

(Kunz, 1984) sexual dimorphism involves the loss of elements in the

male, whereas in species of Huntemannia Poppe an increase in the

number of elements has been reported (Wilson, 1958; Geddes,

1968b). Two new species from the Gulf of Mexico (kirstenae,

cookorum) show 2 outer spines on the distal exopod segment of P4

in the female and a supernumerary spine in the male. All other

species of the Zausodes complex possess 3 spines in both sexes.

(14) Segmentation P4 endopod

Only three species of the Zausodes complex (i.e. arenicolus, kirstenae

and cinctus) have retained the 3-segmented condition of the P4

endopod. In all other species the middle and distal segments have

failed to separate, resulting in a 2-segmented ramus. Lang (1965)

refused to split up Zausodes on the basis of P4 endopod segmentation

since for many other characters close congruence was found between

species with different segmentation. Lang assumed that the 2-

—

123 IAS 1S 6 Te SOR 20) 23 24

VOVERrOVVOOORO!]N

CS) SY PSS NS

oooocooorrcoo

SOorrP RP rE KS Of = oO

SS STN DN IN Yh

OOF FrP ee eS KE OOO rF

COOrrrKr OereKROOooro?e

SSIS) (SISSY SIS (SS)

VyOOCOOCOCCOrFRFFK OO

ywVoooocorcqcocoocooore

IOV Ree VV Ree RO

yVonvrooconryrNrreK OCS

Ye VOCON VRE KER OO

VYrevNOoOCONNrFrK OOS

segmented state had arisen convergently and pointed out that the

original division of the distal segment in Z. sextus is still indicated by

a dentiform notch along the outer margin. An incomplete surface

suture was also found in Z. areolatus (Fig. 11C), suggesting that the

P4 endopod segmentation is probably an evolutionary labile character.

(15) Armature P4 enp-2

Most harpacticid genera displaying a 3-segmented P4 endopod

possess an inner seta on the middle segment. This seta has been lost

in the Zausodes complex (except Z. cinctus), including the two

species in which the middle segment is still separated (kirstenae,

arenicolus).

(16) Armature P4 enp-3

The maximum number of inner setae on the distal (enp-3) endopod

segment of P4 in any species of the Harpacticidae is two. This

number is found in most members of the family, including some (but

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

not all) species of Perissocope such as P. biarticulatus. Within the

Zausodes complex 2 setae are found in only four species (Table 1),

however in both biarticulatus and cookorum the distal segment

represents the fused enp-2 and -3, obscuring the origin of the

proximal inner seta. Comparison with the closely related kirstenae,

in which all segments are expressed, suggests that both inner setae

are derived from enp-3.

(17) Shape P5 exopod of both sexes

The P5 exopod is usually oval or elongate in both sexes. In one

species group of the Zausodes complex the exopod is distinctly

round (e.g. Figs 15D, 18D) which by outgroup comparison with

Perissocope and other genera is regarded here as the apomorphic

condition.

(18) Shape P5 2 endopodal lobe

The endopodal lobe is well developed in the majority of female

harpacticids, including most members of the Zausodes complex. In

four species (biarticulatus, kirstenae, cookorum, cinctus) the whole

baseoendopod is modified, forming a transversely elongated plate,

and the endopodal lobe is no longer expressed (Figs 23B; 30C).

(19-20) Armature P5 2 endopodal lobe

Species belonging to Perissocope and the Zausodes complex typi-

cally have 5 well developed setae on the PS endopodal lobe of the

female. In some species of the latter particular elements have

undergone secondary reduction in size. In the cookorum-kirstenae-

biarticulatus group the innermost seta is rudimentary and sited at

the extreme distal corner near the articulation with the exopod

(Figs 23B, 30C; character 19 in Table 3). Further reduction has

occurred in biarticulatus where the three innermost setae are com-

pletely vestigial (It6, 1979). In the type species Z. arenicolus the

3rd and 4th setae (counted from the innermost according to Huys

et al. (1996)) are very reduced and the innermost one is well

developed. This reduction is treated separately as character 20 in

Table 3 and scored as state 1 in both arenicolus and septimus. In

the latter one of the smaller setae is lost, retaining only 4 elements

_ on the endopodal lobe (Lang, 1965; Mielke, 1990). The reduction

_ of setae 3 and 4 in biarticulatus is regarded here as a further

| derived state of character 19 and not as the apomorphic state of

| character 20.

(21) Armature antennuled

Male antennules in the Harpacticidae are of the subchirocer or chirocer

type. Armature elements are typically modified on the segments

| located either side of the geniculation. In one group of the Zausodes

/ complex the male antennule also possesses a modified element on

| segment 3. Itis represented by a strong spine whichis situated dorsally

near the distal margin of the segment (Figs 12F, 18A).

| (22-23) Modification P2 enp-2¢

| The male P2 endopod is of high significance in understanding the

| phylogeny of the Harpacticidae (It6, 1984). Many genera possess an

Outer spinous apophysis on the middle endopod segment which

| attains its maximum size in Harpacticus and Discoharpacticus.

| Analysis of the phylogenetic relationships within the family (Huys,

| unpubl.) suggests that this apophysis has become gradually smaller

_ during harpacticid evolution and was lost independently in

Paratigriopus, Harpacticella and Zaus-Zausopsis. A similar regres-

sive evolution has also been documented in the Paranannopidae for

| asimilar apophysis on the male P2 endopod (e.g. Gee & Huys, 1991;

Huys & Gee, 1993, 1996). Within the Perissocope—‘Zausodes’

lineage the apophysis is clearly in a state of reduction. The genus

119

Perissocope combines both species with a slender apophysis (P.

biarticulatus, P. exiguus, P. bayeri) and species without such an

uncinate process (P. adiastaltus). Within the former Zausodes com-

plex only the type species Z. arenicolus possesses a short spinous

outgrowth on P2 enp-2 (Fig. 7E) whereas all other species have lost

the apophysis completely (Figs 12D, 17C, 22D).

In both kirstenae and cookorum the inner element of P2 enp-2 is

sexually dimorphic, being setiform in the 9 and modified into a short

stout spine in thec’(character 23 in Table 3; Figs 22D, 29A).

(24) Modification P2 enp-3c%

The outer spine on the distal endopod segment of the male P2 is

frequently modified in the Harpacticidae. In male Harpacticus the

outer spine is usually lost at the final moult or not formed at all in any

male copepodid instar (It6, 1984). In some species such as H.

furcatus Lang the outer spine is represented by a rudimentary setule

(It6 & Fukuchi, 1978). In other genera such as Tigriopus,

Paratigriopus and Zaus the outer spine is not sexually dimorphic

and articulating with the segment. A different modification is found

in male Perissocope where the outer spine is completely integrated

into the distal segment, forming a long, slender apophysis (e.g.

Vervoort, 1964; Pallares, 1975; Watkins, 1987; Wells, 1968). A

similar apophysis was found by It6 (1979) in Z. biarticulatus and in

two new species (kirstenae, cookorum) described here. In the latter

the apophysis is represented by a spinous process which is minutely

pectinate at the inner subapical margin and about equal in length to

the outer spine in the female (Figs 22D, 29A).

(25) Modification P3 enp-2¢

Distinct sexual dimorphism on the P3 endopod is rare in the

Harpacticidae. Differences in surface ornamentation between the

sexes are occasionally found in Harpacticus (It6, 1976; It6 &

Fukuchi, 1978) and in species of the Zausodes complex

(shulenbergeri, kirstenae), however, these have not been included in

the analysis. A more pronounced modification involves the forma-

tion of amucroniform process at the outer distal corner of the middle

segment. This is found in the genus Perissocope and in two closely

related species of the Zausodes complex (kirstenae, cookorum)

(Figs 22E, 29D).

Data matrix and analysis

In order to resolve the relationships within the Zausodes complex

the analysis was executed at the species level. The characters used in

the analysis of phylogenetic relationships between Perissocope and

the 12 species of the Zausodes complex are listed in Table 2. The

character states are explained inside square brackets using the

multistate system: 0 = the ancestral state, | = the derived state, 2 =

a further derived state. The scores for each character and taxon are

compiled in matrix format in Table 3. A question mark indicates

missing data, either because the appendage or structure is unknown

in that species (certain sexually dimorphic characters could not be

scored because only one sex is known) or because it was impossible

to score the character accurately due to the lack of detail in the

original descriptions (cf. Jakobi, 1954). Z. cinctus Krishnaswamy

was excluded from the analysis. Its status is discussed below.

RESULTS AND DISCUSSION

Two most parsimonious trees were obtained with tree-length 36

and consistency index 0.778 (Fig. 33). Both trees differ only in the

position of Z. septimus which in tree A forms a monophyletic group

120 L. BOUCK, D. THISTLE AND R. HUYS

[is

PERISSOCOPE

= biarticulatus | Archizausodes gen. nov.

18, 19, 22, 24

kirstenae l

Mucropedia gen. nov.

13) 2325) = cookorum

CT Bnd INS septimus

Zausodes

arenicolus

sextus

5,6°, 11, 16

areolatus

imi Neozausodes gen. nov.

1.2.3.7, 14, 17,21, 2 limigenus Z g

paranaguaensis

T.L. = 36 10 shulenbergeri

C.I. = 0.778 :

f-value = 138 stammerl

arenicolus

septimus

sextus

areolatus

2 Bates) limigenus

paranaguaensis

f-value = 118 shulenbergeri

stammerli

Fig. 33 Optimal trees depicting relationships between species of the Zausodes complex and the genus Perissocope. Numbers refer to apomorphic states of

characters listed in Table 2 [underlined numbers refer to convergences, superscript letters indicate multistate characters]. T.L. = tree-length; C.I. =

consistency index.

SYSTEMATICS AND PHYLOGENY OF ZAUSODES

with Z. arenicolus, whereas in tree B it occupies a transitionary

position between the type species and the other Zausodes species.

Tree B has a lower f-value (118) than tree A (138), however, we have

selected the latter as the optimal one on account of the lower number

of convergences. In tree A Z. septimus and Z. arenicolus are clus-

tered on the basis of two apomorphies which are unique to these two

species (characters 4 and 20). This grouping is at the expense of

introducing convergences for characters 14 and 22, however, both

these characters already show convergence in other clades (Fig.

33A) and are known to be evolutionary labile. The justification for

grouping Z. septimus with the other Zausodes species in tree B is

based solely on the convergent evolution of characters 14 and 22,

thereby causing additional homoplasies for characters 4 and 20.

The monophyly of the Zausodes complex and its sistergroup

relationship to Perissocope are confirmed. The complex is divided

in two lineages by a strongly supported basal dichotomy and each

lineage is composed of two clades.

The biarticulatus-kirstenae-cookorum lineage is supported by

leg 5 characters such as the loss of the endopodal lobe and the

reduction of the innermost seta of the baseoendopod. Additional

apomorphies are the modification of the distal outer spine on the

male P2 endopod and the sexual dimorphism on the P3 endopod. A

peculiar character shared by these species (but not used in the

analysis) is the presence of a well developed hyaline frill on the

distal endopod segment of P1. Under the traditional light micro-

scope this frill resembles a tuft or fan of spinules sited at the distal

outer corner of enp-2 (Figs 22C, 29E). All three species have

retained the primitive segmentation and setation of the antennary

exopod. Within this lineage Z. biarticulatus occupies the most

primitive position since it is the only species which has retained the

inner seta on P3 enp-2. The other species (cookorum, kirstenae) are

clustered on the basis of their unique sexual dimorphism on the P2

endopod, P3 endopod and P4 exopod.

The monophyly of the second lineage which includes all other

species is supported by the 1-segmented antennary exopod bearing

only 2 setae and the reduced armature on the P4 endopod. A basal

dichotomy divides the lineage into two distinct clades, the

arenicolus-clade and the sextus-clade. The former accommodates

the type species and Z. septimus and is characterized by the pres-

ence of ornate setae on the Qantennule and by the reduction of

particular setae on the 9P5 baseoendopod. Both species have re-

tained primitive antennule characters such as the 8-segmented

condition in the and the complete absence of modified elements

in both sexes. The sextus-clade, encompassing 6 closely related

species, is extremely well supported but largely unresolved. This

is partly due to the deficient descriptions of the Brazilian species

(limigenus, stammeri, paranaguaensis) for which it has proven

_ impossible to score all characters (Table 3). The clade is defined

by the 7(or 6 in areolatus)-segmented 9 antennule, the presence of

_ modified spines in both proximal and distal regions of

the 2 antennule and on segment 3 of thec’antennule, the reduced

| armature on the maxillary praecoxal endite and the round shape of

| the P5 exopod in both sexes. A subgroup, combining

| shulenbergeri and Jakobi’s (1954) species, can be recognized

/ within this clade and is characterized by the presence of only 1

| inner seta on P2 enp-3.

It6 (1979) already remarked that Z. biarticulatus occupied a

| separate taxonomic position within Zausodes and highlighted par-

| ticular similarities with the genus Perissocope. Lang (1965) on the

| other hand favoured a subdivision of the genus Zausodes but was

| reluctant to do so on the basis of P4 endopod segmentation. Our

analysis has revealed marked intrageneric differences in the sexual

dimorphism of all three swimming legs (P2—P4), the setation and

121

armature of the antennary exopod, and the form and modification of

antennulary elements in both sexes. Such variability has not been

recorded for any of the other 8 genera in the family, suggesting that

the Zausodes complex combines distinct lineages which — in accord

with the generic concept currently applied in the Harpacticidae —

would deserve generic status. The genus Zausodes is therefore

redefined to include only Z. arenicolus and Z. septimus, and three

new genera (Archizausodes gen. nov., Mucropedia gen. nov. and

Neozausodes gen. noy.) are proposed, reflecting the basic topology

illustrated in Fig. 33A.

Status of Zausodes cinctus Krishnaswamy, 1954

The taxonomic position of this species from off the Madras coast

(India) is enigmatic since Krishnaswamy’s (1954) description is

erroneous in many aspects. We attempted but were unable to obtain

the type specimens from the Zoological Survey of India in Calcutta.

The strongly elongated PS exopod is unique within Zausodes sensu

lato and leaves little doubt that Z. cinctus is a distinct species.

However, the numerous deficiencies in the original figures make it

impossible to allocate this species to one of the four genera recog-

nized herein. For example, Krishnaswamy (1954) claims that the P1

exopod is only 2-segmented and sexually dimorphic, the male

having only 2 claws and | seta on the distal segment and no outer

seta (corresponding to exp-2). The endopod of this leg is reminiscent

of the laophontid type, bearing only one strong claw on the distal

segment. There is no doubt that the author has overlooked elements

on both rami and that his report of sexual dimorphism is based on

this oversight. Similarly, there is considerable confusion over the

armature formula of the endopods of P2—P4. According to

Krishnaswamy the distal endopod segment of P2—P4 has 1 terminal

and 3 inner setae which Lang (1965) translates as a [211] formula,

implying that an outer spine is present. The latter is invariably short

in Harpacticidae, however, Krishnaswamy’s figures show only a

long plumose seta which is outwardly directed. We speculate that

this unusual orientation of the outer apical seta (perhaps as a result

of imperfect mounting) has obscured the outer spine (cf. It6’s (1979)

drawings of A. biarticulatus) and that the armature formula of P2—

P4 enp-3 is more likely [221] as in Archizausodes and Mucropedia.

If this assumption is correct then Z. cinctus displays the most

primitive swimming leg armature within Zausodes sensu lato since

no other species possesses an inner seta on P4 enp-2 (and A.

biarticulatus being the only other species to exhibit an inner seta on

P3 enp-2). In this context we point out the possible homology

between the latter seta and the proximal inner seta of P4 enp-2 in A.

biarticulatus which we — by reference to the 1.0.221 pattern in

closely related M. kirstenae (Table 1) — have interpreted as originat-

ing from enp-3.

Another remarkable feature is the presence of only 4 elements on

the 9P5 exopod. Krishnaswamy’s illustration shows a distinct gap

between the proximal and distal outer spine which corresponds with

the position of the vestigial seta on the PS of A. biarticulatus (cf. It6,

1979: Fig. 5-1). It is conceivable that a similarly reduced seta is

present in Z. cinctus. Both species, coincidently the only Asian

representatives of the Zausodes complex, also share the absence of

the endopodal lobe and show a similar arrangement of the endopodal

setae (with Z. cinctus having an additional long seta).

The male P2 endopod of Z. cinctus was neither described nor

illustrated by Krishnaswamy (1954). Sexual dimorphism in the P2

endopod is always present in the Zausodes complex, so it is conceiv-

able that it was overlooked. Pending the re-examination of

Krishnaswamy’s types or topotype material we rank Z. cinctus as

species incertae sedis in the Harpacticidae.

122

ACKNOWLEDGEMENTS. We thank Yae Ri Kim of the American Museum

of Natural History for providing the Z. areolatus type material, Dr. Endre

Willassen of the Zoologisk Museum, University of Bergen for providing Z.

areolatus paratype material, and Jan Clark-Walker and Lana Ong of the

Smithsonian Institution for arranging the loan of the Z. arenicolus type

material. This research was supported by ONR grant NO0014—95—1—0750 to

D.T.

REFERENCES

Barnett, P.R.O. 1968. Distribution and ecology of harpacticoid copepods of an

intertidal mud flat. Internationale Revue der gesamten Hydrobiologie 53: 177-209.

Bell, S.S., Hicks, G.R.F. & Walters, K. 1989. Experimental investigations of benthic

reentry by migrating meiobenthic copepods. Journal of experimental marine Biol-

ogy and Ecology 130: 291-303.

& Woodin, S.A. 1984. Community unity: Experimental evidence for meiofauna

and macrofauna. Journal of marine Research 42: 605-632.

Coull, B.C. 1971a. Meiobenthic Harpacticoida (Crustacea, Copepoda) from St. Tho-

mas, U.S. Virgin Islands. Transactions of the American microscopical Society 90:

207-218.

— 1971b. Meiobenthic Harpacticoida (Crustacea, Copepoda) from the North Caro-

lina continental shelf. Cahiers de Biologie marine 12: 195-237.

Foy, M. & Thistle, D. 1991. On the vertical distribution of a benthic harpacticoid

copepod: field, laboratory, and flume results. Journal of experimental marine

Biology and Ecology 153: 153-163.

Geddes, D.C. 1968a. Marine biological investigations in the Bahamas. 5. A new

species of Zausodes (Copepoda, Harpacticoida). Sarsia 32: 63-68.

1968b. A new species of Diagoniceps (Copepoda, Harpacticoidea), and two

previously undescribed male harpacticoids from the Isle of Anglesey. Journal of

natural History 2: 439-448.

Gee, J.M. & Huys, R. 1991. A review of Paranannopidae (Copepoda: Harpacticoida)

with claviform aesthetascs on oral appendages. Journal of natural History 25: 1135—

1169.

Huys, R. 1990. A new harpacticoid copepod family collected from Australian sponges

and the status of the subfamily Rhynchothalestrinae Lang. Zoological Journal of the

Linnean Society 99; 51-115.

& Boxshall, G.A. 1991. Copepod Evolution. 486 pp. Ray Society, London, No.

159.

— & Gee, J.M. 1990. A revision of Thompsonulidae Lang, 1944 (Copepoda:

Harpacticoida). Zoological Journal of the Linnean Society 99: 1-49.

— 1993. A revision of Danielssenia Boeck and Psammis Sars with the establishment

of two new genera Archisenia and Bathypsammis (Harpacticoida: Paranannopidae).

Bulletin of the British Museum of Natural History, Zoology 59: 45-81.

1996. Sentiropsis, Peltisenia and Afrosenia: Three new genera of Paranannopidae

(Copepoda, Harpacticoida). Cahiers de Biologie marine 37: 49-75.

——,, Gee, J. M., Moore, C.G. & Hamond, R. 1996. Synopses of the British Fauna

(New Series): Marine and Brackish Water Harpacticoid Copepods Part 1. viii + 352

pp. Field Studies Council, Shrewsbury, United Kingdom.

It6, T. 1969. Descriptions and records of marine harpacticoid copepods from Hokkaido.

Il. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology 17:

58-77.

1970. The biology of a harpacticoid copepod, Tigriopus japonicus Mori. Journal

of the Faculty of Science, Hokkaido University, Series VI, Zoology 17: 474-500.

1971. The biology of a harpacticoid copepod, Harpacticus uniremis Kroyer.

Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology 18: 235—

D5).

— 1976. Descriptions and records of marine harpacticoid copepods from Hokkaido,

VI. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology 20:

448-567.

1977. New species of marine harpacticoid copepods of the genera Harpacticella

and Tigriopus from the Bonin Islands, with reference to the morphology of copepodid

stages. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology

21: 61-91.

—— 1979. A new species of marine harpacticoid copepod of the genus Zausodes from

the Bonin Islands. Journal of the Faculty of Science, Hokkaido University, Series VI,

Zoology 21: 373-382.

1980. Three species of the genus Zaus (Copepoda, Harpacticoida) from Kodiak

Island, Alaska. Publications of the Seto Marine Biological Laboratory 25: 51-77.

L. BOUCK, D. THISTLE AND R. HUYS

1984. A phylogenetic study of the family Harpacticidae (Harpacticoida): some

problems in character differentiation processes through the copepodid stages. In:

Studies on Copepoda II. Proceedings of the First International Conference on

Copepoda, Amsterdam, The Netherlands, 24-28 August 1981. Crustaceana suppl.

7: 267-278.

—— & Fukuchi, M. 1978. Harpacticus furcatus Lang from the Antarctic peninsula,

with reference to the copepodid stages (Copepoda: Harpacticoida). Antarctic Record

61: 40-64.

— & Kikuchi, Y. 1977. On the occurrence of Harpacticella paradoxa (Brehm) in

Japan; a fresh-water harpacticoid copepod originally described from a Chinese lake.

Annotationes zoologice japonenses 50: 40-56.

Jakobi, H. 1954. Harpacticoida (Cop. Crust.) da microfauna do substrato areno-lodoso

do “Mar de Dentro’ (Ilha do Mel — Baia de Paranagua — Brasil). (Harpacticiden der

Mikrofauna aus sandig-schlammigem Grund im “Mar de Dentro’ (Ilha do Mel — Baia

de Paranagua — Brasil)). Dusenia 5: 209-232.

Krishnaswamy, S. 1954. A new species of harpacticoid copepod from Madras.

Zoologischer Anzeiger 152: 88-92.

Kunz, H. 1984. Beschreibung von sechs Phyllopodopsyllus-Arten (Copepoda,

Harpacticoida) vom Pazific. Mitteilungen aus dem zoologischen Museum der

Universitat Kiel 2(2): 11-32.

Lang, K. Monographie der Harpacticiden (Vorldufige Mitteilung). Almqvist & Wiksells

Boktryckeri Ab, Uppsala: 1-39.

—— 1948. Monographie der Harpacticiden, volume I. 1-896, volume II. 897-1683.

Hakan Ohlssons Boktryckeri, Lund, Sweden.

1965. Copepoda Harpacticoidea from the Californian Pacific coast. Kungliga

Svenska Vetenskaps-akademiens Handlingar (4)10(2): 1-560.

Mielke, W. 1990. Zausodes septimus Lang, 1965 und Enhydrosoma pericoense nov.

spec., zwei benthische Ruderfusskrebse (Crustacea, Copepoda) aus dem Eulitoral

von Panama. Microfauna Marina 6: 139-156.

1997. New findings of interstitial Copepoda from Punta Morales, Pacific coast of

Costa Rica. Microfauna Marina 11: 271-280.

Noodt, W. 1954. Copepoda Harpacticoidea von der chilenischen Meereskiiste. Kieler

Meeresforschungen 10; 247-252.

Pallares, R.E. 1975. Copépodos marinos de la Ria Deseado (Santa Cruz, Argentina).

Contribucion sistematico-ecolégica. IV. Physis (A)34(88): 67-83.

Pfannkuche O. & Thiel, H. 1988. Sample processing. pp. 134-145. In: Introduction

to the study of meiofauna. Smithsonian Institution Press, Washington, D. C.

Ravenel, W.S. & Thistle, D. 1981. The effect of sediment characteristics on the

distribution of two subtidal harpacticoid copepod species. Journal of experimental

marine Biology and Ecology 50: 289-301.

Shirayama, Y., Kaku, T. & Higgins, R.P. 1993. Double-sided microscopic observa-

tion of meiofauna using an HS-Slide. Benthos Research 44; 41-44.

Soyer, J., Thiriot-Quiévreux, C. & Colomines, J.-C. 1987. Description de deux

espéces jumelles du groupe Tigriopus angulatus (Copepoda, Harpacticoida) dans les

archipels Crozet et Kerguelen (Terres Australes et Antarctiques frangaises). Zoologica

Scripta 16: 143-154.

Swofford, D.L. 1993. PAUP (Phylogenetic Analysis Using Parsimony). Version 3.1

(Washington, D.C.: Laboratory of Molecular Systematics. Smithsonian Institution).

—— & Begle, D.P. 1993. PAUP 3.1. User’s Manual. i—vi, 1-257 (Washington, D.C.:

Laboratory of Molecular Systematics. Smithsonian Institution).

Thistle, D. 1980. The response of a harpacticoid copepod community to a small-scale

natural disturbance. Journal of marine Research 38: 381-395.

, Weatherly, G.L., Wonnacott, A. & Ertman, S.C. 1995. Suspension by winter

storms has an energetic cost for adult male benthic harpacticoid copepods at a shelf

site. Marine Ecology Progress Series 125: 77-86.

Varon, R. & Thistle, D. 1988. Response of a harpacticoid copepod to a small-scale

natural disturbance. Journal of experimental marine Biology and Ecology 118: 245—

256.

Vervoort, W. 1964. Free-living Copepoda from Ifaluk Atoll in the Caroline Islands.

Smithsonian Institution United States National Museum Bulletin 236: 1431.

Watkins, R.L. 1987. Descriptions of new species of Bradyellopsis and Perissocope

(Copepoda: Harpacticoida) from the California coast with revised keys to the genera.

Journal of crustacean Biology 7: 380-393.

Wells, J.B.J. 1968. New and rare Copepoda Harpacticoida from the Isles of Scilly.

Journal of natural History 2(3): 397-424.

Westheide, W. & Purschke, G. 1988. Organism processing. pp. 146-160. In: Intro-

duction to the Study of Meiofauna. Smithsonian Institution Press, Washington, D. C.

Wilson, C.B. 1932. The copepods of the Woods Hole region, Massachusetts.

Smithsonian Institution United States National Museum Bulletin 158: 1-635.

Wilson, M.S. 1958. North American harpacticoid copepods. 4. Diagnosis of new

species of fresh water Canthocamptidae and Cletodidae (genus Huntemannia).

Proceedings of the biological Society of Washington 71: 43-48.

Bull. nat. Hist. Mus. Lond. (Zool.) 65(2): 123-131

Issued 25 November 1999

Nybelinia southwelli sp. nov. (Cestoda,

Trypanorhyncha) with the re-description of N.

perideraeus (Shipley & Hornell, 1906) and

synonymy of N. herdmani (Shipley & Hornell,

1906) with Kotorella pronosoma (Stossich,

1901)

HARRY W. PALM

Marine Pathology Group, Department of Fisheries Biology, Institut fiir Meereskunde an der Universitat Kiel,

Diisternbrooker Weg 20, D 24105 Kiel, Germany

THORSTEN WALTER

Marine Pathology Group, Department of Fisheries Biology, Institut fiir Meereskunde an der Universitat Kiel,

Diisternbrooker Weg 20, D 24105 Kiel, Germany

SYNOPSIS.

During a study of Nybelinia material deposited at The Natural History Museum, London, Nybelinia southwelli sp.

noy. was discovered amongst material identified and described as Tetrarhynchus perideraeus Shipley & Hornell, 1906 from

Rhina ancylostoma and Nebrius ferrugineus from Sri Lanka. The new species belongs to the subgroup IBa of Palm et al. (1997),

which includes species having a homeoacanthous heteromorphous metabasal armature and a characteristic basal armature where

the basal hooks are smaller or equal in size to the metabasal hooks. It can easily be distinguished from all other members of this

group by having characteristic rose-thorn shaped metabasal and slender basal hooks. The type material of Nybelinia perideraeus

(Shipley & Hornell, 1906) was borrowed from the Natural History Museum, Vienna, for comparison, and is re-described. N.

dakari Dollfus, 1960 is considered synonymous with N. perideraeus. Nybelinia herdmani (Shipley & Hornell, 1906), also placed

in the subgroup IIBa by Palm et al. (1997), is considered synonymous with Kotorella pronosoma (Stossich, 1901) Euzet &

Radujkovic, 1989. The subgroupings of Nybelinia species based on the species specific tentacular armature appear to be useful

for further taxonomic studies within the genus.

INTRODUCTION

Trypanorhynch cestodes are common parasites of marine

elasmobranchs, where they mature in the stomach or the spiral

valve. The plerocercoids are parasitic in many teleosts and a variety

of invertebrates while the first intermediate hosts are crustaceans.

Among trypanorhynch cestodes, Nybelinia Poche, 1926 is the larg-

est genus. Palm ef al. (1997) listed 43 adequately described species

while leaving 4 species of uncertain status, and Jones & Beveridge

(1998) added N. queenslandensis. Vijayalakshmi et al. (1996) de-

scribed Tentacularia scoliodoni on the basis of the tentacular

armature, not considering the most recent generic definitions of

Tentacularia and Nybelinia in the key of Campbell & Beveridge

(1994). The species strongly resembles N. indica Chandra, 1986 and

N. africana Dollfus, 1960, and should be treated as species of

uncertain status pending on examination of further material. Thus,

with a total of 44 adequately described species, the genus Nybelinia

currently comprises the most species-rich genus within the order

Trypanorhyncha.

One of the biggest problems for taxonomic work within the

genus, apart from poor original descriptions, remains the lack of

information on material available in museum collections for com-

parative morphological studies. Many species have a similar scolex

morphology and tentacular armature. Additionally, several species

descriptions are based on single specimens and data on intraspecific

variability are scarce. Studies of Nybelinia deposited in collections

are needed to determine validity as well as for re-descriptions.

During a study on Nybelinia material deposited at the British

Museum, Natural History, slides labelled and described as

Tetrarhynchus perideraeus Shipley & Hornell, 1906 from the T.

Southwell collection (Southwell, 1929a, p. 257-259) appeared to

bear a species different to that indicated. The present study was

carried out to clarify the identity of this material. The type material

of Nybelinia perideraeus was borrowed from the Natural History

Museum, Vienna, for comparison, and re-description. Beside this,

the taxonomic position of NV. herdmani (Shipley & Hornell, 1906) is

clarified.

MATERIAL AND METHODS

Standard measurements and drawings of the scoleces of Nybelinia

specimens deposited in the Parasitic Worms Division, The Natural

History Museum London (BMNH), were made using a Leitz Wetzlar

Dialux 20 microscope with an ocular micrometer. The type speci-

mens of Nybelinia perideraeus and N. herdmani were borrowed

from the collection of the Naturhistorisches Museum Wien (VNHM)

and examined with a Leitz Wetzlar Orthoplan microscope. Draw-

ings were made using a Leitz Wetzlar Dialux 22 microscope with a

drawing tube.

124

The following measurements were taken: Scolex length (SL),

scolex width at level of pars bothridialis (SW), pars bothridialis

(pbo), pars vaginalis (pv), pars bulbosa (pb), pars postbulbosa (ppb),

velum (vel), appendix (app), bulb length (BL), bulb width (BW),

bulb ratio (BR), proportions of pbo/pv/pb (SP), tentacle width (TW),

and tentacle sheath width (TSW). If possible, the tentacle length

(TL) was estimated. Additionally, the tentacular armature was de-

scribed as follows: armature homeomorphous or heteromorphous,

hooks per half spiral row (hsr), total hook length (L) and the total

length of the base (B).

All measurements are given in micrometers unless otherwise

indicated. Illustrations are provided where useful, otherwise the

reader is referred to illustrations of other authors. The classification

follows that of Palm (1995, 1997) and the orientation of the tentacu-

lar surfaces follows that of Campbell & Beveridge (1994).

RESULTS

The comparison of Tetrarhynchus perideraeus Shipley & Hornell,

1906, BMNH 1977.11.4.7-9, 1977.11.11.38 from the Southwell

collection with the co-type material of 7: perideraeus from the

VNHM (2109, 2111) revealed differences. The BMNH material

corresponds neither with the co-types from the VNHM nor with

specimens of T. perideraeus as re-described by Dollfus (1942, Figs

98-100). Similarly, the type material of 7: perideraeus from the

VNHM clearly differs from the specimens described by Dollfus

(1942). Thus, the material deposited and described above belongs to

three different Nybelinia species.

In the following, Nybelinia perideraeus (Shipley & Hornell,

1906) is re-described and the material collected by T. Southwell and

deposited in the BMNH, which does not fit in any of the currently

accepted species (Palm et al., 1997), is described as N. southwelli sp.

nov. Another species deposited in the VNHM, Tetrarhynchus

herdmani (Shipley & Hornell, 1906), can be considered synony-

mous with Kotorella pronosoma (Stossich, 1901) Euzet &

Radujkovic, 1989.

Superfamily TENTACULARIOIDEA Poche, 1926

Family TENTACULARIIDAE Poche, 1926

Genus NYBELINIA Poche, 1926

Nybelinia southwelli sp. nov. (Figs 1-3c)

SYNONYMY.

N. perideraeus (Shipley & Hornell, 1906) of Southwell (1924,

1929a, b, 1930)

MATERIAL DESCRIBED. Holotype, BMNH 1977.11.4.7, J. Pearson

leg., 30.9.1925, 1 adult from Rhina ancylostoma Bloch & Schneider,

1801 (=Rhynchobatus anchylostomus) Sri Lanka (Ceylon); Paratype,

BMNH 1977.11.4.8-9, J. Pearson leg., 30.09.1925, 1 adult from

Nebrius ferrugineus (Lesson, 1830) (=Ginglymostoma concolor),

Sri Lanka. Other material: BMNH 1977.11.4.8—9 (2 slides) and

BMNH 1977.11.11.38.

DESCRIPTION. With the characters of the genus Nybelinia: The

scolex (BMNH 1977-11.4.8-9, Fig. 28B in Southwell, 1929a;

BMNH 1977.11.11.38, see Fig. 1) is craspedote with a total length

(with velum) of 1701/holotype (1739/paratype). The length of the

bothridia is more than half the scolex length, the width at the pars

H.W. PALM AND T. WALTER

Fig. 1 Scolex of Nybelinia southwelli sp. nov. from Nebrius ferrugineus.

Scale bar=150 um.

bothridialis is 945 (1134); pbo=1078 (1058), pv=982 (926), pb=485

(415), ppb=56 (38), vel=298 (420), BL=474 (404), BW=166 (185),

BR=2.9:1 (2.2:1), SP=2.2:2:1 (2.5:2.2:1).The tentacles are long and

slender and diminish in size towards the tip; TW basal=46—S1 (51—

56), TW metabasal 33-38. A basal tentacular swelling is not present.

The tentacle sheaths are sinuous or spirally coiled; TSW 66-70 (51—

56). Prebulbular organs and muscular rings around the basal part of

the tentacle sheaths are absent. The retractor muscles originate in the

basal part of the bulbs.

The armature is homeoacanthous, heteromorphous with a charac-

teristic basal armature consisting of 13—14 rows of homeomorphous

hooks (Figs 2a, c(i)). The number of hooks per half spiral diminishes

towards the apical part of the tentacles: hsr=6 (basal), hsr=4—5

(apical). The massive hooks of the metabasal (Figs 2b, c(ii)) and

apical (Figs 2b, c(ii1)) armature are different in shape and size on

bothridial and antibothridial tentacle surfaces. The metabasal ten-

tacular armature on the bothridial surface consists of strongly

recurved solid hooks with a large base; L=17—18 (13-15), B=14-16

(10-12). On the antibothridial surface, the hooks are more slender

and slightly curved with a stout base; L=20—22 (15-18), B=12-14

(8-9). The basal armature is homeomorphous, basal hooks with a

stout base, a slender shaft, and strongly recurved at the tip (L=18—20

(14-16), B=7-8 (6-7)) (Figs 2a, c(i)). The first basal hooks are

smaller than those of the remaining basal armature.

The morphology of the mature and gravid segments of N.

southwelli sp. noy. is given in Southwell (1929a, Figs 28E-F), a

description and measurements of the proglottids is given in Southwell

(1929a, p. 259). The morphology of the strobila and mature and

gravid proglottids of BMNH 1977.11.11.38 is given on Figs 3a-c. N.

southwelli sp. nov. has a long acraspedote strobila of more than 232

proglottids (BMNH 1977.11.4.8—-9, strobila not complete), which

DESCRIPTION OF THREE NYBELINIA SPECIES

2a 2b

Fig. 2a—c_ Nybelinia southwelli sp. nov. a. homeomorphous basal

tentacular armature, external surface. b. metabasal tentacular armature,

external surface. c. basal (i), metabasal (ii) and apical (iii) tentacular

hooks. Scale bar=20 um.

are wider than long and have distinct convex margins (Fig. 3a). The

size of the proglottids is similar along a large part of the strobila

(around 130th proglottid: 800-870 x 260-300, last proglottids: 900—

970 x 300-370). The genital atrium is ventrosubmarginal in about

the middle of the proglottids and alternates irregularly. The cirrus

sac is elongate, large, directed anteromedially from the genital

atrium and the sac is thin-walled (Figs 3b—c). The cirrus is unarmed,

coiled within the sac and an internal seminal vesicle was not seen;

external seminal vesicle absent. Testes arranged in double layer,

number 70-80, ovoid, 25—42 in diameter, encircle the female genital

complex, and some testes are present anterior to the cirrus sac.

Vagina not seen. Ovary bilobed, 130-160 wide x 80-105 long

(BMNH 1977.11.4.8—9). Gravid segments with vitelline follicles of

15-20 in diameter, uterus extending over most of the proglottids.

Other details of the female genital complex not seen.

ETYMOLOGY. The new species was named after T. Southwell, in

whose collection the present specimens were found.

REMARKS.

Southwell (1924, 1929a, 1930) gave a first description of WN.

| southwelli sp. nov. but identified the specimens as N. perideraeus

| Shipley & Hornell, 1906. His scolex measurements lie within the

| same range (Southwell, 1929a, p. 257—258; 1930, p. 84-86), and the

illustrations of the tentacular armature are similar to Figs 2a—c. Fig.

| 28d in Southwell (1929a) as well as Fig. 16d in Southwell (1930)

illustrate the slender, strongly recurved hooks of the basal tentacular

125

armature (Fig. 2a), and Southwell’s Figs (28c and 16c) illustrate the

metabasal armature with the rose-thorn shaped hooks (Fig. 2b).

However, in contrast to his drawings, Southwell wrongly interpreted

the tentacular hooks as being uniform in size, between 10 and 12 um,

and shape.

The present material illustrates that the material belongs to

Nybelinia subgroup UBa of Palm et al. (1997), which includes

species having an homeoacanthous heteromorphous metabasal ar-

mature, a characteristic basal armature and basal hooks smaller than

or equal to the metabasal hooks. The species can be easily distin-

guished from N. nipponica Yamaguti, 1952, N. rougetcampanae

Dollfus, 1960 and N. yamagutii Dollfus, 1960 by the lack of bill

hooks and the presence of a homeomorphous basal armature. N.

herdmani can be considered synonymous with Kotorella pronosoma

(see following), and has a different scolex as well as a different

tentacular armature. Nybelinia southwelli sp. nov. is similar to N.

beveridgei Palm, Walter, Schwerdtfeger & Reimer, 1997, the only

other species having a homeomorphous basal and heteromorphous

metabasal armature. It can be distinguished by a much smaller

scolex size, smaller tentacular hooks, 13—14 rows of basal hooks in

contrast to 6—7 in N. beveridgei, and the absence of a muscular ring

around the tentacle sheaths.

It has to be pointed out that though the form and characteristic

arrangement of the tentacular armature was the same, N. southwelli

from the two different elasmobranch species differs slightly in hook

sizes along the tentacle. The holotype obtained from Rhina

ancylostoma had basal hooks with a maximal length of 20, while 3

scolices taken from Nebrius ferrugineus had basal hooks with a

maximal length of 16. Similarly, the metabasal hooks of the holotype

were larger. This observation can be interpreted as a record of

morphological variability for NV. southwelli depending on two differ-

ent elasmobranch hosts.

Nybelinia perideraeus (Shipley & Hornell, 1906) Dollfus,

1930 (Figs 4-6)

SYNONYMY.

Tetrarhynchus perideraeus Shipley & Hornell, 1906

Stenobothrium perideraeum (Shipley & Hornell, 1906) Pintner,

1913

Nybelinia dakari Dollfus, 1960 (new synonymy)

MATERIAL EXAMINED. Co-types VNHM 2109 and 2111; 3 adults

from the small intestine of Glyphis gangeticus (Miller & Henle,

1839) (=Carcharhinus gangeticus) (collection of T. Southwell).

DESCRIPTION. The scolex is craspedote (Fig. 4) with a total length

(with velum) of 1222, 1092/co-type VNHM 2109 (1352/ co-type

VNHM 2111); SW 767, 770 (715), pbo=546, 533 (637), py=520,

390 (540), pb=408, 461 (429), ppb=59, 16 (69), vel=195, 299 (276),

BL=390, 430 (445), BW=103, 114 (115), BR=3.8:1, 3.8:1 (3.9:1),

SP=1.3:1.3:1, 1.2:0.8:1 (1.5:1.3:1). A basal tentacular swelling is

absent, TW basal=39, 33 (42), TW metabasal=30, 33 (35), TW

apical=20, TL=500-570; prebulbular organs and muscular rings

around the tentacle sheaths are absent; the retractor muscle inserts in

the basal part of the bulbs; TSW=35—40.

The armature is homeoacanthous, heteromorphous, and the hooks

of the basal armature are similar to those of the metabasal armature

(Figs 5a—b). hsr=6—7. The hooks of the metabasal armature are

different in shape and size on bothridial and antibothridial tentacle

surfaces (Figs 5a). On the bothridial surface, the tentacular armature

consists of strongly recurved, solid hooks with a large base; L=10.5—

13.0, B=10.5—11.5. On the antibothridial surface, the hooks are

126

H.W. PALM AND T. WALTER

Fig. 3a—c Strobila of Nybelinia southwelli sp. nov. a. acraspedote arrangement of the proglottids with characteristic convex margins. b. mature proglottid

with the large cirrus sac and oviform testes. c. gravid proglottid. Scale bar b=100 um and scale bar c=110 pm.

more slender and slightly curved; L=7.5—10.0, B=8—9. The basal

armature is heteromorphous (Fig. 5b). The basal hooks are of the

same shape and size as those in the metabasal region of the tentacle.

External surface hooks, L=10.5—11.5, B=10.5—11.8; internal hooks,

L=6.5-8, B=8-9.

The morphology of the mature proglottid of N. perideraeus

(VNHM 2109) is given as Fig. 6. N. perideraeus has a long

acraspedote strobila of about 300 proglottids (strobila on 2 slides).

While the anterior proglottids are wider than long (520-560 x 266—

300), the final proglottids are longer than wide (559-741 x 520-530),

and continuously increasing in size. The genital atrium is

ventrosubmarginal in about the anterior third of the proglottids and

alternates irregularly. The cirrus sac is elongate (254 x 60), directed

anteromedially from the genital atrium and the sac is thin-walled.

The cirrus is unarmed, coiled within the sac and an internal seminal

vesicle was not seen; external seminal vesicle absent. Testes ar-

ranged in double layer, number 86—97, ovoid, 33-49 in diameter,

encircle the female genital complex, and some testes are present

anterior to the cirrus sac. Other details of the female genital complex

not seen.

REMARKS.

In the original description of Tetrarhynchus perideraeus, Shipley &

Hornell (1906) described long worms with a slender scolex bearing

long bulbs as well as slender tentacles. The tentacles as well as the

tentacular sheaths are short and the tentacular armature consists of

oblique rows of very minute hooks of uniform size. However, these

characters do not adequately define the species. Dollfus (1930)

remarked that without examination of the original material, WN.

perideraeus is not distinguishable from N. lingualis. A description

of Stenobothrium perideraeum by Pintner (1930) did not consider

the form and arrangement of the tentacular armature, and thus, was

not helpful in solving this taxonomic problem. Southwell (1924,

1929a, 1930) described specimens which he named N. perideraeus.

However, Pintner (1930) noticed that the material observed by

Southwell (1929a, 1930) belonged to a different species.

Dollfus (1942) gave a description of N. perideraeus, summarising

the information given by Shipley & Hornell (1906) and Pintner

(1930), and illustrated the species on basis of material collected

from Carcharhinus melanopterus (Quoy & Gaimard, 1824) from

the Gulf of Suez, Egypt. While remarking that the descriptions of the

DESCRIPTION OF THREE NYBELINIA SPECIES

Fig. 4 Scolex of Nybelinia perideraeus sp. nov. from Glyphis gangeticus.

Scale bar=150 pm.

tentacular hooks by Shipley & Hornell (1906) and Pintner (1930)

were not unambiguous, he added with his own illustrations given in

figs 97-100 a further type of tentacular armature for N. perideraeus.

He described a characteristic basal armature, where the hook form

changes from rose-thorn shaped in the basal part to slender spiniform

with sharply recurved tip in the metabasal part. Additionally, the

size of the scolex illustrated, 400-500 pm, is much smaller than that

given before for N. perideraeus. The illustrated specimens from C.

melanoperus correspond in scolex size and morphology as well as in

the detailed described tentacular armature to N. africana Dollfus,

1960 (compare Figs 97—100 in Dollfus (1942) with figs 10-19 in

Dollfus (1960). Thus, we consider both sets of material to belong to

the same species, N. africana Dollfus, 1960.

Vijayalakshmi et al. (1996) described N. perideraeus from

Scoliodon palasorrah from India with a uniform tentacular armature

of minute curved hooks 10um long. The co-type material examined

in the present study demonstrates that the tentacular armature of N.

perideraeus is homeoacanthous heteromorphous with rose-thorn

shaped tentacular hooks of the same size along the tentacle. Thus,

the identity of the material described by Vijayalakshmi et al. (1996)

still needs to be clarified.

The measurements and figures of the co-type specimen VNHM

2109 as well as the size of the tentacular hooks correspond closely

with those of N. dakari Dollfus, 1960 from the west African coast

and it is therefore considered synonymous with N. perideraeus.

Thus, Nybelinia perideraeus is the only species in subgrouping I[Ab

of Palm et al. (1997), characterized by a homeoacanthous, hetero-

morphous metabasal armature without a characteristic basal armature

and basal tentacular hooks of similar size or bigger than in the

metabasal part of the tentacle.

NAY

Fig. 5a—b Nybelinia perideraeus. a. metabasal tentacular armature,

internal surface. b. basal tentacular armature, external surface.

Abbreviation: B=bothridia. Scale bar=20 um.

Kotorella pronosoma (Stossich, 1901) Euzet &

Radujkovic, 1989 (Figs 7-9)

SYNONYMY.

Rhynchobothrium pronosomum Stossich, 1901

Nybelinia pronosomum (Stossich, 1900) Dollfus, 1930

Otobothrium pronosomum (Stossich, 1900) Dollfus, 1942

Tetrarhynchus herdmani Shipley & Hornell, 1906 of Southwell

(1929a, b 1930)

Stenobothrium herdmani (Shipley & Hornell, 1906) Pintner, 1913

Nybelinia (Nybelinia) herdmani (Shipley & Hornell, 1906) Dollfus,

1930

MATERIALEXAMINED. Type VNHM 2095, | adult from Himantura

imbricata (Bloch & Schneider, 1801) (=Trygon walga), Sri Lanka

(Ceylon) (collection of Shipley & Hornell); VNHM 2097, 1 adult

from Himantura imbricata, Sri Lanka (collection of Shipley &

Hornell).

DESCRIPTION. Kotorella pronosoma was described in detail by

Euzet & Radujkovic (1989). The scolex measurements of K.

pronosoma together with the measurements of the type material of

128 H.W. PALM AND T. WALTER .

° 50 Cte

° ° ° ° 3 °

eeaec 00° 0% oe 2% 5008 © ? °

oo °p °0 0 8 Og 6

Fig.6 Mature proglottid of Nybelinia perideraeus. Scale bar=100 um.

N. herdmani are summarised in Table 1. In addition to these data, the

following characters were observed: The 4 bothridia of N. herdmani

(Shipley & Hornell, 1906) have free lateral and posterior margins

with a distinct space between the bothridia (Fig. 7). The bothridial

margins seem not to be fused with the scolex even apically.

Prebulbular organs around the tentacle sheaths are absent and

muscular rings are not visible.

The armature of Kotorella pronosoma was described by Euzet &

Radujkovic (1989) and Campbell & Beveridge (1994). The arma-

ture of the type material of N. herdmani is homeoacanthous,

heteromorphous (Figs 8a—b). The tentacular hooks on the

antibothridial tentacle surface increase in size towards the distal part

of the tentacle, the hooks on the bothridial tentacular surface are of

similar size along the tentacle. The metabasal hooks on the bothridial

surface are tightly packed and have a broad, diamond-shaped basal

plate (L=13.5—14.5, B=8). The distance between these hooks ap-

pears to be slightly wider towards the apical part of the tentacle. On

the antibothridial surface, slender and spiniform hooks without

enlarged basal plates increase in size towards the end of the tentacle.

The hooks are more widely spaced than on the bothridial surface.

Basal hooks: L=6—8, B=2—3; metabasal hooks: L=13—14, B=3—4. A

basal tentacular swelling is absent. hsr (basal)=8, hsr (metabasal)=6—

The morphology of the mature proglottid of N. herdmani is given

in Fig. 9. N. herdmani has a short acraspedote strobila of about 76

proglottids behind the velum. While the anterior proglottids behind

the velum are wider than long (345-360 x 20-40), their length

increases in size towards a rectangular shape (276-310 x 175-215).

The final proglottids are longer than wide (715-755 x 560-610).

The genital atrium is ventrosubmarginal, pre-equatorial and alter-

nates irregularly. The cirrus sac is elongate (242 x 70), directed

medially from the genital atrium and the sac is thin-walled. The

cirrus is unarmed, coiled within the sac and an internal seminal

vesicle was not seen; external seminal vesicle absent. Testes over-

lapping but arranged in single layer, number between 35-48. The

Fig. 7 Scolex of Kotorella pronosoma (Nybelinia herdmani) from size of ovoid testes varies depending on number of proglottid

Himantura imbricata. Scale bar=150 um. (anterior proglottids: 37-47; median proglottids: 53-64; posterior

DESCRIPTION OF THREE NYBELINIA SPECIES

129

Fig. 8a-—b Kotorella pronosoma (Nybelinia herdmani). a. metabasal tentacular armature, external surface. b. basal tentacular armature, external surface.

Scale bars=10 um.

proglottids: 71-85 in diameter). Testes encircle the female genital

complex (Fig. 9). Female genital complex median.

REMARKS.

In 1906, Shipley & Hornell described Tetrarhynchus herdmani from

the alimentary canal of Himantura imbricata and Rhynchobatus

djeddensis from the Gulf of Mannar (Sri Lanka). However, only a

few measurements were given and the tentacular hooks were de-

scribed as being similar and of the same size (10 um) along the

tentacle. Southwell (1929a) cited Shipley and Hornell (1906) and

listed T: herdmani with T. perideraeus as a species with extremely

minute (practically equal in size) hooks arranged in spirals

(Southwell, 1929b). Pintner (1930) re-described the type material of

T. herdmani and reported a homeoacanthous, heteromorphous arma-

ture. His description of the tentacles with about 10 small hooks per

row, tightly arranged and forming a mosaic on one side, was

emended by Dollfus (1942), who reported 14 um large hooks with a

large base. The drawings of Pintner (1930, Figs 67a—b’) also give a

metabasal hook size between 10-11 um on the lateral (antibothridial)

and 10-14 um on the medial (bothridial) tentacle surface (7—8 um of

basal antibothridial hooks and 10-14 um of basal bothridial hooks?

/ Fig. 67a’and 67b’). Thus, the drawings of the tentacular armature

as given by Pintner (1930) correspond to the armature of the type

material as described above. Our scolex measurements of the types

of N. herdmani also correspond to those given by Pintner (1930) and

Dollfus (1942) for N. herdmani (Table 1).

Euzet & Radujkovic (1989) re-described Kotorella pronosoma

(Stossich, 1901) from the spiral valve of Dasyatis pastinaca L. from

the Mediterranean Sea. Though the absolute values of their scolex

measurements are about 1/3™ smaller than those given for Nybelinia

herdmani (Table 1), the scolex and bulb ratios are very similar (see

above). The hooks size as given by Euzet & Radujkovic (1989) for

K. pronosoma is also about 1/3 smaller (hooks size between 5-8

uum). Campbell & Beveridge (1994, Figs 7.48-7.50) gave additional

figures of the scolex and tentacular armature of K. pronosoma with

a metabasal/apical hook size of about 10-11 um (bothridial and

antibothridial) and a basal hooks size of about 8—9 um (bothridial)

and 5—6 wm (antibothridial). The arrangement of the tentacular

hooks, however, correspond between all specimens of N. herdmani

and K. pronosoma considered above.

The only detailed description of the strobila is given by Euzet &

Radujkovic (1989) for Kotorella pronosoma. The general morphol-

ogy of the proglottids (Fig. 2 in Euzet & Radujkovic, 1989), the

central female genital complex, the pre-equatorial irregularly alter-

nating cirrus sac and number of testes is corresponding to the type

material of N. herdmani (Fig. 9). Thus we conclude that both

material belongs to the same species, Kotorella pronosoma (Stossich,

1901) Euzet & Radujkovic, 1989.

DISCUSSION

With the description of Nybelinia southwelli sp. nov. and the syn-

onymy of N. dakari with N. perideraeus and N. herdmani with

Kotorella pronosoma, the number of adequately described valid

species within the genus Nybelinia is reduced from 44 to 43.

However, the genus remains the most species-rich within the order

Trypanorhyncha.

Palm et al. (1997) pointed out that the genus Nybelinia seems to

have many species with a cosmopolitan distribution pattern. In the

present study, the two synonymies reported further extend the

reported range of distribution for both species. Nybelinia perideraeus

now can be considered to have a transoceanic distribution. It was

originally described from Sri Lanka by Shipley & Hornell (1906),

and was re-described as N. dakari from the north-west African coast

(Dollfus, 1960) and recorded as N. dakari from the China Sea by

Yang et al. (1995). If the specimens labelled N. perideraeus in the

130

H.W. PALM AND T. WALTER

Fig.9 Mature proglottid of Kotorella pronosoma (Nybelinia herdmani). Scale bar=100 um.

Table 1 Scolex measurements (in um) of Kotorella pronosoma (Stossich, 1901) Euzet & Radujkovic, 1989 and Nybelinia herdmani (Shipley & Hornell,

1906) (n=number of specimens examined)

species Kotorella pronosoma Nybelinia herdmani

Author / Euzet & Radujkovic Shipley & Hornell Pintner Present study

Year (1989) (1906) (1930)

n 2 7 - 2

Scolex length: 650 1000 900 (880)?—1000 980 (900-1060)

Scolex width! - - - 374 (297-450)

Pars bothridialis 380 - 600 (570-630) 610 (570-650)

Pars vaginalis 550 ~ 615 (590-640) 615 (590-640)

Pars bulbosa 110 80-100 155 (150-160) 192 (188-195)

Bulb length 100 Short 160 (140-180) 170 (160-180)

Bulb width 60 - 110 (90-130) 100 (90-110)

Velum 140 - 160 (140-180) 160 (140-180)

Bulb length/bulb width 145 2 il - Ilse A/S

pbo/pv/pb.. 35) a5) 8 | - 3,9:4,0:1 SPAS)? Bull

Tentacle length 250-275 - - 308 (260-357)

Tentacle width 12-15 = - 16-29

'Maximum width

? Pintner (1930) in Dollfus (1942)

drawings by Dollfus (1942) are considered to belong to N. africana,

N. africana has now been reported to occur all around Africa, from

the Mediterranean, the Gulf of Suez and the north-west and south-

east African coasts (Dollfus, 1942, 1960, Palm et al., 1997). Similarly,

Kotorella pronosoma (N. herdmani) is known to occur in the Medi-

terranean (Euzet & Radujkovic, 1989) and in the Indian Ocean

(Shipley & Hornell, 1906). This indicates not only a transoceanic

distribution pattern for the tentaculariid trypanorhynch species within

the genera Jentacularia and Nybelinia but also for Kotorella. Thus,

it seems that the tentaculariid trypanorhynchs sensu Palm (1995,

1997) not only demonstrate a remarkable morphological uniformity

within the family but also a similar distribution pattern, indicating a

similar life cycle biology. This supports the suppression of the

family Kotorellidae Euzet & Radujkovic, 1989, as proposed by

Campbell & Beveridge (1994) and Palm (1995, 1997).

The synonymy of Nybelinia herdmani with Kotorella pronosoma

demonstrates the high similarity between species belonging to these

two tentaculariid genera. However, in K. pronosoma, the basal

hooks with a diamond shaped basal plate also demonstrate a similar-

ity to the basal hooks of Tentacularia coryphaenae Bosc, 1797 (see

Figs 2-4 in Palm, 1995). Additionally, a wide space between the

elongated bothridia appears to be characteristic only for these two

genera, which is in contrast to more triangular and more tightly

spaced bothridia within the genus Nybelinia. These differences still

DESCRIPTION OF THREE NYBELINIA SPECIES

justify the genus Kotorella Euzet & Radujkovic, 1989 within the

Tentaculariidae Poche, 1926. However, the gross morphological

characters such as scolex form, proportions and form of the bulbs

indicate a close phylogenetic relationship between Kotorella and

Nybelina, as proposed by Campbell & Beveridge (1994) and Palm

(1995, 1997). Interestingly, a cladistic analysis of the genera within

the Trypanorhyncha failed to assign the genus Kotorella to the same

clade as the other tentaculariid genera (Beveridge et al., 1999).

The scolex measurements for Nybelinia southwelli sp. nov. ap-

pear to be variable. Although having a similar scolex size to the

holotype, the tentacular hooks of the paratype were distinctly smaller.

It appears that measurements of armature within a species can show

variability as do other scolex measurements, e.g. scolex length (N.

nipponica: 1.35—2.9; N. karachii: 1.25—2.5 (Yamaguti, 1952, Kurshid

& Bilgees, 1988)), scolex width (N. beveridgei: 2.1-3.1; N. thyrsites:

0.66—1.06 (Palm et al., 1997, Beveridge & Campbell, 1996)) and

bulb length (N. nipponica: 310-550 (Yamaguti, 1952)). The syn-

onymy of Nybelinia herdmani with Kotorella pronosoma gives a

further example on scolex variability within tentaculariid

trypanorhynchs. The absolute values of scolex measurements as

well as hook sizes varied about 1/3™ of total value between the

different specimens. Kotorella pronosoma as described by Euzet &

Radujkovic (1989) can be considered as smaller specimens than the

material examined by us, which is reflected in both, smaller scolex

measurements and smaller hooks. This observation generally ques-

tions the usage of minor absolute values in scolex and hook

measurements as main species distinguishing characters within

tentaculariid cestodes. A similar variability in the scolex morphol-

ogy of trypanorhynch plerocerci has been demonstrated for

Otobothrium penetrans by Palm et al. (1993). Whether such differ-

ences are generally due to different host species or a different age of

the postlarvae, plerocerci or adults compared cannot be decided at

present.

This variability within trypanorhynch cestodes has resulted in the

description of several invalid species, especially within the genus

Nybelina, as proposed by Palm ef al. (1997). However, the

subgrouping of Nybelinia species based on characters of the tentacu-

lar armature appears to be a useful tool for further taxonomic studies

within the genus (see Palm et al., 1997). In the present study, all

species within the subgroupings IIAb and IIBa are clearly defined.

Further studies are needed to clarify the validity of species within the

other 6 groupings, leading to a complete revision of the genus

Nybelina.

ACKNOWLEDGEMENTS. Our thanks are extended to Dr. D. Gibson and E.

Harris, Parasitic Worms Division, Natural History Museum London, and Dr.

H. Sattmann, Naturhistorisches Museum Wien, for providing access to the

examined material. We are grateful to Dr. R.A. Bray for revising an earlier

draft of the manuscript. Financial support was provided by the Institut fiir

Meereskunde Kiel.

131

REFERENCES

Beveridge, I. & Campbell, R.A. 1996. New records and descriptions of trypanorhynch

cestodes from Australian fishes. Records of the South Australian Museum 29: 1-22.

, Campbell, R.A. & Palm, H. 1999. Preliminary cladistic analysis of genera of the

cestode order Trypanorhyncha Diesing, 1863. Systematic Parasitology 42: 29-49.

Campell, R.A. & Beveridge, I. 1994. Order Trypanorhyncha Diesing, 1863. pp. 51-

148. In: Khalil, L.F., Jones, A. & Bray, R.A. (eds) Keys to the cestode parasites of

vertebrates. CAB International, Wallingford.

Dollfus, R.P. 1930. Sur les Tétrarhynques. (2°contribution). Définition des genres

(suite). Mémoires de la Société Zoologique de France 29: 139-216.

1942. Etudes critiques sur les Tétrarhynques du Museum de Paris. Archives du

Muséum national d ‘Histoire Naturelle 19: 1466.

1960. Sur une collection de Tétrarhynques homéacanthes de la famille des

Tentaculariidae recoltées principalement dans la region de Dakar. Bulletin de

ULFA.N., Série A, 22: 788-852.

Euzet, L. & Radujkovic, B.M. 1989. Kotorella pronosoma (Stossich, 1901) n. gen., n.

comb., type des Kotorellidae, nouvelle famille de Trypanorhyncha (Cestoda), para-

site intestinal de Dasyatis pastinaca (L., 1758). Annales de Parasitologie Humaine

et Comparée 64: 420-425.

Jones, M. & Beveridge, I. 1998. Nybelinia queenslandensis sp. nov. (Cestoda:

Trypanorhyncha) parasitic in Carcharhinus melanopterus, from Australia, with

observation on the fine structure of the scolex including the rhyncheal system. Folia

Parasitologica 45: 295-311.

Khurshid, N. & Bilqees, F.M. 1988. Nybelinia karachii new species from the fish

Cybium guttatum of Karachi coast. Pakistan Journal of Zoology 20: 239-242.

Palm, H.W. 1995. Untersuchungen zur Systematik von Riisselbandwiirmern (Cestoda:

Trypanorhyncha) aus atlantischen Fischen. Berichte aus dem Institut fiir Meereskunde

Kiel 275: 1-238.

1997. An alternative classification of trypanorhynch cestodes considering the

tentacular armature as being of limited importance. Systematic Parasitology 37: 8\1—

92.

——, Moller, H. & Petersen, F. 1993. Otobothrium penetrans (Cestoda;

Trypanorhyncha) in the flesh of belonid fish from Philippine waters. /nternational

Journal for Parasitology 23: 749-755.

, Walter, T., Schwerdtfeger, G. & Reimer, L.W. 1997. Nybelinia Poche, 1926

(Cestoda: Trypanorhyncha) from the Mozambique coast with description of N.

beveridgei sp. nov. and systematic considerations on the genus. South African

Journal of Marine Science 18: 273-285.

Pintner, T. 1913. Vorarbeiten zu einer Monographie der Tetrarhynchoideen.

Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften Wien, mathematisch-

naturwissenschaftliche Klasse, Abteilung 1, 122: 171-253.

—— 1930. Wenigbekanntes und Unbekanntes von Riisselbandwiirmern.

Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften Wien, mathematisch-

naturwissenschaftlichen Klasse, Abteilung 1, 139: 445-537.

Shipley, A.E. & Hornell, J. 1906. Report on the cestode and nematode parasites from

the marine fishes of Ceylon. Report to the Government of Ceylon on the Pearl Oyster

Fisheries of the Gulf of Manaar, Part 5: 43-96.

Southwell, T. 1924. Notes on some tetrarhynchid parasite from Ceylon marine fishes.

Annales of Tropical Medicine and Parasitology 18: 459-491.

1929a. A monograph on cestodes of the order Trypanorhyncha from Ceylon and

India, Part 1. Ceylon Journal of Science, Section B, 15: 169-317.

1929b. On the classification of cestodes. Ceylon Journal of Science 15: 49-72.

1930. The fauna of British India including Ceylon and Burma. Cestoda, Vol. 1.

Stephenson, J. (ed) Today & Tomorrows Printers and Publishers, New Delhi, 391 pp.

Vijayalakshmi, C., Vijayalakshmi, J. & Gangadharam T. 1996. Some trypanorhynch

cestodes from the shark Scoliodon palasorrah (Cuvier) with the description of a new

species, Tentacularia scoliodoni. Rivista di Parassitologia 13 (57): 83-89.

Yang Wenchuan, Lin Yuguang, Liu Gencheng & Peng Wenfeng 1995. Five species

of Trypanorhyncha from marine fishes in Xiamen, Fujian, China. Journal of Xiamen

University (Natural Science) 34: 811-817.

Yamaguti, S. 1952. Studies on the helminth fauna of Japan. Part 49. Cestodes of fishes,

Il. Acta Medicinae Okayama 8: 1-76.

Bull. nat. Hist. Mus. Lond. (Zool.) 65(2): 133-153 Issued 25 November 1999

Nybelinia Poche, 1926, Heteronybelinia gen.

nov. and Mixonybelinia gen. nov. (Cestoda,

Trypanorhyncha) in the collections of The

Natural History Museum, London

HARRY W. PALM

Marine Pathology Group, Department of Fisheries Biology, Institut fiir Meereskunde an der Universitat Kiel,

Diisternbrooker Weg 20, D-24105 Kiel, Germany

SYNOPSIS. With a total of 43 adequately described species, the cosmopolitan genus Nybelinia is the most species-rich genus

within the order Trypanorhyncha. As an initial part of a revision of the genus, the present study was carried out to examine

unidentified and identified Nybelinia specimens deposited at The Natural History Museum London. A total of 17 different species

was found, four new species are described and 2 new genera, Heteronybelinia gen. nov. and Mixonybelinia gen. nov., are erected:

Nybelinia aequidentata (Shipley & Hornell, 1906); N. africana Dollfus, 1960; N. jayapaulazariahi Reimer, 1980; N. lingualis

(Cuvier, 1817); N. riseri Dollfus, 1960; N. sakanariae sp. nov.; N. schmidti sp. nov.; N. scoliodoni (Vijayalakshmi, Vijayalakshmi

& Gangadharam, 1996) comb. nov.; Nybelinia sp.; Heteronybelinia elongata (Shah & Bilgees, 1979) comb. nov.; H. estigmena

(Dollfus, 1960) comb. nov.; H. heteromorphi sp. nov.; H. minima sp. noy.; H. robusta (Linton, 1890) comb. nov.; H. yamagutii

(Dollfus, 1960) comb. noy.; Mixonybelinia beveridgei (Palm, Walter, Schwerdtfeger & Reimer, 1997) comb. noy. and M.

southwelli (Palm & Walter, 1999) comb. nov.. Tentacularia scoliodoniis transferred to the genus Nybelinia. Nine new locality and

15 new host records were established. The adults of Heteronybelinia estigmena and H. yamagutii are reported for the first time.

It is proposed that the morphological variation within the different species is much higher than considered in the recent literature.

Many species within the genus have a world-wide distribution pattern and a low host specificity, both in their fish second

intermediate/paratenic hosts and in their final hosts.

INTRODUCTION

Trypanorhynchs are cosmopolitan marine cestodes and mature in

the stomach or the spiral valve of marine elasmobranchs, while their

postlarvae are parasitic in teleosts and invertebrates, with the first

intermediate hosts being crustaceans (Palm, 1997a, Sakanari &

Moser, 1989). Within the order Trypanorhyncha, the genus Nybelinia

Poche, 1926 is particularly difficult to study. Palm er al. (1997)

listed 43 adequately described species while leaving 4 as species of

uncertain status. Jones & Beveridge (1998) added a further species,

N. queenslandensis, and Palm & Walter (1999) described N.

southwelli, and synonymised Nybelinia dakari Dollfus, 1960 and N.

herdmani (Shipley & Hornell, 1906) with N. perideraeus (Shipley &

Hornell, 1906) and Kotorella pronosoma (Stossich, 1901) respec-

tively. Thus, with a total of 43 adequately described species, the

genus Nybelinia is the most species-rich genus within the order

Trypanorhyncha.

In contrast our knowledge of their biology is poor. The first

intermediate hosts are unknown and the occurrence of postlarvae in

marine plankton (Dollfus, 1974) is enigmatic. Postlarvae of these

robust worms are found in unusual sites such as the human palatine

tonsil (Kikuchi et al., 1981) as well as in anadromous Lampetra

Japonica, 1000-3000 km away from the sea in the Amur river

(Shulman, 1957). Additionally, members of the genus Nybelinia

infest the fish flesh (Oshmarin et al., 1961, Palm, 1997b), and

parasitic infestation of the musculature of commercially important

fish species causes heavy losses to the fish processing industry

(Arthur et al., 1982, Deardorff et al., 1984).

One of the biggest problems for taxonomic work within the genus

Nybelinia, apart from incomplete original descriptions, remains the

lack of information on material deposited in museum collections.

The genus has not been revised since 1942, and due to the morpho-

logical similarity of several species, many Nybelinia specimens

found have not been identified to species level, and consequently

have been deposited as Nybelinia sp. Additionally, several species

descriptions are based on single specimens.

The present study was carried out to examine unidentified species

of Nybelinia deposited at The Natural History Museum, London.

Measurements and drawings of most specimens are given as verifi-

cation of the identifications made. Beside the establishment of new

host and locality records, species identifications provide further

insight into the zoogeographical distribution. The comparison of the

scolex measurements with those from original descriptions allows

comments to be made on the level of intraspecific morphological

variation of some Nybelinia species, data which are necessary for

further taxonomic studies within the genus. The description of adult

specimens allows comparative investigations on strobilar morphol-

ogy within the genus.

MATERIAL AND METHODS

Standard measurements and drawings of the scoleces of Nybelinia

specimens deposited in the Parasitic Worms Division, The Natural

History Museum, London (BMNH), were made using a Leitz Wetzlar

Dialux 20 microscope with an ocular micrometer. Special attention

was given to unidentified specimens deposited simply as Nybelinia

sp., while other deposited and identified material was also exam-

134

ined. As additional material, slides from the Natural History Mu-

seum, Vienna (NHMV No. 2111) and from the U.S. National

Parasite Collection, Beltsville (USNPC No. 7727 (M130-6)) were

borrowed. Similarly, deposited Nybelinia species were studied in

the Muséum National d“Histoire Naturelle, Paris (MNHN Paris), for

comparison.

The following measurements were made: Scolex length (SL),

scolex width at level of pars bothridialis (SW), pars bothridialis

(pbo), pars vaginalis (pv), pars bulbosa (pb), pars postbulbosa (ppb),

velum (vel), appendix (app), bulb length (BL), bulb width (BW),

bulb ratio (BR), proportions of pbo/pv/pb (SP), tentacle width (TW),

and tentacle sheath width (TSW). If possible, the tentacle length was

estimated. Additionally, the tentacular armature was described as

follows: armature homeomorphous or heteromorphous, hooks per

half spiral row (hsr), total hook length (L) and the total length of the

base of the hooks (B). The abbreviation nm (not measured) indicates

that no measurement was taken.

All measurements are given in micrometers unless otherwise

indicated. Specimens belonging to the same species from different

hosts or localities were measured in the same order as the specimens

are listed under Material examined. If more than two measurements

were taken, the mean is given with the range in parentheses, unless

otherwise indicated. Illustrations are provided if useful for future

identification of the species; otherwise the reader is referred to

illustrations of other authors. The classification follows that of Palm

(1995, 1997a) and the orientation of the tentacular surfaces follows

that of Campbell & Beveridge (1994).

RESULTS

A total of 17 species was identified, and 4 new species are described.

Nine new locality and 15 new host records were established. The

information on the single specimens measured with comments on

their taxonomy and distribution are given below.

Superfamily TENTACULARIOIDEA Poche, 1926

Family TENTACULARIIDAE Poche, 1926

Genus NYBELINIA Poche, 1926

1. Nybelinia aequidentata (Shipley & Hornell, 1906)

(Figs 1-2)

MATERIAL EXAMINED. BMNH 1992.7.1.193-196, A. Roy leg., 1

postlarva from Lepturacanthus savala, Sugar Island, Bay of Bengal.

DESCRIPTION. The type material of N. aequidentata, which is

deposited at the Natural History Museum, Vienna, was re-described

by Pintner (1927). The scolex and tentacular armature of the present

specimen is given in Figs 1-2. Measurements: SL=3400; SW=1700;

pbo=1510; pv=1890; pb=813; ppb=57; vel=530; app=585; BL=780

(756-813); BW=237 (227-265); BR=3.3:1; SP=1.9:2.3:1. TW

metabasal=54—58, TW apical=46—51. A basal tentacular swelling is

absent. The tentacle sheaths are straight; TSW=33-38. Prebulbar

organs are absent, muscular rings around the basal part of the

tentacle sheaths are present. The retractor muscles originate in the

basal part of the bulbs.

The armature is homeoacanthous, homeomorphous, and a charac-

teristic basal armature is absent. The massive hooks of the metabasal

armature are similar in shape (Fig. 2), diminishing in size from the

6"" row towards the basal part of the tentacle. The size of the hooks

also diminish slightly towards the apical end of the tentacles. The

H.W. PALM

hook size in the metabasal armature was L=33—38, B=13—17; hsr=8.

REMARKS. The present specimen is similar to the type material,

having a large scolex and pbo and slender tentacular hooks with a

long shaft and a rounded base. The tentacular hooks of the type

specimen are similarly shaped along the tentacle and diminish in

size towards the tip and at the base (compare with Pintner 1927, p.

562). Additionally, both specimens were found in the same region,

off the Indian coast. However, the present specimen also shows

some differences to those described by Shipley & Hornell (1906)

and Pintner (1927). The scolex measurements of the type (4500—

5000, SW=2000) as well as the hook sizes (L=up to 48) are larger.

Similarly, the scolex proportions of the two specimens differ (type:

BR=4.3:1 and SP=1:1.7:1). In both cases, the descriptions are based

on a single specimen only, and no data on the morphological

variability within N. aequidentata are available.

The present specimen belongs to subgroup IAa of Palm et al.

(1997) and due to the characteristically shaped slender hooks with a

rounded base, slender shaft and strongly re-curved tip, it has simi-

larities with N. edwinlintoni and N. goreensis. N. edwinlintoni is

smaller, has a different bulb ratio (2.5:1) and scolex proportion

(2.4:1.6:1) as well as a larger TW, TSW and smaller (L=18—20,

B=10) hooks (Dollfus, 1960). NV. goreensis is also smaller (SL=1235—

1325), has a slightly different bulb proportion (2.5—3:1), a larger

TW, TSW and smaller hooks. In addition, Dollfus (1960) remarked

on the uniformity of the hooks. Two species with a similar tentacular

armature, N. anantaramanorum and N. syngenes, were placed in

subgroup [Ab by Palm et al., 1997, with hooks of similar size in the

basal and metabasal part of the tentacles. N. anantaramanorum from

the Gulf of Bengal differs in having smaller hooks and a smaller

scolex (Reimer, 1980). However, there is a close relationship be-

tween N. aequidentata and N. anantaramanorum. N. syngenes

resembles the present specimen in having similar tentacular hooks.

However, it clearly differs by having a distinctly smaller scolex and

larger hooks (L=68; Pintner, 1929, Dollfus, 1942). Thus, the present

specimen is identified as NV. aequidentata, and represents a new host

record. However, the similarities between these species have to be

kept in mind.

2. Nybelinia africana Dollfus, 1960 (Fig. 3)

MATERIAL EXAMINED. BMNH 1982.4.6.37-45, R. van der Elst

leg., 11.05.1984, 1 adult from the lower gut/upper intestine of

Carcharhinus obscurus, South Africa; BMNH 1985.11.8.63-64, R.

van der Elst Jeg., 11.5.1984, 1 adult from Carcharhinus leucas,

Richards Bay, South Africa. Other material: BMNH 1982.4.6.18—

22, R. Bray leg., from the lower stomach of Carcharhinus obscurus,

Durban, South Africa; BMNH 1985.11.8.53-54, R. van der Elst

leg., 2.4.81, from the stomach of Carcharhinas leucas; BMNH

1985.11.8.55—56, R. Bray leg., from the stomach of Mustelus canis

(=M. canis or M. queketti), stomach, Durban, Natal.

DESCRIPTION. Nybelinia africana was described in detail by

Dollfus (1960, see figures 9-19) and Palm et. al. (1997). Measure-

ments: SL=536, 440; SW=420, 485; pbo=327, 337; pv=205, 122;

pb=178, 150; vel=210, 164; BL= 174 (168-178), 133 (120-150);

BW=73 (70-75), 70 (60-78); BR=2.4:1, 1.9:1, SP=1.8:1.1:1,

2.2:0.8:1; Short tentacles, about 200 long, with TW basal=28, 27;

TW metabasal 23, 24; The tentacle sheaths are sinuous or spirally

coiled, TSW=18—23, 17—20. The characteristic tentacular armature

is homeomorphous with a basal armature of about 6 rows with rose-

thorn-shaped hooks. The metabasal armature consists of slender

hooks witha strongly re-curved tip (L=13.5—15.2, 12.5-14.8; B=5.6—

7.2, 4.0-5.5). The tentacular hooks of the basal armature were

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

‘

Fig. 1 Nybelinia aequidentata isolated from Lepturacanthus savala.

Scolex. Scale bar=500 um.

rose-thorn shaped (L=9.6-12.0, 8.8-12.0; B=7.2-8.8, 7.2-8.8);

hsr=7-8.

The strobila is acraspedote, with about 240 segments, last proglot-

tid with rounded proximal end. The first 70 proglottids are very short

(10-50 long x 370-530 wide), the next enlarge in size towards 400—

500 x 940-1030. The last 20 proglottids are a bit wider than long

1050-1200 x 1250-1450. In mature proglottids (Fig. 3), genital

atrium ventro-submarginal, in anterior half of the segment; genital

pores alternate irregularly. Cirrus sac elongate and slender, 80 x 450

in size, directed anteromedially, sac thin-walled; cirrus unarmed and

coiled within sac, internal and external seminal vesicle not seen; vas

deferens coils medially to mid-line, then posteriorly towards genital

complex. Testes of different shape, often ovoid, 70-95 in diameter

(55-70 in proglottids 71-160), arranged in a single layer; testes

number 80-90 per proglottis, encircle female genital complex and

occupy entire medulla except for region of female genital complex

and anterior of it. Ovary centrally, follicular, x-shaped with 2 major

branches, each 95 x 160. Uterine ducts coiled before they enter the

sacciform uterus. Vitelline follicles 25-35 in diameter.

REMARKS. Dollfus (1960) described larvae of N. africana from

the body cavity of Galeoides polydactylus, Mullus barbatus, Pagellus

sp. Serranus cabrilla, and Trigla sp.. The 3 scoleces measured by

Dollfus were variable in size, ranging for example between 750-

1100 (SL), 397-540 (pbo) and 19-35 (TW). The BR and SP were

between 2.6:1—3.4:1 and 2.1:0.9:1—2.3:1.4:1 respectively and the

| hook size in the metabasal armature was between 14-17. The

135

Fig. 2 N. aequidentata. Homeomorphous metabasal armature. Scale

bar=25 um.

measurements for the present specimens were smaller and only the

SP of the specimen from Carcharhinus leucas directly corresponds

to specimen in tube 465 described by Dollfus (1960). However, the

similar form and size of the basal and metabasal hooks together

with a similar TW lead to the identification proposed. Palm et al.

(1997) reported specimens of N. africana from the Mozambique

coast which were larger in scolex and hook sizes than the above

material. However, the form of the hooks along the tentacle as well

as the BR, SP and TW were similar to those described by Dollfus

(1960). Thus, it seems that N. africana has a variable scolex size,

and, depending on this, a different hook size. However, the charac-

teristic hook forms along the tentacle remain the same. Palm &

Walter (1999) recognised adults of N. africana from Carcharhinus

melanopterus from the Gulf of Suez, Egypt (named as N.

perideraeus in Dollfus, 1942) on bases of the scolex size and the

tentacular armature, and the present description of adult NV. africana

supports this synonymy. The strobila characters of the present

specimens correspond with that of Dollfus’s description in a similar

size and shape of the first (10-50 x 370-530 vs 11 x 290) and last

(1050-1200 x 1250-1450, a bit wider than long vs 1100 x 900, a

bit longer than wide) proglottids, the follicular ovary, and similar

sized vitellaria (25-35 vs 26-31). The present study records speci-

mens from two further carcharhinid shark species and from Mustelus

canis from South Africa. They represent new host and locality

records, which indicates a circum-African distribution and a low

host specificity of adult N. africana, as was earlier proposed for the

postlarvae by Palm et al. (1997).

136 H.W. PALM

Fig.3 WN. africana. Mature segment. Scale bar=60 um.

Fig.5 N. jayapaulazariahi. Homeomorphous metabasal armature with

Fig. 4 Nybelinia jayapaulazariahi from Harpodon nehereus. Scolex. slender hooks, metabasal hook as given in Reimer (1980), figure 4

Scale bar=50um. (arrow). Scale bar=10 um.

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

3. Nybelinia jayapaulazariahi Reimer, 1980 (Figs 4-5)

MATERIAL EXAMINED. BMNH 1980.12.2.1, A. Roy leg., 14.9.79,

1 postlarva from Harpodon nehereus, Houghly estuary, India (Figs

4-5).

DESCRIPTION. Measurements: SL=530; SW=326; pbo=298;

pv=285; pb=165; app=114; vel=96; BL=157 (150-165); BW=54;

BR=2.9:1: SP=1.8:1.7:1; TW=16-18.5; TSW=12.5—15.5; a basal

tentacle swelling is absent; the tentacle sheaths are straight; Prebulbar

organs and muscular rings around the basal part of the tentacle

sheaths are absent. The retractor muscles originate at the basal part

of the bulbs.

The tentacular armature is homeoacanthous, homeomorphous,

and a characteristic basal armature is absent. The size of the slender,

regularly curved hooks increases slightly towards the metabasal part

of the tentacle; L=9.6—11.2; B=5.6—7.2 (metabasal) and L=5.6—7.2;

B=5.6—7.2 (basal); hsr=6.

REMARKS. ‘The present specimen from Harpodon nehereus corre-

sponds closely with that of the original description by Reimer

(1980) from Cynoglossus sp.. Beside a similar scolex form (Fig. 7 in

Reimer, 1980) and similar scolex and bulb ratios (SP 1.9:—:1 and BR

3:1), the hook size is identical and the hook form (as given in

Reimer, 1980, Fig. 8) resembles that given in Fig. 5 (see arrow). The

hook form with its slender, regularly curved shaft is distinct from the

robust rose-thorn shaped hooks of many other Nybelinia species.

The values of the TW extracted from Fig. 7 of Reimer are slightly

higher (ca. 20-25 um) than those of the present specimen. Both

specimens were found in the same part of the Indian Ocean, Houghly

estuary, India, and the Bay of Bengal, India. Harpodon nehereus

represents a new host for Nybelinia jayapaulazariahi.

4. Nybelinia lingualis (Cuvier, 1817) (Figs 6-9)

MATERIAL EXAMINED. BMNH 1987.3.2.19, R. Bray leg., 1

postlarva from the gut of Torquigener pleurogramma, Adelaide,

South Australia; BMNH 1987.4.23.11—12, R. Bray leg., 03.12.1986,

2 postlarvae from the branchial chamber of Arnoglossus imperialis,

Cirolana 76—78 m, 49°50'S"N, 3°44'3"W; BMNH 1987.4.23.18-32,

R. Bray leg., 03.12.1996, 1 postlarva from the intestinal wall of

Pagusa lascaris, Cirolana, English Channel, 49°50'S"N, 3°44'3"W,

76-78 m.

DESCRIPTION. WNybelinia lingualis was described in detail by

Dollfus (1942). The scolex of the specimen from T: pleurogramma

is shown in Fig. 6. Measurements: SL=1606, 1720, 1700, 2040;

SW=718, 982, 907, 1172; pbo=700, 1096, 1096, 1172; pv=642, 907,

907, 1171; pb=397, 321, 298, 341; ppb=75, 0, 0, 10; app=490, 510,

491, nm; BL=365 (326-397), 313 (303-322), 292 (289-294), 341;

BW=138 (130-140), 128 (117-140), 114 (112-117), nm; BR=2.6:1,

Pale 2.6:1, nm; SP=1-8:1.6:1, 3:4:2.8:1, 3.7:3:1, 3.4:3.4:1. The

tentacles are long and slender and diminish in diameter towards the

tip; TW basal=39, 42, 46, 46, TW metabasal=32, 33, 33, 38; TW

distal=24, nm, nm, nm. A basal tentacular swelling is not present.

The tentacle sheaths are coiled in 1 to 2 spirals near the bulbs; TSW=

| 36,46, 42, 40. Prebulbar organs and muscular rings around the basal

| part of the tentacle sheaths are absent. The retractor muscles origi-

| nate in the basal part of the bulbs.

The armature is homeoacanthous, homeomorphous, and a charac-

| teristic basal armature is present (Figs 7-9). The tentacular hook

, form changes towards the apical part of the tentacle from compact,

rounded rose-thorn (Fig. 7), lacking an posterior extension of the

| basal plate, to more slender rose-thorn shaped hooks (Figs 8-9). The

| hooks in the basal part of the tentacle are smaller (L=11.0-13.0,

137

11.6-13.6, 11.6-13.6, 11.6-13.6; B=9.3-11.2, 7.2-9.6, 7.2-9.6,

7.2—9.6) than in the metabasal armature (L=14.5—16.7, 16.0-18.4,

16.0-18.4, 16.0-18.4; B=9.3-13.0, 12.0-13.5, 12.0-13.5, 12.0-

13.5). The number of hooks per half spiral diminish towards the

apical part of the tentacle; hsr=6—7 (basal), hsr=5—6 (apical).

REMARKS. The present specimens correspond with those described

by Dollfus (1942). Although the scolex measurements as well as

hook sizes are smaller than those given by Dollfus (1942), the scolex

form as well as the form and arrangement of the tentacular hooks

correspond with drawings of N. lingualis found in Sepia filliouxi, S.

officinalis and Mullus barbatus (see Dollfus, 1942, Figs 88-91).

According to Dollfus (1942), the bulbs are typically short (about

300-400 um long), with a BR of about 2.2—2.5:1. Additionally,

Dollfus (1942) demonstrated a high degree of morphological vari-

ability within the species with a scolex size between 1.2—-3.2 mm. As

with Tentacularia coryphaenae, Nybelinia lingualis has a wide

zoogeographical distribution and a low host specificity. The present

findings with the exception of specimens in Pagusa lascaris are new

host records and extend the known range of distribution for the

species to Australian waters. Palm (1995) examined specimens of

the same species (BMNH 1987.4.23.18-32 from P. lascaris) and

tentatively identified them as N. lingualis. The present finding

confirms this identification. Thus, the surface morphology of

Nybelinia lingualis with filiform microtriches on the distal bothridial

surface and hook-like microtriches on the bothridial borders corre-

sponds to those as described for Tentacularia coryphaenae, N.

alloiotica, N. edwinlintoni, N. queenslandensis and N. c.f.

senegalensis (Palm, 1995, Jones & Beveridge, 1998).

5. Nybelinia riseri Dollfus, 1960 (Figs 10-11)

MATERIAL EXAMINED. BMNH 1985.11.8.65, G. Ross leg.,

30.11.1979, 3 postlarvae from Trachyurus felicipes (Figs 10-11),

stomach wall, East Cape, South Africa.

DESCRIPTION. Measurements: SL=1455 (1380-1587); SW

(pbo)=580 (510-680); SW (pv)=400 (300-454); pbo=630 (585-

662); py=636 (567-700); pb=294 (280-303); ppb=204 (151-233);

app=331 (312-360); BL=284 (270-303); BW=100 (84-117);

BR=2.8:1 (2.7:1—3.2:1); SP=2.1:2.2:1. The tentacles are not com-

pletely evaginated, a basal tentacle swelling is absent. TW=51-S6.

The tentacle sheaths are straight and the TSW without invaginated

tentacles is nearly half as small (TSW=23-—28) than with invaginated

tentacles (TSW=42-46). Prebulbar organs and muscular rings around

the basal part of the tentacle sheaths are absent. The retractor

muscles originate in the basal part of the bulbs.

The tentacular armature is homeoacanthous, homeomorphous,

and consists of compact rose-thorn-shaped tentacular hooks (upper

basal armature, L=14—19; B=12—15). The hooks are in tight spirals

(Fig. 11) and the hooks diminish in size towards the basal part of the

tentacles (L=12—14; B=9-12); hsr=6—7.

REMARKS. Only two species, WN. riseri and N. lingualis, have been

described as having a similar champion-shaped scolex form as well

as a homeoacanthous, homeomorphous tentacular armature such as

described for the present specimens. N. riseri is characterised by the

champion-shaped scolex (see Dollfus, 1960), however, the hooks in

the basal part of the tentacle (L=11—12, B=11—12) are smaller than

observed for the present specimens. WN. lingualis corresponds with a

similar basal armature (see above) and scolex proportions as de-

scribed for specimens of N. lingualis taken from Trachyurus felicipes

(see Dollfus, 1942). However, the general scolex form with the

small banana-shaped bulbs of Nybelinia lingualis (see Dollfus,

1942) clearly differs to the present specimens. Thus, they are

138

Fig.6 Nybelinia lingualis from Torquigener pleurogramma. Scolex.

Scale bar=100 um.

identified as belonging to Nybelinia riseri on basis of the character-

istic scolex form. It has to be kept in mind that the tentacles of the

present specimens were not completely evaginated. The present

finding represents a new host and locality record.

6. Nybelinia sakanariae sp. nov. (Figs 12-13)

MATERIALEXAMINED. Holotype and paratype, BMNH 1976.1.7.9,

Hecht /eg., 2 postlarvae from the stomach of Xiphiurus capensis,

South Africa. Additional material: BMNH 1976.1.7.7—8, Hecht

leg., 1 postlarva from the testes of Trachurus trachurus, Algoa Bay,

South Africa.

DESCRIPTION (Fig. 12). Measurements: SL=1512, 1507; SW=775,

747; pbo=700, 700; pv=680, 647; pb=397, 386; ppb=94, 100;

vel=360, 335; app=360, 335; BL=387, 335; BW=116, 113; BR=3.3:1,

3:1; SP=1.8:1.7:1, 1.8:1.7:1. A basal tentacle swelling is absent.

TW=51-56. The tentacle sheaths are short, little coiled with a

TSW=5 1-56. Prebulbar organs and muscular rings around the basal

part of the tentacle sheaths are absent. The retractor muscles origi-

nate in the basal part of the bulbs.

The armature is homeoacanthous, homeomorphous, and con-

sists of compact rose-thorn-shaped tentacular hooks (Fig. 13);

upper basal and metabasal armature, L=16—22; B=13.5-17.0).

Characteristic basal hooks are absent. However, the hooks dimin-

ish in size towards the basal part of the tentacles (L=12-14;

B=11—13); hsr=6—7.

H.W. PALM

Fig. 7 N. lingualis from T. pleurogramma. Homeomorphous basal

armature consisting of rounded hooks without anterior extension of the

basal plate. Scale bar=10 um.

ADDITIONAL MATERIAL. SL=3270; SW=1020; pbo=1134;

pv=1172; pb=605; ppb=567; vel=756; app=740; BL=580; BW=147;

BR=3.9:1; SP=2:2:1. The tentacles are short and a basal tentacle

swelling is absent. TW=56-61. The tentacle sheaths are straight,

prebulbar organs and muscular rings around the basal part of the

tentacle sheaths are absent. The retractor muscles originate in the

basal part of the bulbs. Metabasal armature, L=21—23; B=15-17. A

characteristic basal armature is absent, the hooks diminish in size

towards the basal part of the tentacles (L=11—13; B=11—13); hsr=7.

REMARKS. The present specimens correspond with Nybelinia

strongyla in having a similar scolex, SP, BR, TW and a similar hook

size. However, the scolex size is smaller than indicated by Dollfus

(1960) and the type material deposited at the MNHN Paris revealed

a different hook shape. The material also resembles N. riseri as

described by Dollfus (1960) with corresponding values of SL, BL,

BW, BR, ppb and a similar basal hook size. The hook form of N.

riseri appears massive with a broad base, and hooks are tightly

packed along the tentacle. However, the hooks of the armature of N.

riseri of about 11-12 um are distinctly smaller than in the present

specimens, and the characteristic scolex form of N. riseri (see

above) was not present. The specimens also have some similarities

with Nybelinia queenslandensis Jones & Beveridge, 1998 with a

similar hook form. However, the specimens clearly differ in having

the hooks more tightly spaced and different values for SL, TW, BR

and SP. Thus, the present specimens represent a new species,

Nybelinia sakanariae sp. nov. Interestingly, the additional material

obtained from another host had a much larger scolex than observed

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

Fig. 8 WN. lingualis from T. pleurogramma. Homeomorphous metabasal

armature. Scale bar=10 um.

Fig.9 NWN. lingualis from T. plearogramma. Homeomorphous apical

armature. Scale bar=10 um.

Fig. 10 Nybelinia riseri. Scolex from Trachyurus felicipes. Scale

bar=100 um.

139

for the type material but the same kind of tentacular armature. The

size should be considered as a case of intraspecific morphological

variability within the species.

ETYMOLOGY. ‘The new species is named after J.A. Sakanari, in

honour to her work on the life cycle of trypanorhynch cestodes.

7. Nybelinia schmidti sp. nov. (Figs 14-15)

MATERIAL EXAMINED. Holotype BMNH 1982.12.3.1, G. Ross

leg., 23.07.1978, 1 adult from the stomach of Jsurus glaucus, Algoa

Bay, South Africa.

DESCRIPTION (Figs 14-15). Measurements: SL=1172; SW=832;

pbo=794; pv=473; pb=289; ppb= 46; vel=373; BL=289; BW=104

(94-117); BR=2.8:1; SP=2.7:2.6:1. The tentacles are long and

slender; TW=18.4—23.5; and a basal swelling is absent. The tentacle

sheaths are spirally coiled; TSW=46-51. Prebulbar organs and

muscular rings around the basal part of the tentacle sheaths are

absent. The retractor muscles originate at the basal part of the bulbs.

The tentacular armature is homeoacanthous, homeomorphous,

and a characteristic basal armature is absent. The massive and rose-

thorn shaped hooks increase in size towards the metabasal part of the

tentacle, L=13.5—15.0; B=11.7—13.3 (metabasal) and L=9.0—10.3;

B=8.3-9.0 (basal); the hooks in the metabasal part of the tentacle are

slightly more slender than in the basal part; hsr=5-6.

The strobilar is acraspedote, with about 240 very large segments,

wider than long. The proglottids in the anterior part of strobila are

140-155 long x 1400-1540 wide, the final proglottids enlarge in

size towards 450-560 x 2800-3080. In mature proglottids, genital

Fig. 11 WN. riseri. Homeomorphous basal armature consisting of rounded

hooks without anterior extension of the basal plate. Scale bar=15 um.

140

Fig. 12 Nybelinia sakanariae sp. noy. Scolex from Xiphiurus capensis.

Scale bar=150 pm.

atrium ventro-submarginal, in anterior third of the segment; genital

pores alternate irregularly. Cirrus sac elongate and slender, in final

segments 55-90 x 1200-1330 in size, directed anteromedially,

parallel to anterior end of the proglottids; sac thin-walled; cirrus

unarmed and coiled within sac. Other internal structures not seen.

REMARKS. The present specimen belongs to subgroup [Aa of

Palm et al. (1997) and resembles, with a rose-thorn-shaped basal and

metabasal tentacular armature, N. anthicosum, N. palliata, N.

strongyla, N. riseri, N. sphyrnae and N. thyrsites. A comparison with

the type material of N. anthicosum and N. palliata, deposited at the

U.S. National Parasite Collection, Beltsville, revealed differences in

oncotaxy. NV. strongyla has a much larger TW=55 and SL=2300 and

larger hooks, and WN. riseri has smaller hooks together with a larger

TW and a different scolex form (Dollfus, 1960). N..sphyrnae and N.

thyrsites also differ in hook and scolex form/size (see Beveridge &

Campbell, 1996). Thus, the present specimen represents a new

species, Nybelinia schmidti sp. nov.

ETYMOLOGY.

D. Schmidt.

The new species is named after the parasitologist G.

H.W. PALM

Fig. 13 N. sakanariae sp. nov. from X. capensis Homeomorphous basal

and metabasal armature. Scale bar=20 um.

8. Nybelinia scoliodoni (Vijayalakshmi, Vijayalakshmi &

Gangadharam, 1996) comb. nov. (Jentacularia scoliodoni)

(Figs 16-17)

MATERIAL EXAMINED. BMNH 1976.11.5.42-43, R. van der Elst

leg., 1 adult from the gut of Carcharhinus limbatus, South Africa.

Additional material: NHMV 2111, A.E. Shipley /Jeg., 1 adult from

Glyphis gangeticus (=Carcharhinus gangeticus), India.

DESCRIPTION (Fig. 16-17). Measurements: SL=667; SW=320;

pbo=267; pv=227; pb=144; vel=267; BL=133 (125-144); BW=59

(56-64); BR=2.2:1; SP=1.9:1.6:1. The tentacles are 173-200 long

and a basal tentacle swelling is absent. The TW varies along the

tentacle; at the most proximal part of the basal armature, TW=14—

17; at the basal armature, TW=23-25; at the apical armature,

TW=12-13. The tentacle sheaths are straight (TSW=18-21),

prebulbar organs and muscular rings around the basal part of the

tentacle sheaths are absent. The retractor muscles originate in the

basal part of the bulbs.

The metabasal armature is homeoacanthous, homeomorphous,

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

Fig. 14 Nybelinia schmidti sp. nov. Scolex from Jsurus glaucus. Scale

bar=100 um.

and a distinctive basal armature is present (Fig. 17). The basal

armature consists of about 11 rows with compact rose-thorn-shaped

hooks, increasing in size (row 1—5: L=3.5—5.6, B=3.5—-4.9, and row

6-11: L=7-9.8, B=5.6-8.4). From rows 12-14, the hook form

changes to long, spiniform metabasal hooks (L=22—26) with a small

base (B=7.7—10.5); hsr basal=6—7, hsr metabasal=4—5.

No complete strobila is present. The first acraspedote proglottids

are wider than long (330 x 50) and slightly increasing in size (490 x

205). Other internal structures were not seen.

REMARKS. Palm & Walter (1999) considered Nybelinia (Tentacul-

aria) scoliodoni (Vijayalakshmi, Vijayalakshmi & Gangadharam,

1996) as a species of uncertain status due to an uncomplete original

description and a strong similarity to Nybelinia indica Chandra,

1986. However, the present specimen confirms the validity of

Tentacularia scoliodoni, and assigns the species to the genus

Nybelinia Poche, 1926. Though the scolex measurements of the

present specimen are smaller and the scolex and bulb ratios show

differences to those given in the original description, the tentacular

armature corresponds in detail with N. scoliodoni. The drastic

change in form from rose-thorn shaped basal to spiniform metabasal

hooks, with a size between L=8-—11 in the basal and L=30, B=3 in the

metabasal armature as given by Vijayalakshmi er al. (1996), is

unique within the genus. As with the scolex size, the hooks of the

present specimen are slightly smaller than those of the original

description. However, Vijayalakshmi et al. (1996, figure 8) demon-

strated minute hooks on the basal part of the tentacle, similar to those

in rows 1—5 of the present specimen, and also indicated the charac-

teristic change in TW along the tentacles (figure 7). The known

range of distribution is extended to South Africa, and Carcharhinus

141

Fig. 15 N. schmidti sp. nov. Homeomorphous basal and metabasal

armature. Scale bar=10 um.

limbatus is a new host for N. scoliodoni. Under the co-type material

of Nybelinia perideraeus (Shipley & Hornell, 1906), slide No. 12f,

an adult NV. scoliodoni with an uncomplete strobila was found. The

scolex size and tentacular armature corresponds to the material

deposited at the BMNH. Thus, Glyphis gangeticus represents a new

host for N. scoliodoni, and this finding supports its occurrence in

Indian Ocean waters.

N. scoliodonihas similarities with N. indica Chandra, 1986, which

was also described from the Indian Ocean. N. indica differs due to its

larger size, a large ppb, a larger TW in the basal part of the tentacle and

a more gradual change in hook form along the tentacles (Chandra,

1986). In contrast to this, the form of the hooks as well as their size

show similarities to both N. scoliodoni and the present specimen. The

real identity of N. indica and a possible synonymy with N. scoliodoni

cannot be decided until a re-examination of the type material is

undertaken. Therefore, both species remain valid, and on the basis of

the above described characters, the present specimen is identified as NV.

scoliodoni. The present specimen was obtained from a carcharhinid

shark from South Africa, which further extends the distribution of the

species from the Indian to the South African coast.

Palm (1997b) found similar small Nybelinia specimens (SL=640,

SP=3.6:2:1) with a similar tentacular armature (L=5—24, rose-thorn

shaped basal and spiniform metabasal hooks (Fig. 18; figure 17 in

Palm, 1992) in Pseudupenaeus maculatus from the North-East

Brazilian coast and described the specimens as N. indica with a

homeomorphous metabasal armature. The drawing of the tentacular

armature of one of the specimens as given in Palm (1992) shows

similar hooks as demonstrated for the present specimens. However,

its affinities with N. indica or N. scoliodoni cannot be decided at

present (see above).

142

Fig. 16 Nybelinia scoliodoni. Scolex from Carcharhinus limbatus. Scale

bar=50 um.

Fig. 18 N. indica. Homeomorphous basal and metabasal armature (Palm

1992). Scale bar=20 pm.

H.W. PALM

Fig. 17 N. scoliodoni. Homeomorphous basal and metabasal armature

consisting of rose-thorn shaped and falcate hooks. Scale bar=20 ym.

9. Nybelinia sp.

MATERIAL EXAMINED. BMNH 1979.9.13.94, leg. R. van der Elst,

2 postlarvae from the kidney of Coryphaena hippurus, Cape Vidal,

South Africa.

DESCRIPTION. The following measurements were taken: SL=1172,

1228; SW=775, 907; pbo=888, 850; pv=624, 548; pb=252, 257;

ppb= 33, 38; app=364, 294; vel= 186; 150; BL=246 (234-247), 251

(224-266); BW=99 (84-112), 114 (112-117); BR=2.5:1, 2.2:1;

SP=3.5:2.5:1, 3.3:2.1:1. The tentacles are long, TL=586—606, 583

and slender, TW=32.8-35.2, 32.8-35.2 and a basal swelling is

absent. The tentacle sheaths are sinuous; TSW=32.8-37.6, 32.8—

37.6. Prebulbar organs and muscular rings around the basal part of

the tentacle sheaths are absent. The retractor muscles originate at the

basal part of the bulbs.

The tentacular armature is homeoacanthous, homeomorphous

and a characteristic basal armature is absent. The small and rose-

thorn shaped hooks are of the same size along the tentacle,

L=8.0-10.4, 8.0-10.4; B=8.8—11.0, 8.8—11.0; hsr=6.

REMARKS. The present specimens resemble N. oodes and N. risert

as described by Dollfus (1960), both species having small rose-thorn

shaped homeomorphous hooks along the tentacle. N. riseri has a

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

different scolex form (see above), larger TW and TSW and the

tentacular hooks are larger. In contrast, the morphological measure-

ments SL, TL, TW, TSW and the small size and form of the hooks

are similar to N. oodes (SL=920, TL=400-500, TW=24-27,

TSW=40-48, B=9.3—10.6) as described by Dollfus (1960). Exami-

nation of the type material revealed a slightly heteromorphous

tentacular armature for N. oodes. This neither corresponds to the

original description (see Dollfus, 1960, Figs 36-37) nor to the

present specimens. Thus, the present postlarvae should not be

assigned to Nybelinia oodes and might represent a new Nybelinia

species. This needs to be decided after re-description of the Nybelinia

type material deposited at the MNHN Paris.

Heteronybelinia gen. nov.

Trypanorhynchs with the characters of the Tentaculariidae Poche,

1926. Scolex compact, 4 triangular bothridia, with hook-like

microtriches along the bothridial borders and filamentous

microtriches on the rest of the bothridia and the scolex. 4 tentacles

emerging from bulbs, retractor muscle originates at base of bulbs. 4

proboscis of variable length and width, armed with hooks; metabasal

tentacular armature homeoacanthous with heteromorphous hooks

on different tentacle surfaces. Basal hooks heteromorphous, charac-

teristic basal armature absent or present. Cirrus unarmed, cirrus sac

alternates irregularly.

TYPE SPECIES. Heteronybelinia estigmena (Dollfus, 1960).

OTHER SPECIES. H. alloiotica (Dollfus, 1960), H. cadenati (Doll-

fus, 1960), H. elongata (Shah & Bilquees, 1979), H. eureia (Dollfus,

1960), H. heteromorphi sp. nov., H. karachii (Khurshid & Bilgees,

1988), H. minima sp. nov., H. nipponica (Yamaguti, 1952), H.

perideraeus (Shipley & Hornell, 1906), H. punctatissima (Dollfus,

1960), H. robusta (Linton, 1890), H. rougetcampanae (Dollfus,

1960), H. senegalensis (Dollfus, 1960), H. yamagutii (Dollfus,

1960), all formerly belonging to the genus Nybelinia Poche, 1926.

COMMENT. This new genus comprises subgroup II in Palm er al.

(1997).

10. Heteronybelinia elongata (Shah & Bilqees, 1979)

comb. nov. (Figs 19-25)

MATERIALEXAMINED. Types BMNH 1989.5.18.5, Shah & Bilgees

leg., 1979, 2 postlarvae from Pellona elongata, Pakistan; BMNH

1980.6.23.13, A. Roy Jleg., 1 postlarva from the gonads of

Lepturacanthus savala, Hooghly estuary, India. Other material not

measured: BMNH 1992.7.1.193-196, A. Roy leg., postlarva from

Lepturacanthus savala, Sugar Island, Bay of Bengal.

DESCRIPTION. The scolex morphology of the type material of H.

elongata (Shah & Bilgees, 1979) from Pellona elongata, together

with the scoleces and armature of specimens from Lepturacanthus

savala, are given in Figs 19—25. The type material is re-described as

follows (Fig. 19): The scolex is about 2 mm large, but is variable in

size, SL=2173, 2362 (a third specimen on the same slide: 1740);

SW=1000, 1021; pbo=982, 964; pv=1021, 1021; pb=536, 548;

ppb= 227, 252; app=605, 624; vel=302, 300; BL=514 (490-536),

525 (510-548); BW=130 (125-135), 128 (112-144.8); BR=3.9:1,

4.1:1; SP= 1.8:1.9:1. The tentacles are long and slender with a TW

metabasal =15.2—17.6; TW basal= 17.6—20.8, diminishing slightly

towards the metabasal part of the tentacle. A basal tentacular

swelling is absent. Prebulbar organs were absent, muscular rings

around the basal part of the tentacle sheaths were visible in some

143

specimens (see also Fig. 22). Tentacle sheaths straight; retractor

muscles originate at the basal part of the bulbs.

The tentacular armature is homeoacanthous, heteromorphous,

and a characteristic basal armature is absent (see Figs 23-24). The

form of the hooks is rose-thorn shaped. The hook size in the

metabasal region (see Fig. 25) ranged between L=11.2—12.8; B=9.2—

11.2, 11.2-12.8 (bothridial) and L=9.2—11.2, 8.8-11.2; B=5.6-7.2,

7.2—9.2 (antibothridial), and the hook size in the basal region of the

tentacle was between L=9.2—11.2; B=9.2—11.2 (bothridial) and

L=5.6-7.2; B=4—5.6, 5.6-7.2 (antibothridial); the hook size in-

creases only on the antibothridial tentacle surface; hsr=6—7.

Postlarvae from Lepturacanthus savala (Fig. 20): Measurements:

SL=1360; SW=642; pbo=662; pv=605; pb=397; ppb=61; app=257;

vel=233; BL=387 (377-397), BW=91 (89-94); BR=4.2:1; SP=

1.7:1.5:1. The tentacles are long and slender with a TW metabasal

=20.8-24; TW basal= 2427.2. A basal tentacular swelling is ab-

sent. Prebulbar organs are absent and muscular rings around the

basal part of the tentacle sheaths are present; TSW= 32.8-36,

straight; retractor muscles originate at the basal part of the bulbs.

The hook size in the metabasal armature ranged between L=9.6—

11.2; B=9.2-11.2 (bothridial) and L=8.0—-9.2; B=5.6-7.2

(antibothridial), and the hook size in the basal part of the tentacle

was between L=7.2—9.2; B=7.2—9.6 (bothridial) and L=4—5.6; B=

5.6—7.2 (antibothridial); The hook size increases mainly on the

antibothridial tentacle surface towards the metabasal part of the

tentacle; hsr=6—7.

Scoleces, muscular ring and the tentacular armature of specimens

BMNH 1992.7.1.193—196 are shown in Figs 21—25.

REMARKS. The type material of NV. elongata from Pellona elongata

is re-described, as well as additional material of the same species

collected from Lepturacanthus savala. Though the material differs

in absolute morphometrical values, BR, SP and the tentacular

armature are very similar. Recently, Palm & Walter (1999) exam-

ined the type material of N. perideraeus from the Natural History

Museum Vienna and re-described the species as having a

homeoacanthous, heteromorphous tentacular armature. The authors

considered N. dakari to be synonymous with N. perideraeus, char-

acterised by tentacular hooks of similar size in the basal and metabasal

part of the tentacle. The present material of NV. elongata also has very

similar scolex measurements as well as similar tentacular hooks to

those of N. perideraeus. However, the hook size increases on the

antibothridial tentacle surface towards the metabasal part of the

tentacle. Thus, until further material becomes available, both spe-

cies are considered valid. The position of N. elongata changes from

subgoup IAb to [Aa in Palm ef al. (1997).

N. elongata appears to have a high degree of scolex variability,

e.g. the SL ranges between 1739 and 2362 in 3 different specimens

on the same slide. As well as similarities between N. elongata and N.

perideraeus, a close relationship can be seen to other species from

subgroup IIAa, all having a similar armature with similar sized

tentacular hooks. Itis recommended that the type material of species

in subgroup II1Aa described by Dollfus (1960) be compared with WN.

perideraeus and N. elongata to clarify the species identity within

this subgroup (also see below).

11. Heteronybelinia estigmena (Dollfus, 1960) comb. nov.

(Figs 26-28)

MATERIAL EXAMINED. BMNH 1976.11.5.42—-43, R. van der Elst

leg., 1 adult from the gut of Carcharhinus limbatus, South Africa;

BMNH 1985.11.8.63-64,. R. van der Elst Jeg; 11.05.1984, 1 adult

from Carcharhinus leucas, Richards Bay, South Africa; BMNH

‘

144

Fig. 20 H. elongata. Scolex from Lepturacanthus savala. Scale bar=100

Fig. 19 Heteronybelinia elongata. Scolex from Pellona elongata. Scale

um.

Fig. 22 H. elongata from L. savala.. Muscular ring around tentacle

bar=200 pm.

50 pm.

sheath. Scale bar

H. elongata. Scolex from L. savala. Scale bar=100 pm.

Fig. 21

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

145

Fig. 23 H. elongata from L. savala. Heteromorphous basal armature, external surface. Scale bar=10 um.

Fig. 24 H. elongata from L. savala. Heteromorphous basal armature, bothridial surface, external face on left hand side. Scale bar=10 um.

Fig. 25 H. elongata from L. savala. Heteromorphous metabasal armature, external surface. Scale bar=10 um.

1996.8.19.1—3, D.T.J. Littlewood leg., Aug. 1995, | postlarva from

the stomach of a kingfish, Port Royal, Kingston, Jamaica.

DESCRIPTION. The scolex of a specimen from C. limbatus is

shown in Fig. 26. Measurements: SL=1210, 1134, 1000; SW=700,

nm, 493; pbo=700, 642; 500; pyv=510, 473, 500; pb=448, 330; 307;

ppb=95, 75, 27; vel=170, 232, 160; BL=442 (428-448), 326 (312-

331), 287 (280-294); BW=128 (126-130), 104 (84-107), 81 (75-92);

Bommel o-S3l: Se 6:0: 1) 19:1 421° 1.6:1.6:1. The ten-

tacles are long and slender, with TW=27-30; 23-28, 20-22; TSW

increases in size towards the base of the tentacles (24—27, 22-28,

29-32), a basal tentacular swelling is absent. Prebulbar organs are

absent and muscular rings around the basal part of the tentacle

sheaths are present in specimens from Carcharhinus spp. The

retractor muscles originate at the base of the bulbs.

The tentacular armature is homeoacanthous, heteromorphous,

and a characteristic basal armature is absent (Figs 27—28). The

hooks diminish in size towards the basal part of the tentacle, the

hooks are rose-thorn shaped on both sides of the tentacles. The

single hook sizes of the three specimens in the metabasal armature

were L=9.2-11.2, B=9.2-11.2; L=10.4-12, B=10.4-12; L=9.2-

10.5, B=9.3-10.5 (mean L bothridial=10.4) and L=7.2—9.6,

B=7.2-9.6; L=9.6-10.4, B=10.4-12; L=7.4-8, B=7.4-8 (mean L

antibothridial=8.7), and in the basal part of the tentacle L=7.2—9.2,

B=7.2-9.2; L=7.2-8.8, B=7.2-8.8; L=7.2-8, B=7.2-8 (bothridial)

and L=5.6—7.2, B=5.6—7.2; L=5.6—7.2, B=4.8-5.6; L=5-6, B=5-6,

(antibothridial); hsr=6—7.

The slightly stained strobila of the specimen from Carcharhinus

limbatus consists of about 190 acraspedote proglottids. Proglottids

wider than long and increasing in size (about 50" proglottid: 55-60

x 475-485; 100": 185-210 x 560-585; 150": 360-420 x 755-780;

190": 670-730 x 840-900). 80-90 testes in a single layer, 33-55

(between 100" and 150" segments) and 50—65 (final segments) in

diameter. Genital pores ventro-lateral, in the anterior half near the

middle of the proglottids, alternate irregularly; cirrus sac elongate,

directed anteromedially, reaching the anterior end of the proglottids;

increasing in size, from 50-60 x 290-350 until 85-90 x 345-365 in

last segments. Other internal structures not seen. The acraspedote

proglottids of the specimen from Carcharhinus leucas vary in size,

Fig. 26 Heteronybelinia estigmena. Scolex from Carcharhinus limbatus.

Scale bar=100 pm.

146

27 28

Fig. 27 #H. estigmena from C. limbatus. Heteromorphous basal armature,

bothridial surface. Scale bar=10 ym.

Fig. 28 H. estigmena from C. limbatus. Heteromorphous metabasal

armature, antibothridial surface. Scale bar=10 um.

depending on contraction (anterior segments: 80 x 330-20 x 520),

final segments 300-370 x 860-880; testes 33-55 in diameter.

REMARKS. The present specimens are most similar to H. alloiotica,

H. punctatissima and H. estigmena, which were considered as

belonging to subgroup I[Aa by Palm et al. (1997), comprising

species having a heteromorphous tentacular armature with hooks

diminishing in size towards the basal part of the tentacle, and no

characteristic basal armature. Dollfus (1960) described 6 species, H.

dakari, H. estigmena, H. punctatissima, H. senegalensis, H. alloiotica

and H. cadenati, with a heteromorphous tentacular armature and

small hooks of about 10—11 pm (bothridial) and 8 um (antibothridial).

All these species have a very similar scolex and hook morphology,

mainly differing from each other by a different bulb ratio and

different scolex proportions. Palm & Walter (1999) proposed the

synonymy of Nybelinia dakari Dollfus, 1960 with H. perideraeus,

differing from the other species in having a basal armature of similar

size to the metabasal armature. Though Dollfus (1960) stated that

the bulb ratio of H. dakari was small (about 2.5:1), his drawing

(figure 43) indicates a ratio of about 4. His bulb measurements of

0.380—0.386 x 0.96—0.100 mm are faulty (0.96 might stand for

0.096), which would also indicate a bulb ratio of about 3.9, thus,

corresponding to the ratio of H. perideraeus (see Palm & Walter,

1999). H. senegalensis, H. alloiotica and H. cadenati also have a

bulb ratio of about 4, and H. punctatissima differs from H. estigmena

by having a slightly different bulb ratio and different scolex dimen-

sions (2.1:1.6:1 vs 1.5:1:1). However, these two species appear to be

very similar, and the tentacular armature of H. alloiotica (Figs 29—

30), which was re-described by Palm (1995) from Carcharhinus

limbatus from the Gulf of Mexico, also corresponds with that of the

present material. The present finding represent 3 new host and

locality records for H. estigmena.

This and a previous study (Palm & Walter, 1999) demonstrate

wide intraspecific variability in scolex morphology within several

species of Nybelina (see also H. africana) and Heteronybelinia,

similar to that described earlier for other tentaculariid genera

Tentacularia and Hepatoxylon (Palm, 1995). Additionally, Palm et

al. (1997) pointed out the dubious value of the 2 characters tentacle

width and bulb ratio, which Dollfus used to distinguish the above 6

H.W. PALM

Fig. 29 Heteronybelinia alloiotica from Carcharhinus limbatus.

Heteromorphous basal armature, bothridial surface. Scale bar=10 um.

Fig. 30 4. alloiotica. Heteromorphous metabasal armature, antibothridial

surface. Scale bar=10 um.

species. The identification of the present specimens as

Heteronybelinia estigmena needs to be confirmed by re-examining

the type material of the above mentioned species. The possibly

synonymy of all these species has to be kept in mind.

Heteronybelinia cf. estigmena (Dollfus, 1960) comb. nov.

MATERIAL EXAMINED. BMNH 1989.1.18.2, R. Bray leg.,

14.01.1971, Cirolana, Atlantic Ocean off Morocco, 33°43'N, 8°38'W,

222-236 m. | postlarva from Scomber scolias.

REMARKS. Due to its scolex morphology and the homeoacanthous,

heteromorphous tentacular armature with a basal hook size of

L=8.8-10.4, B=8.8—10.4 (bothridial) and L=5.6—-7.2, B=5.6—7.2

(antibothridial), the present specimen was tentatively identified as

H. estigmena. However, the partly invaginated metabasal armature

and the unusual form due to fixation prevent precise identification.

The presence of a muscular ring around the tentacle sheaths could

not be demonstrated to be of any taxonomic significance.

12. Heteronybelinia heteromorphi sp. nov. (Figs 31-33)

MATERIAL EXAMINED. Holotype and paratype, BMNH

1982.4.26.282—284, R. van der Elst /eg., 16.5.78, 2 adults from the

stomach of Sphyrna mokarran, South Africa; Additional material:

BMNH 1968.2.14.30-31, Gooding /eg., 2 adults from Sphyrna

blochii, Singapore.

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

147

Fig. 31 Heteronybelinia heteromorphi sp. nov.. Scolex from Sphyrna makorran. Scale bar=100 um.

Fig. 32. H. heteromorphi sp. nov. from S. makorran. Heteromorphous metabasal armature, bothridial (left hand side) and antibothridial (right hand side)

surfaces. Scale bar=15 um.

Fig. 33H. heteromorphi sp. nov. from S. makorran. Heteromorphous basal armature, bothridial (left) and antibothridial (right) surfaces. Scale bar=15 pum.

DESCRIPTION (Figs 31-33). With the characters of the genus

Heteronybelinia. Measurements: SL=1367, 1300, 1367, 1467;

SW=833, 934, 800, 800; pbo=767, 734, 734, 867; pyv=534, 500, 567,

506; pb=500, 447, 334, 427; ppb=20, 40, 105, 160; vel=333, 340,

317, 300; BL=437 (414-454), 404 (387-414), 327 (308-334), 405

(368-427); BW=154 (134-163), 181 (174-187), 158 (137-175),

iGm@WiS—i79): BR=2.8:1,, 2-2:15 211. 2.321; SP=1.5:1.1:1,

1.6:1.1:1, 2.2:1.7:1, 2.0:1.2:1. The tentacles are long, robust and

increase in diameter towards the tip of the tentacle; TL=540 (27

rows of hooks), 480 (23 rows), 560 (25 rows), nm; TW basal=53-60,

53-60, 48-50, 52-54; TW apical=75—80, 65-70, 58-61, nm; a basal

swelling is absent. The tentacle sheaths are straight; TSW=53-66,

45-54, 68-70, 69-74. Prebulbar organs and muscular rings around

the basal part of the tentacle sheaths are absent. A thickening,

encircling more than half of the tentacle sheath near the entrance to

the bulbs, is present. The retractor muscles originate at the basal part

of the bulbs.

The tentacular armature is homeoacanthous, heteromorphous,

and a characteristic basal armature is absent. The form of the hooks

is rose-thorn shaped becoming more slender towards the tip of the

tentacle (Fig. 32). Similarly, the form changes from the bothridial to

the antibothridial surface. The hook sizes of the metabasal tentacular

armature for BMNH 1982.4.26.282—284 and 1968.2.14.30-31 are

as follows: above 22th row, L=24—28, B=19-21; L=25-—28, B=15-—

17 (bothridial) and L=28-32, B=12-15; L=30-32, B=12-15

(antibothridial); about 14th row, L=22—25, B=16—-17; L=21-23,

B=16-17 (bothridial) and L=25—28, B=11—15; L=30-32, B=12-15

(antibothridial); The basal hooks (Fig. 33) ranged between L=16—18

and B=10-12; hsr=7-8.

The strobila of the largest specimen of BMNH 1982.4.26.282—

284 consists of about 350 acraspedote proglottids. The proglottids

are uniform in measurements, much wider (934—1034) than long

(50-134). Proglottids of smaller specimens measured about 600 in

width and 100 in length. The genital pores alternate irregularly;

cirrus sac 35-40 x 140-160. Small testes (25-40 in diameter) and

vitellaria (10-15); other internal structures not seen.

REMARKS. The present specimens belong to subgroup I[Aa (Palm

et al., 1997), with a heteromorphous armature and hooks increasing

in size towards the metabasal part of the tentacle. The large hook size

148

Fig. 34 Heteronybelinia minima sp. nov.. Scolex from Harpodon

nehereus. Scale bar=50 pm.

and the tight arrangement of the hooks along the tentacle is charac-

teristic for the specimens, and together with the heteromorphous

armature, the character combination corresponds only with

Heteronybelinia eureia as described by Dollfus (1960). Though the

morphometrical data correspond, the drawings of the tentacular

armature of H. eureia as given by Dollfus (1960, figures 33-35)

indicate more widely spaced and more slender hooks than was

observed in the present specimens. This was confirmed by examina-

tion of the type material at the MNHN Paris. Additionally, the

description by Dollfus, based on postlarvae, precludes comparison

of the strobilar characters. Thus, the present specimens represent a

new species, Heteronybelinia heteromorphi sp. nov. Other similar

species with a compact hook pattern are Nybelinia queenslandensis

and N. strongyla (see Jones & Beveridge, 1998, Dollfus, 1960).

However, these species have a homeomorphous tentacular armature.

ETYMOLOGY. The new species is named after the characteristic

heteromorphous armature.

13. Heteronybelinia minima sp. nov. (Figs 34-38)

MATERIAL EXAMINED. Holotype and paratype, BMNH

1980.12.2.1, A. Roy leg., 14.09.79, 2 postlarvae from Harpodon

H.W. PALM

Fig. 35 4H. minima sp. nov.. Scolex from Polynemus paradiseus. Scale

bar=100 um.

Fig. 36 H. minima sp. nov. from P. paradiseus. Heteromorphous

metabasal armature, bothridial (left hand side) and antibothridial (right

hand side) surfaces. Scale bar=15 um.

Fig. 37 H. minima sp. nov., hooks on bothridial surface. Scale bar=15

uum.

Fig. 38H. minima sp. nov., hooks on antibothridial surface. Scale

bar=15 ym.

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

nehereus, Houghly estuary, India. Other postlarvae identified as H.

minima sp. nov.: BMNH 1980.6.23.13 from Polynemus sp.;

1980.6.23.14, A. Roy leg., Polynemus sp., Houghly estuary, India (4

postlarvae); 1992.7.1.189 from Harpodon nehereus; 1992.7.1.190—

192, A. Roy leg., Polynemus paradiseus, Sugar Island, Bay of

Bengal (5 postlarvae).

DESCRIPTION. With the characters of the genus Heteronybelinia.

The scolex of the holotype as well as the scolex and basal and

metabasal tentacular armature of a specimen from P. paradiscus are

shown in Figs 34 and 35-38 respectively. The scolex is small,

differing in size and shape between specimens. Measurements (from

types 1980.12.2.1): SL=706, 926; SW=386, 642; pbo=427, 454;

pv=267, 397; pb=200, 252; app=280, 270; vel=84, 186; BL=191

(187-200), 237 (229-252); BW=54 (43-66), 83 (74-89); BR=3.5:1,

2.9:1; SP=2.1:1.3:1, 1.8:1.6:1. The tentacles are long, in inverted

condition nearly reaching the apical end of the bulbs, with a TW=23-

28; TW increases towards the tip of the tentacles, a basal tentacular

swelling is absent. Prebulbar organs and muscular rings around the

basal part of the tentacle sheaths are absent. The retractor muscles

originate at the base of the bulbs (Fig. 34).

The tentacular armature is homeoacanthous, heteromorphous and

a characteristic basal armature is absent (Figs 36-38). The hooks

diminish in size towards the basal part of the tentacle, the form of the

hooks differs from compact and rose-thorn shaped (bothridial) to

falcate hooks with a stout base (antibothridial). The hook size in the

metabasal armature ranged between L=20.8-—24; B=15.2-16.8

(bothridial) and L=24—27.2; B=5.6-7.2 (antibothridial), and the

hook size in the basal part of the tentacle was between L=12-—17.6;

B=7.2-12 (bothridial) and L=15.2—17.6; B=7.2—8.8 (antibothridial);

hsr=6.

ETYMOLOGY. ‘The new species is named for its small size.

REMARKS. H. minima sp. nov. is easily identifiable by its small

scolex size and the characteristic tentacular armature. The present

specimens from Harpodon nehereus, Polynemus paradiseus and

Polynemus sp. clearly demonstrate a heteromorphous armature,

where the hook form changes from rose-thorn shaped to falcate

hooks, giving the tentacles a heteroacanthous appearance. However,

the quincunx formation of the hooks is still recognisable. The

absence of a characteristic basal armature places the species in

subgroup IIAa of Palm et al. (1997).

14. Heteronybelinia robusta (Linton, 1890) (Figs 39-41)

MATERIAL EXAMINED. BMNH 1976.11.5.42-43, R. van der Elst

leg., 1 adult from the gut of Carcharhinus limbatus, South Africa.

Additional material: USNPC 7727, E. Linton /eg., 3 adults from

Dasyatis centroura, Woods Hole, USA.

DESCRIPTION (Figs 39-41). With the characters of the genus

Heteronybelinia. Measurements: SL=1020; SW=699; pbo=510;

pv=377; pb=257; vel=294; BL=246 (233-257); BW=82 (79-84);

BR=3:1; SP=2:1.5:1. The tentacles are slender, and increase in

width towards the metabasal and decrease towards the apical part of

the tentacle; TW=24—30; a basal swelling is absent. The tentacle

sheaths have two spiral coils; TSW=24-27. Prebulbar organs and

muscular rings around the basal part of the tentacle sheaths are

absent. The retractor muscles originate at the basal part of the bulbs.

The tentacular armature is homeoacanthous, heteromorphous and

a characteristic basal armature is absent. The form of the hooks

changes slightly from compact and rose-thorn shaped (bothridial) to

more slender hooks with a stout base (antibothridial) (Fig. 40). The

149

hook size in the metabasal armature ranged between L=11.7—12.5;

B=7.2-9.2 (bothridial) and L=13.0-14.0; B=5.6—7.2 (antibothridial),

and hooks of the basal part of the tentacle (Fig. 41) were minute,

between L=5.6—7.2; B=5.6—7.2 (bothridial) and L=4—-5.6; B=4—5.6

(antibothridial), continuously increasing towards the tip; hsr=6—7.

The strobila of the small specimen consists of 71 acraspedote

proglottids. Measurements of the proglottids were as follows: proglot-

tid 20: length=48, width=320; proglottid 48: length=140, width=400;

proglottid 62: length=490, width=656; proglottid 70: length=610,

width=746. Genital pores ventro-lateral, in the anterior third of the

proglottids, alternate irregularly; cirrus sac elongate, directed

anteromedially, reaching the anterior end of the proglottids. Other

internal structures were not seen.

REMARKS. ‘The present specimen corresponds to 3 specimens

described as N. robusta by Linton (1924). Scolex measurements and

the characteristic tentacular armature lie within the same range.

Thus the present specimen is identified as belonging to the same

species. However, as the type material of N. robusta is not available

at the USNPC, the taxonomy of N. robusta still needs to be clarified.

There are several species which have rose-thorn-shaped hetero-

morphous hooks along the tentacle. H. robusta differs from all

adequately described species due to the small scolex size with

minute basal hooks, continuously increasing in size from 5 to 12.5

(bothridial) and 4 to 14 um (antibothridial). The general hook form

remains rose-thorn shaped along the tentacles. Thus, the present

specimen belongs into subgroup [Aa of Palm et al. (1997).

15. Heteronybelinia yamagutii (Dollfus, 1960) nov. comb.

(Fig. 42-44)

MATERIAL EXAMINED. BMNH 1976.11.5.41, R. van der Elst leg.,

| adult from the stomach of Sphyrna lewini, South Africa.

DESCRIPTION. Nybelinia yamagutii was described in detail by

Dollfus (1960, see figures 1-5) and Palm et al. (1997). The follow-

ing measurements were taken: SL=2646; SW=1080; pbo=1134;

pv=1000; pb=1455; vel=140; BL= 1430 (1418-1455); BW= 236

(220-247); BR=6.1:1; SP=0.8:0.7:1. The tentacles are long and

slender and deminish in size along the tentacle; TW metabasal=90—

98, TW apical=66—75. A basal tentacular swelling is not present.

The tentacle sheaths are sinuous; TSW=51—56. Prebulbar organs

and muscular rings around the basal part of the tentacle sheaths are

absent. The retractor muscles originate in the basal part of the bulbs.

The armature is homeoacanthous, heteromorphous, and a charac-

teristic basal armature with bill-hooks is present. The hooks of the

metabasal armature are different in shape and size on bothridial and

antibothridial tentacle surfaces. The form of the hooks is described

in detail in Dollfus (1960). The hook size in the metabasal armature

was between L=69-—75 (bothridial) and L=60—65 (antibothridial).

The size of the basal hooks was between L=18-23. The bill-hooks

were in rows 3-4 with a total length of 41-46.

The 12.5 cm long worm has a craspedote strobilar with several

hundred segments increasing in size (Figs 42-44); last proglottid

with rounded proximal end. The size varies in the first 2 cm of the

strobila between 70-100 long and 300-420 wide, from 4-5 cm

between 195-220 and 780-900 (Fig. 42), from 7-8 cm between

360-420 and 1260-1400 (Fig. 43), and at the final proglottids

between 360-400 and 1680-1820 (Fig. 44). In mature proglottids,

the elongate cirrus sac is directed anteromedially, and alternates

irregularly (Fig. 42). Testes often ovoid, in double layer, often not in

middle of segments. Testes number per proglottis (62—70 and 80-90),

size (40-55 and 50—70 in diameter) and size of vitellaria (13-16 and

15—33 in diameter) increases between the first 3 cm and after 7 cm

150

H.W. PALM

Fig. 39 Heteronybelinia robusta. Scolex from Carcharhinus limbatus. Scale bar=100 um.

Fig. 40H. robusta Heteromorphous metabasal armature, bothridial (right hand side) and antibothridial (left hand side) surfaces. Scale bar=10um.

Fig. 41 4H. robusta. Heteromorphous basal armature, antibothridial surface. Scale bar=10 um.

of the strobila respectively. Ovary centally, follicular, with 2 major

branches.

REMARKS. The scolex measurements as well as the form and size

of the tentacular armature correspond with those in the original

description (Dollfus, 1960) and those of specimens from the Mo-

zambique coast (Palm et. al., 1997). A high variability in scolex

morphology has been described from 20 specimens of 7 host species

by Palm et al. (1997). However, H. yamagutii is easily distinguish-

able from all other Heteronybelinia species by its metabasal tentacular

armature consisting of large claw-like hooks and its basal armature

consisting of smaller hooks and characteristic bill hooks. Adult H.

yamagutii is a large trypanorhynch with segments of different shape

and size along the strobila. The testes number as well as the size of

testes and vitellaria also vary along the strobila. The present finding

is the first report of adult H. yamagutii, occurring in Sphyrna lewini

from South Africa. A world-wide distribution for the species has

been proposed by Palm et al. (1997).

Mixonybelinia gen. nov.

Trypanorhynchs with the characters of the Tentaculariidae Poche,

1926. Scolex compact, 4 triangular bothridia, with hook-like

microtriches along the bothridial borders and filamentous

microtriches on the rest of the bothridia and the scolex. 4 tentacles

emerging from bulbs, the retractor muscle originates at the base of

the bulbs. 4 proboscides of various length and width, armed with

massive hooks; metabasal tentacular armature homeoacanthous with

heteromorphous hooks on different tentacle surfaces. Characteristic

basal armature consisting of homeomorphous hooks present. Cirrus

unarmed, cirrus sac alternates irregularly.

TYPE SPECIES. Mixonybelinia beveridgei (Palm, Walter,

Schwerdtfeger & Reimer, 1997) (subgroup II in Palm et al., 1997).

OTHER SPECIES. Mixonybelinia southwelli (Palm & Walter, 1999)

16. Mixonybelinia beveridgei (Palm, Walter,

Schwerdtfeger & Reimer, 1997) comb. nov.

MATERIAL EXAMINED. The Natural History Museum London:

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

Fig. 42-44 H.. yamagutii. Strobila 4-5 cm (42) and 7-8 cm (43) behind

scolex, and last proglottids (44). Scale bar=500um.

BMNH 1997.3.24.1, 1997.3.24.2, 1997.3.24.3-4, 1997.3.24.5. M.

beveridgei was described in detail by Palm et al. (1997).

17. Mixonybelinia southwelli (Palm & Walter, 1999)

comb. nov.

MATERIAL EXAMINED. The Natural History Museum London:

BMNH 1977.11.4.7, 1977.11.4.8-9. M. southwelli was described in

detail by Southwell (1929) and Palm & Walter (1999).

DISCUSSION

Of the material deposited at the British Museum Natural History, 17

different trypanorhynch species, formerly all belonging to the genus

Nybelinia Poche, 1926, were identified. In addition, two new gen-

era, Heteronybelinia gen. nov. and Mixonybelinia gen. nov., are

erected, and 4 new species, N. sakanariae sp. nov., N. schmidti sp.

nov., H. heteromorphi sp. nov., and H. minima sp. nov., are de-

scribed. The new genera separate species with a homeoacanthous,

homeomorphous (Nybelinia) from those having a homeoacanthous,

heteromorphous metabasal armature with heteromorphous basal

hooks (Heteronybelinia gen. nov.) and from species with a

heteromophous metabasal and homeomorphous basal armature,

which are assigned to Mixonybelinia gen. nov. Mixonybelinia is a

tentaculariid genus in which two different armature types occur

along the tentacle. This has been described earlier for non-

tentaculariid trypanorhynchs, such as the mixodigmatid Mixodigma

151

leptaleum Dailey & Vogelbein, 1982 and the lacistorhynchid

Dasyrhynchus talismani, Dollfus, 1935 (Dailey & Vogelbein, 1982;

Beveridge & Campbell, 1993)

After a first subdivision of the genus by Dollfus (1960), Palm er

al. (1997) recently subdivided the different Nybelinia species on the

basis of the tentacular armature and discussed the erection of

subgenera. However, the authors did not split the genus into several

genera or subgenera. The material in the Natural History Museum

clearly demonstrates that the species of the subgroupings as pro-

posed by Palm ef al. (1997) can be consistently separated on the

basis of their characteristic metabasal and basal tentacular armature.

They can clearly be recognised, though there is a higher level of

intraspecific variation associated with the scolex as well as hook

sizes along the tentacles than previously indicated.

Following Campbell & Beveridge (1994) and Palm (1995), the

erection of different genera on the basis of the tentacular armature is

justified. In their most recent classification, Campbell & Beveridge

(1994) used the tentacular armature at the superfamily level, and

Palm (1995) at the generic level. In other families within the order,

several genera can be distinguished mainly on basis of their charac-

teristic tentacular armature, such as the genera Callitetrarhynchus,

Lacistorhynchus, Mixodigma, Poeciloacanthum and Pseudolacisto-

rhynchus (other examples see Campbell & Beveridge, 1994, Palm,

1995). This simplifies further studies of tentaculariid trypanorhynchs

of the Nybelinia type.

The present study again demonstrates a high level of morphologi-

cal variation within different species of Nybelinia and Hetero-

nybelinia. Nybelinia africana and Heteronybelinia yamagutii have

been re-described and do not correspond in every detail with the

original descriptions of the type material. Similar morphological

variation occurs in other tentaculariid trypanorhynchs, such as

Tentacularia coryphaenae, evidenced by the numerous synonymies

in the literature (see Dollfus, 1942, Palm, 1995). In comparing the

detailed descriptions of 16 Nybelinia species recognised by Dollfus

(1960), several of them are very similar and can be distinguished

only on the basis of minor differences of the hooks, which lie within

the limits of intraspecific variation for this character in more re-

cently described species (see Palm & Walter, 1999). Additionally,

Palm et al. (1997) demonstrated a low host specificity of several

Nybelinia species, which leads to the suggestion that some of the

material examined by Dollfus, which was mainly obtained from the

same region off Dakar but from different host fish species, might

belong to the same species. This is especially possible in subgroup

Il[Aa (Heteronybelinia estigmena species complex) and in the

Nybelinia aequidentata species complex (see remarks above). It is

recommended that until the type material and more material from

the Dakar region can be examined, the species described by Dollfus

(1960) remain valid. However, several are possible synonyms.

Adult tentaculartids also can show a low level of host specificity

and different shark species can harbour several Nybelinia and

Heteronybelinia species. During the present study, Carcharhinus

limbatus and C. leucas were found to be infested with 3 species

(Nybelinia scoliodoni, Heteronybelinia estigmena, H. robusta) and

2 species (Nybelinia africana, Heteronybelinia estigmena) respec-

tively. A similar wide host range has been also demonstrated for

some other trypanorhynchs (Palm & Overstreet in press, Palm,

1997b) as well as other marine parasite species, such as Antarctic

parasites infesting the rock cod Notothenia coriiceps from the

South Shetland Islands (Palm et al., 1998). This behaviour seems

to be characteristic for cosmopolitan marine parasitic helminths,

such as the nematodes Contracaecum osculatum and

Pseudoterranova decipiens. In conclusion, it is postulated that the

currently known tentaculariid genera and most of the species are

152

characterised by a cosmopolitan distribution pattern, which distin-

guishes those trypanorhynchs from species such as the

eutetrarhynchids of endemic Australian and South American rays

(see also Palm et al., 1997, Rego & Dias, 1976). A low level of

specialisation of tentaculariids with a flexible, unspecialised life

cycle pattern might be essential for these oceanic trypanorhynchs,

which would explain for example their occurrence in marine plank-

ton (Dollfus, 1974) as well as the enigmatic infestation of humans

(Fripp & Mason, 1983).

The present and previous studies demonstrate that several species

exist which change their kind of tentacular armature continuously

along the tentacle, such as N. africana and N. lingualis. Some

species change more abrupt between a characteristic basal and

metabasal armatures, such as H. scoliodoni and M. southwelli, while

others retain their general hook shape but continuously increase the

hook size, such as in H. estigmena and H. robusta. In N. aequidentata,

the hook size decreases towards the basal and apical part of the

tentacle. It is evident that the tentacular armature within the group is

highly variable, making the description of completely evaginated

tentacles essential for identification. However, these differences in

hook type and size along the tentacles represent an ideal tool for

future taxonomic work within these tentaculariid genera.

CLASSIFICATION

The subgroupings of Palm et al. (1997) remain a basis for further

taxonomic work within tentaculariid trypanorhynchs. Together with

the studies of Palm & Walter (1999) (N. southwelli) and Jones &

Beveridge (1998) (N. queenslandensis), 48 species belong to the

genera Nybelinia (31 species), Heteronybelinia (15) and Mixo-

nybelinia (2). The current classification of tentaculariid cestodes is

as follows:

1. Genus: Tentacularia Bosc, 1797

(type and only species: Tentacularia coryphaenae Bosc, 1797)

2. Genus Nybelinia Poche, 1926 (subgroup I in Palm et al., 1997)

(type species: Nybelinia lingualis (Cuvier, 1817))

A Species without characteristic basal armature

a Size of basal hooks smaller than metabasal hooks:

N. aequidentata (Shipley & Hornell, 1906), NV. anthicosum

Heinz & Dailey, 1974, N. edwinlintoni Dollfus, 1960, N.

goreensis Dollfus, 1960, N. jayapaulazariahi Reimer,

1980, N. palliata (Linton, 1924), N. queenslandensis

Jones & Beveridge, 1998, N. riseri Dollfus, 1960, N.

sakanariae sp. noy., N. schmidti sp. nov., N. sphyrnae

Yamaguti, 1952, N. thyrsites Korotaeva, 1971

b Size of basal hooks equal to metabasal hooks

N. anantaramanorum Reimer, 1980, N. bengalensis

Reimer, 1980, N. oodes Dollfus, 1960, N. pintneri

Yamaguti, 1934, N. rhynchobatus Yang Wenchuan, Lin

Yuguang, Liu Gencheng & Peng Wenfeng, 1995, N.

strongyla Dollfus, 1960, N. surmenicola Okada, 1929, N.

syngenes (Pintner, 1929), N. tenuis (Linton, 1890),

Nybelinia sp.

c Size of basal hooks larger than metabasal hooks

N. basimegacantha Carvajal, Campbell & Cornford, 1976

H.W. PALM

B Species with characteristic basal armature

a Size of basal hooks smaller than or equal to metabasal

hooks

N. africana Dollfus, 1960, N. anguillae Yamaguti, 1952,

N. bisulcata (Linton, 1889), N. erythraea Dollfus, 1960,

N. indica Chandra, 1986, N. lingualis (Cuvier, 1817), N.

manazo Yamaguti, 1952, N. scoliodoni (Viyayalakshmi,

Vijayalakshmi & Gangadharam, 1996)

b Size of basal hooks larger than metabasal hooks

N. gopalai Chandra & Hanumantha Rao, 1985

3. Heteronybelinia gen. nov. (subgroup II in Palm et al., 1997)

(type species: Heteronybelinia estigmena (Dollfus, 1960))

A Without characteristic basal armature

a Size of basal hooks smaller than metabasal hooks

H. alloiotica (Dollfus, 1960), H. cadenati (Dollfus, 1960),

H. elongata(Shah & Bilqees, 1979), H. estigmena(Dollfus,

1960), H. eureia (Dollfus, 1960), H. heteromorphisp. nov.,

H. karachii (Khurshid & Bilgees, 1988), H. minima sp.

nov., H. punctatissima (Dollfus, 1960), H. robusta (Linton,

1890), H. senegalensis (Dollfus, 1960)

b_ Size of basal hooks equal to or larger than metabasal hooks

H. perideraeus (Shipley & Hornell, 1906)

B With characteristic basal armature

a Size of basal hooks smaller or equal than metabasal hooks

H. nipponica (Yamaguti, 1952), H. rougetcampanae

(Dollfus, 1960), H. yamagutii (Dollfus, 1960)

4. Mixonybelinia gen. nov.

(type species: Mixonybelinia beveridgei (Palm, Walter,

Schwerdtfeger & Reimer, 1997))

Mixonybelinia beveridgei (Palm, Walter, Schwerdtfeger &

Reimer, 1997), M. southwelli (Palm & Walter, 1999)

5. Kotorella Euzet & Radujkovic, 1989

(type and only species: Kotorella pronosoma (Stossich, 1901))

Nybelinia lingualis has been considered as belonging to subgroup

TAa by Palm et al. (1997) and is assigned to subgroup Ba on basis of

the gradual change of hook form along the tentacle (see Figs 7-9).

The basal hooks without an anterior extension of the base easily

distinguish the species from most Nybelinia, and therefore are

interpreted as a characteristic basal armature. Some other species

listed in this classification might change their position after re-

examination of the type-material. However, classification as well as

comparative discussions on species validity is simplified if using the

presented scheme. How strobila morphology such as the shape of

segments and structure of the genital complex can be incorporated

into this classification will be an important task for future studies.

PHYLOGENY

The above classification most probably does not reflect the phylogeny

within tentaculariid trypanorhynchs. Palm et al. (1997) failed with

their cladistic analysis of the genus Nybelinia and the present study

TENTACULARIID TRYPANORHYNCHS FROM THE NHM

describes in more detail the high morphological variability in hook

patterns within the genera Nybelinia and Heteronybelinia. Although

the armature types help in distinguishing between the different

species within the group, the same hook forms and patterns are

found within Nybelinia, Heteronybelinia and Mixonybelinia spe-

cies. Beveridge eral. (1999) suggested that the transition in armature

types from homeoacanthous to heteroacanthous has occurred once

and the transition from heteroacanthous to poeciloacanthous types

has occurred several times within trypanorhynch evolution. How-

ever, it has to be considered that the development of heteromorphous

from homeomorphous hook patterns might also have occurred

several times within different species, as proposed by Palm (1995).

Methods other than morphology will be essential to clarify the

phylogenetic situation within the Tentaculariidae

ACKNOWLEDGEMENTS. _ | wish to thank Drs. D. Gibson and R. Bray for the

possibility to study the trypanorhynchs in their collection, and E. Harris for

making material available after my return to Kiel. My thank belongs to Dr. I.

Beveridge for his kind advice in writing this manuscript. Financial support

was provided by the Institut fiir Meereskunde Kiel and The Natural History

Museum, London.

REFERENCES

Arthur, J.R., Margolis, L., Whitaker, D.J. & McDonald, T.E. 1982. A quantitative

study of economically important parasites of walleye pollock (Theragra

chalcogramma) from British Columbian waters and effects of post mortem handling

on their abundance in the musculature. Canadian Journal of Fisheries and Aquatic

Sciences 39: 710-726.

Beveridge, I & Campbell, R.A. 1993. A revision of Dasyrhynchus Pintner (Cestoda:

Trypanorhyncha), parasitic in elasmobranch and teleost fishes. Systematic Parasitol-

ogy 24: 129-157.

1996. New records and descriptions of trypanorhynch cestodes from Australian

fishes. Records of the South Australian Museum 29: |—22.

——,, Campbell, R.A. & Palm, H.W. 1999. Preliminary cladistic analysis of genera of

the cestode order Trypanorhyncha Diesing, 1863. Systematic Parasitology 42: 29-49.

Campbell, R.A. & Beveridge, I. 1994. Order Trypanorhyncha Diesing, 1863. pp. 51—

82. In: Khalil, L.F., Jones, A. & Bray, R.A. (eds) Keys to the cestode parasites of

vertebrates. CAB International, Wallingford.

Chandra, K.J. 1986. Nybelinia indica n. sp. (Cestoda: Trypanorhyncha) from teleost

fishes off Waltair coast, Bay of Bengal. Rivista di Parassitologia 3: 199-202.

Dailey, M.D. & Vogelbein, W. 1982. Mixodigmatidae, a new family of cestode

(Trypanorhyncha) from a deep sea, planktivorous shark. Journal of Parasitology 68:

145-149.

Deardorff, T. L; Raybourne, R. B. & Mattis, T. E. 1984. Infections with trypanorhynch

plerocerci (Cestoda) in Hawaiian fishes of commercial importance. Sea Grant

Quarterly 6: 1-6.

Dollfus, R. P. 1942. Etudes critiques sur les Tétrarhynques du Muséum de Paris.

Archives du Musée National d’Histoire Naturelle 19: 1466.

1960. Sur une collection de Tétrarhynques homéacanthes de la famille des

Tentaculariidae recoltées principalement dans la région de Dakar. Bulletin de

ULFA.N., Série A, 22: 788-852.

— 1974. Enumeratrion des cestodes du plancton et des invertebrés marins. 8

Contribution. Annales de Parasitologie Humaine et Comparée 49: 381-410.

153

Fripp, P. J. & Mason, P. R. 1983. Spurious human infection with a trypanorhynchiid

tapeworm. South African Journal of Science 79: 473.

Jones, M. & Beveridge, I. 1998. Nybelinia queenslandensis sp. nov. (Cestoda:

Trypanorhyncha) parasitic in Carcharhinus melanopterus, from Australia, with

observations on the fine structure of the scolex including the rhyncheal system. Folia

Parasitologica 45: 295-311.

Kikuchi, Y., Takenouchi, T., Kamiya, M. & Ozaki, H. 1981. Trypanorhynchiid

cestode larva found on the human palatine tonsil. Japanese Journal of Parasitology

30: 497-499.

Linton, E. 1924. Notes on cestode parasites of sharks and skates. Proceedings of the

United States National Museum 64: 1-114.

Oshmarin, P. G., Parukhin, A. M., Mamaev, Y. L. & Baeva, O. M. 1961. On

infection of walleye pollock with Nybelinia larvae and the utilization of this fish as

food. Soobschcheniya Dal ‘nevostochnogo Filiala Sibirskogo Otdeleniya Akademii

Nauk SSSR, No. 14, 77-80 (Transl. From Russian by Fisheries Research Board of

Canada, Translation Series No. 709, 1966).

Palm, H.W. 1992. Identifizierung und Quantifizierung von Bandwurmlarven bei

Fischen aus verschiedenen Regionen des Atlantiks. M.Sc. thesis University Kiel,

120 S.

— 1995. Untersuchungen zur Systematik von Riisselbandwiirmern (Cestoda:

Trypanorhyncha) aus atlantischen Fischen. Berichte aus dem Institut fiir Meereskunde

Kiel 275: 1-238.

1997a. An alternative classification of trypanorhynch cestodes considering the

tentacular armature as being of limited importance. Systematic Parasitology 37: 81—

92.

1997b. Trypanorhynch cestodes of commercial fishes from northeast Brazilian

coastal waters. Memoires Instituto Oswaldo Cruz, Rio de Janeiro 92: 69-79.

—— & Overstreet, R. in press. Ofobothrium cysticum (Cestoda: Trypanorhyncha)

from the muscle of butterfishes (Stromateidae). Parasitology Research.

& Walter, T. 1999. Nybelinia southwelli sp. nov. (Cestoda: Trypanorhyncha) with

the re-description of N. perideraeus (Shipley & Hornell, 1906) and the synonymy of

N. herdmani (Shipley & Hornell, 1906) with Kotorella pronosoma (Stossich, 1901).

Bulletin of the Natural History Museum London (Zoology series) 65(2): 123-131.

, Walter, T., Schwerdtfeger, G. & Reimer, L.W. 1997. Nybelinia Poche, 1926

(Cestoda: Trypanorhyncha) from the Mocambique coast, with description of N.

beveridgei sp. nov. and systematic consideration on the genus. South African Journal

of Marine Science 18: 273-285.

, Reimann, N., Spindler, M. & Plotz, J. 1998. The role of the rock cod Notothenia

coriiceps in the life cycles of Antarctic parasites. Polar Biology 19: 399-406.

Pintner, T. 1927. Kritische Beitraege zum System der Tetrarhynchen. Zoologische

Jahrbiicher 53: 559-590.

—— 1929. Tetrarhynchen von den Forschungsreisen des Dr. Sixten Bock. Géteborgs

Kunglige Vetenskaps och Vitterhets Samhdlles Handlingar, Serie B, 1: 1-48.

Rego, A. A. & Dias, A. P. L. 1976. Estudos de cestoides de peixes do Brasil, 3.a Nota:

Cestoides de raias fluviais Paratrygonidae. Revista Brasileira de Biologia 36: 941-

956.

Reimer, L.W. 1980. Larven der Ordnung Trypanorhyncha (Cestoda) aus Teleostiern

des Indischen Ozeans. Angewandte Parasitologie 21: 221-231.

Sakanari, J.A. & Moser, M. 1989. Complete life cycle of the elasmobranch cestode,

Lacistorhynchus dollfusi Beveridge and Sakanari, 1987 (Trypanorhyncha). Journal

of Parasitology 75: 806-808.

Shipley, A.E. & Hornell, J. 1906. Report on the cestode and nematode parasites from

the marine fishes of Ceylon. Report to the Goverment of Ceylon on the Pearl Oyster

Fisheries of the Gulf of Manaar, Part 5: 43-96.

Southwell, T. 1929. A monograph on cestodes of the order Trypanorhyncha from

Ceylon and India, Part 1. Ceylon Journal of Science, Section B, 15: 169-317.

Shulman, S.S. 1957. Material on the parasitofauna of lampreys from the basins of the

Baltic and the White Seas. /zvvestiya Gosudarstvennogo Nauchno-Isseldovatel ‘skogo

Instituta Ozernogo T Rechnogo Rybnogo Khozyaista 42: 282-298 (Translated from

the Russian by the Israel program for scientific translations, No. 105, 1961).

Vijayalakshmi, C., Vijayalakshmi, J. & Gangadharam T. 1996. Some trypanorhynch

cestodes from the shark Scoliodon palasorrah (Cuvier) with the description of a new

species, Tentacularia scoliodoni. Rivista di Parassitologia 13(57): 83-89.

‘

—oy -

Me to herge®

ory i a

iy ery ; mou)

~The T

Pa? ane

hd cst) «belie \\

La eS

0 ocyel &e

dC wat gd + Divuea

d ~~ @

Pe es

f ¥ Pr

. u bo <=

- se i\.,qphane

, » a

—

«@

Apia) A, rant

nisms ia prove tk aS

: ee ate oe a

=s6/ 15 xrtes ‘

o ee ie mf a

The Segond Ubg itt eirey i

Ty aie Aw Cees od Ueda haere

donot Deer

welirw x " Dig ties 5

aval ey

ee nie

A cul deve toner

“ony cima innphaseet aa ds

00! pale ed baeeqoi] 6 oer low Wei sid

(Mreteoat ail a gol

ane orrta-ves | Cae

% \ bd Lay? na,

Loe poet LW 24 le at hl

yl yea eg peed get +¥ oF

geet Pa aes Sy oli

aye gore pelapditn,

ay > aaa foe

— Qa,

a Legend Ae LAS ag ih

6 wegen’ vl

oo Wye’ a ete

—

a g "

- yor

—S = “=

~ *

Bull. nat. Hist. Mus. Lond. (Zool.) 65(2): 155-164

A new species of Microgale (Lipotyphla,

Tenrecidae) from isolated forest in

southwestern Madagascar.

PAULINA D. JENKINS

Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.

STEVEN M. GOODMAN

Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605 and WWF,

Aires Protégées, B.P. 738, Antananarivo (101), Madagascar.

SYNOPSIS. Anew species of Microgale is described on the basis of two specimens collected in southwestern Madagascar. This

species occurs in the Parc National de Zombitse-Vohibasia at 780 m in dry deciduous forest and in the montane habitat of the

nearby Analavelona Forest at 1050 m, characterised by a mixture of eastern (humid) and western (dry) plant species. This new

species has several distinct cranial modifications that appear to be adaptations for living in areas with semi-xeric conditions. A

considerable amount of data is available from southwestern Madagascar on local climatic changes during the Holocene. The

biogeography of this new Microgale is examined in light of these environmental vicissitudes.

RESUME. Une nouvelle espéce de Microgale est décrite sur la base de deux spécimens collectés dans le sud-ouest de

Madagascar. Cette espéce est présente dans le Parc National de Zombitse-Vohibasi 4 780 m dans les foréts séches caducifoliées

ainsi que dans |’ habitat montagneux de la Forét d’ Analavelona a 1050 m, dont les plantes sont une composition d’ espéces de I’ est

(humide) et de l’ ouest (seche). Cette nouvelle espéce présente plusieurs modifications craniennes distinctes qui semblent étre le

résultat de l’ adaptation a des zones de conditions semi-xérophiles. Des données considérables sont disponibles sur la région du

sud-ouest de Madagascar sur les changements climatiques durant le Holocéne. La biogéographie de ce nouveau Microgale est

examinée a la lumiére de ces vicissitudes environnementales.

Issued 25 November 1999

INTRODUCTION

When MacPhee (1987) conducted his revision of the shrew-tenrecs

belonging to the genus Microgale, little recently collected material

was available for study and numerous taxa were represented by

unique or small series of specimens, often poorly preserved and/or

poorly prepared. MacPhee’s work utilized the vast majority of

material available in the world’s natural history museums, which

amounted at that time to about 120 specimens. Over the past decade

there has been a renaissance in field zoological studies on Madagas-

car, often in the context of biological inventories, and a considerable

amount of new small mammal material has been obtained. For

example, the number of recently obtained Microgale specimens is

many times greater than that available for MacPhee’s revision. This

new material provides the means to clarify the relationships among

some named taxa, a redefinition of species limits, and the descrip-

tion of several new species (Jenkins 1992, 1993; Jenkins et al., 1996,

1997; Goodman and Jenkins, 1998).

During field missions in southwestern Madagascar to the Vohibasia

Forestin early 1996 and another tothe AnalavelonaForestinearly 1998

single individuals of a shrew tenrec were captured that, after compari-

son with the literature and reference collections at several museums,

could not be identified to species. Even though the animal is known

currently only from two specimens, one of which lacks an associated

skull, we feel that its unique pelage and cranial features clearly

distinguish it from known taxa and a description is provided below.

MATERIALS AND METHODS

All measurements are in millimeters (mm), with the exception of

weight which is in grams (g). Standard external measurements were

taken in the field and are defined as follows:

Ear length (E): notch at base of ear to the distalmost edge of the

pinna.

Head and body length (HB): tip of the nose to the distalmost point of

the body (at base of tail).

Hind foot length (HF): heel to tip of the longest toe (excluding claw).

Tail length (TL): base of tail (at ight angles to the body) to end of

distal-most vertebra, excluding terminal hair tuft.

Weight (Wt): taken with a Pesola spring balance to the nearest 0.5

grams (g).

Cranial measurements were taken using digital calipers or using a

microscope measuring stage. Cranial nomenclature follows that of

McDowell (1958), Meester (1963) and MacPhee (1981); dental

nomenclature that of Mills (1966), Swindler (1976), Butler and

Greenwood (1979), and MacPhee (1987). Dental notations are

given in the text in the following manner, with premaxillary and

maxillary teeth denoted by upper case, mandibular teeth by lower

case: incisor (I/i), canine (C/c), premolar (P/p), molar (M/m); thus i3

refers to the third lower incisor.

156

I Town & Site

Coast and River

Natlonal Road

Protected Area

—

Ss)

Toliara

Analavelona

Antanimen:

P.D. JENKINS AND S.M. GOODMAN

Morondava

Ankazoabo

Bo Site

‘ates ft

a =

Andranoheza f Agi

“77 Zombitse

Fig. 1 Map of southwestern Madagascar showing the positions of the Vohibasia and Analavelona forests, as well as other sites mentioned in the text.

RESULTS

Microgale nasoloi sp. nov.

Figs 2-4, 7

HOLOTYPE. FMNH 156187, field number SMG-—7875, adult fe-

male, skin, skull and skeleton. Collected by S. M. Goodman and

R. Rasoloarison on 12 January 1996. The specimen is deposited in

the Field Museum of Natural History, Chicago.

TYPE LOCALITY. Vohibasia Forest [Forét de Vohibasia], 59 km

northeast of Sakaraha, Province de Toliara, southwestern Madagas-

car, 22°27.5'S, 44°50.S'E, 780 m, in transitional dry deciduous

forest.

REFERRED MATERIAL. FMNH 161575, field number SMG—10,230,

juvenile male, skin [skull and skeleton lost]. Collected by S. M.

Goodman on 14 March 1998 in the Analavelona Forest [Forét

d’Analavelona], near Antanimena, 12.5 km northwest of

Andranoheza, 22°40.7'S, 44°11.5'E, 1050 m, on an isolated massif

with elements of eastern (humid) and western (deciduous) forests.

The specimen is currently at the Field Museum of Natural History

and will be repatriated to the Département de Biologie Animale,

Université d’ Antananarivo, Antananarivo.

DIAGNOSIS. Pelage grey. Interorbital region constricted; braincase

shallow; ectotympanic posteriorly positioned; tympanic processes

of alisphenoid and basisphenoid reduced. Roots of P2 adpressed;

M3 anteroposteriorly compressed, bucco-lingually elongated; p3

scarcely greater in size than p2.

DESCRIPTION. Based on holotype unless otherwise stated. Me-

dium sized Microgale (see Table 1), superficially mouse-like in

appearance (see Figs 2 and 7), tail thin, well-clothed with long scale

A NEW SPECIES OF Microgale (LIPOTYPHLA, TENRECIDAE) FROM ISOLATED FOREST IN SW MADAGASCAR 157

Table 1 Selected dimensions of the holotype and paratype of Microgale nasoloi compared with adult specimens of M. cowani and M. brevicaudata. Data

is presented as mean + standard deviation, followed by range, with sample size in parentheses.

M. brevicaudata

Character

HB 75.00 + 4.47

66-82 (10)

jue 35.64 + 2.84

30-41 (11)

HF 12.55 + 0.49

12-13 (11)

E 11°82 + 1.11

10-13 (11)

Wt 11.0+ 0.89

10-12.5 (6)

Condylo-incisive length 20.87 + 0.66

19.9-22.0 (12)

Upper toothrow length OS 033

8.7-10.0 (12)

Rostral breadth 3.53+0.16

3.3-3.8 (12)

Interorbital breadth 5.10 + 0.14

4.9-5.4 (12)

Braincase breadth 8.83 + 0.25

8.5—9.2 (12)

Braincase height 5.66 + 0.18

5.4-6.1 (12)

hairs, shorter than head and body (TL: HB 0.65). Pinnae large and

prominent, eyes moderately large. Hindfoot relatively short (HF:

HB 0.16). First digit of hindfoot just reaches base of second digit,

third digit longest, second and fourth subequal, both slightly longer

than fifth. Pelage soft and fine in texture, grey dorsally, grading into

darker grey ventrally; manus and pes light buffy grey; lateral portion

of rostrum from nose to eyes brown; tail grey, slightly darker above

than below, well-clothed with long scale-hairs. Hairs of dorsal

pelage grey basally, with pale buffy grey tips, intermixed with guard

hairs with grey bases, brown tops and light grey tips. Ventral pelage

with grey bases and buffy grey tips. The Analavelona specimen

differs slightly in the more pronounced buffy wash on the postero-

dorsal and ventral surfaces. Mammary formula: axial 1, abdominal

2, inguinal 1.

Skull medium in length (for dimensions see Table 1) but flattened

in appearance and with a narrowly constricted interorbital region

(see Fig. 3). Rostrum broad, parallel-sided; interorbital region shal-

low, long, very narrow and markedly concave; braincase shallow

and long, with angular supra-articular facets; lambdoid crest well

developed; occipital short, vertically inclined relative to long axis of

skull; sinus canal shallowly curved; right and left upper toothrows

from I1 to P2 sub-parallel; anterior incisive foramina very large,

posterior incisive foramina lie between anterior region of canines;

mesoptery goid region long and narrow; mesopterygoid fossa postero-

ventrally constricted by markedly inwardly curved pterygoid

processes; mandibular fossa broad and shallowly curved; tympanic

processes of alisphenoid and basisphenoid very reduced, rostral

tympanic process of petrosal reduced; ectotympanic occupies poste-

rior position within tympanic region, not in contact with entoglenoid

process of squamosal, tympanic process of alisphenoid or tympanic

process of basisphenoid. Mandible moderately robust; coronoid

process broad; angular process short and slender but dorsal surface

flattened and broad; ascending ramus robust with large dorsal and

M. cowani M. nasoloi M. nasoloi

Vohibasia Analavelona

FMNH 156187 FMNH 161575

77.78 + 5.64 81 70

68-85 (12)

65.44 + 3.00 53 62

61-71 (11)

16.03 + 0.60 13 14

15-17 (12)

14.19 + 1.42 16 16

12-17 (12)

13.75 + 0.90 14.0 5.9

12.5—15.5 (8)

22.38 + 0.44 2B)

21.4-23.0 (12)

10.73 + 0.19 10.2

10.4-11.0 (12)

2.47 + 0.85 Sil

2.3—2.6 (12)

5.23 = 0:15 43

5.0-5.6 (12)

10.07 + 0.18 9.2

9.8-10.3 (12)

6.59 + 0.14 4.9

6.4-6.8 (12)

ventral articular facets; distance between angular process and as-

cending ramus short. See Figs 3 and 4 for illustrations of the

dentition. First upper incisor (I1) robust, pro-odont, greater in crown

height than C, distostyle well developed; short diastema between I1

and [2; [2 robust, approximately equal in crown height to C, anterior

accessory cusp and distostyle well developed; [3 small, anteroflexed,

slightly taller than distostyle of 12, with which it is in contact; C

robust, with small anterior accessory cusp and distostyle; P2 small,

slightly greater in crown height than distostyle of C, with which it is

in contact, tooth with two closely adpressed roots; P3 small, slightly

greater in crown height than I3, protostyle well developed, anterior

ectostyle and distotyle present, talon reduced; P4 large, mesostyle,

anterior ectostyle and distostyle well developed, talon well devel-

oped, especially protocone; well developed, bucco-lingually

elongated talons also present on M1 to M3; M3 anteroposteriorly

compressed, bucco-lingually elongated. First lower incisor (il)

large, subequal in crown height to 12, hypoconulid (posterior acces-

sory cuspid) well developed; i2 robust, slightly greater in crown

height than c, hypoconulid well developed; i3 small, slightly greater

in crown height than hypoconulid of i2; c moderately robust, no

anterior accessory cuspid, hypoconulid present; p2 small, subequal

in crown height to 13, two roots present; p3 small, slightly greater in

crown height than p2, with small paraconid and hypoconid; p4, m1

and m2 as in other species of Microgale; m3 talonid with low

hypoconid, oblique crest and hypoconulid, and shallow talonid

basin.

DISTRIBUTION. Known only from the forests of Vohibasia and

Analavelona in southwestern Madagascar between 780 and 1050 m

(Figure 1).

ETYMOLOGY. This new species is named in honor of the late

Nasolo Rakotoarison who was Curator of Mammals at Parc

Botanique et Zoologique de Tsimbazaza, Antananarivo. Nasolo was

158 P.D. JENKINS AND S.M. GOODMAN

gee. re ~

Fig. 2 Dorsal view of skin of Microgale nasoloi (FMNH 156187).

Fig. 3 Dorsal and ventral view of skull, lateral view of skull and mandible of Microgale nasoloi (FMNH 156187).

A NEW SPECIES OF Microgale (LIPOTYPHLA, TENRECIDAE) FROM ISOLATED FOREST IN SW MADAGASCAR 159

Fig.4 Dentition of Microgale nasoloi (FMNH 156187). Buccal view of

left 11 — P2 (above), buccal view of left il — p2 (middle), lingual view of

left m3 (below). Scale = 1 mm.

passionately interested in mammals and a keen scientist and natural-

ist.

COMPARISON WITH OTHER SPECIES. Externally Microgale nasoloi

is readily distinguished from all other species of Microgale by the

distinctive soft, grey pelage. While it is similar in body size to other

medium sized species such as M. cowani Thomas, 1882, M. taiva

Major, 1896a, and M. drouhardi G. Grandidier, 1934, larger speci-

mens of M. fotsifotsy Jenkins et al., 1997 (for dimensions see

Jenkins et al., 1996, 1997) and M. brevicaudata G. Grandidier,

1899, the thin, relatively short tail, serves to distinguish it from all of

these species with the possible exceptions of M. brevicaudata and

M. cowani. In the case of the latter two species, M. brevicaudata has

a shorter tail relative to head and body and skull length than M.

nasoloi, while M. cowani has a relatively longer tail (ratio of TL:

condylo-incisive length 1.47—1.85 mean 1.70 SD 0.11 n= 10 in M.

brevicaudata; 2.28 in M. nasoloi; 2.7—3.1 mean 3.0 SD 0.13 n= 10

in M. cowani).

Microgale nasoloi differs from all other species of Microgale in

its cranial morphology, particularly the flattened appearance of the

skull, in which the shallow braincase is scarcely deeper than the

rostrum, the long and very constricted interorbital region and the

reduction of some elements of the auditory region. The presence of

a well-marked lambdoid crest is a feature shared with M. brevicaudata

and, to a greater degree, M. dobsoni Thomas, 1884 and M. talazaci

Major, 1896b. The long interorbital region, angular braincase with

prominent supra-articular facets and short vertically inclined oc-

ciput of the new species also resembles the condition in M. dobsoni

and M. talazaci.

Microgale nasoloi shows slight similarities in dentition to M.

fotsifotsy and M. soricoides Jenkins, 1993. In M. nasoloi 11 is less

robust and less pro-odont than that of M. soricoides, but more so

than in M. fotsifotsy and much more so than in other species of

Microgale; 12 is scarcely smaller than C in M. nasoloi and M.

soricoides; 13 is very small relative to I2 in M. soricoides, small in

M. nasoloi and M. fotsifotsy; C is robust but short in crown height as

in M. soricoides; P2 is small and P3 notably smaller than P4, unlike

species of Microgale other than M. dobsoni and M. talazaci.

Microgale nasoloi differs from other species of Microgale in its

bucco-lingually elongated talons of P4 to M3, and anteroposteriorly

compressed, bucco-lingually elongated M3. Relative sizes of the

teeth of the lower anterior dentition are similar to that of M.

fotsifotsy, with il and i2 subequal in crown height and 13 small,

unlike M. soricoides which has i] larger than 12.

Preliminary biomolecular analysis provides strong support for a

sister relationship between M. nasoloi and M. fotsifotsy and equally

strong support for their sister relationship with M. soricoides (Olson,

personal communication).

DISCUSSION

Ecology

Vohibasia (15,500 ha) is part of a complex of isolated forest blocks

that include Zombitse (14,200 ha) and several smaller satellite

forests (see Fig. 1; these surface area estimates are based on 1991

aerial photographs (Langrand and Goodman, 1997). These forests

are floristically transitional between eastern humid forest and west-

ern dry deciduous forest (Morat, 1973; Du Puy er al., 1994), yet

structurally they are closer to dry deciduous forest than humid forest

(Fig. 5). Other than these isolated fragments, which were once

contiguous, little remains of this transitional forest habitat in south-

western Madagascar, largely as a result of clearing and burning

forest for cattle pasture (Salomon, 1993). In 1998, these two forest

blocks and the smaller satellite site of the Isoky-Vohimena Forest,

were declared as a new reserve known as the Pare National (PN) de

Zombitse-Vohibasia.

The Vohibasia Forest generally has a relatively dense understorey,

that may at least in part be the result of regeneration after selective

removal of hardwoods a few decades ago. Average tree height is less

than 10 m (Pétignat et al., 1997). In general the woody vegetation is

not particularly spiny in comparison to sub-arid thorn scrub (spiny

bush) slightly further west and south. The soils are fine alluvial

sands from the Isalo Formation, surface water is highly seasonal,

and there is generally little or no soil humus.

The vertebrate communities inhabiting the Zombitse-Vohibasia

forests are apparently typical of those found in other arid regions.

The known small mammal community consists of five tenrecid

lipotyphlans (Jenrec ecaudatus Schreber, 1778, Setifer setosus

(Schreber, 1778), Echinops telfairi Martin, 1838, Microgale nasoloi

and Geogale aurita Milne Edwards & G. Grandidier, 1872), one

soricid (Suncus madagascariensis [Coquerel,1848]), two exotic

murine rodents (Rattus rattus (Linnaeus, 1758] and Mus musculus

Linnaeus, 1758) and two nesomyine rodents (Eliurus myoxinus

Milne Edwards, 1885 and Macrotarsomys bastardi Milne Edwards

& G. Grandidier, 1898) (Goodman & Ganzhorn, 1994; Goodman &

Rasoloarison, 1997).

To the west of the Zombitse-Vohibasia Forest, a region character-

ised by a dry climate and distinct deciduous vegetation, is the

160

P.D. JENKINS AND S.M. GOODMAN

Fig. 5 View down old road in the Vohibasia Forest that was cut for geological exploration. Note the relatively dense understorey and sandy soils lacking

leaf litter or humus. The trapping site of Microgale nasoloi was to the right of the road and about 10 m into the forest. (Photograph by S. M. Goodman).

isolated mountain of Analavelona rising to over 1300 m (FTM,

1979). On the basis of earlier botanical classifications, Humbert &

Cours Darne (1965) described the upper zone of the Analavelona

Forest as low sclerophyllous forest (‘Forét basse sclérophylle’),

surrounding areas of low-lying forests to the east (e.g. Zombitse-

Vohibasia) as dry dense forest (“forét dense séche’) and to the west

as Didiereaceae and Euphorbia bush (‘Didiéréacées et Euphorbia

haut fourré’). The nearest low sclerophyllous forest to the

Analavelona Massif is in the Isalo range, about 110 km to the east.

Thus, according to this classification the massif holds a different

flora from the immediately surrounding forests.

On the eastern side of the Analavelona Massif the foothills start at

about 600 m, and the lower limit of the forest is at about 1000 m and

runs to the upper reaches of the mountain. On the basis of botanical

research conducted in this forest by Nathalie Messmer and Pierre

Jules Rakotomalaza during the March 1998 expedition to the site, in

the lower altitudinal portion of the forest massive emergent Ficus

and Eugenia trees with diameter at breast height of 95-110 cm reach

heights of up to 25 m. The generic composition of these forest trees

indicate that the site is a mixture of eastern humid and western

deciduous forest. Considerable ground humus and leaf litter and

some epiphytic plants are present, the understorey is open and small

streams drain the steep hills. These characteristics are unlike

sclerophyllous forest, therefore the classification presented by

Humbert & Cours Darne (1965) for Analavelona is inaccurate,

although it is possible that the final summital ridge of the mountain

is dominated by sclerophyllous plants. On the basis of numerous

phytological characteristics the portion of the forest that we visited

is much closer to Humbert & Cours Darne’s mid-elevation humid

forest (‘types humides, moyenne altitude (800-1300 m)’). In sum-

mary, the forested portion of the Analavelona Massif is heterogenous

with regards to vegetative structure, particularly differences be-

tween the western and eastern slopes (Koechlin et al., 1974).

The Analavelona Massif is distinctly moister than any other

region of southwestern Madagascar that we are aware of, including

portions of the Isalo Massif. Presumably on the basis of orographic

position, Analavelona receives regular and considerable precipita-

tion and even during the dry season the summital zone is often

shrouded in mist. The extant fauna and flora contain elements that

indicate that this site may be a refuge for biota that had much more

extensive distributions in southwestern Madagascar when this re-

gion was moister in the relatively recent geological past (Raxworthy

and Nussbaum, 1997; Goodman, unpublished). The known small

mammal community of Analavelona is relatively depauperate and

consists of three tenrecid lipotyphlans (Tenrec ecaudatus, Echinops

telfairi and Microgale nasoloi), one soricid (Suncus madagas-

cariensis), one introduced murine rodent (Rattus rattus) and one

nesomyine rodent (Eliurus myoxinus) (Goodman, unpublished).

Trapping

Generally on Madagascar, pit-fall buckets have produced good

results in capturing ground-dwelling vertebrates, particularly rep-

tiles, amphibians, and lipotyphlans (Raxworthy & Nussbaum, 1994;

Goodman et al., 1996). During the April 1993 mission to the

Zombitse Forest 528 pit-fall bucket days were amassed; in January

1996 in the Vohibasia Forest, 165 pit-fall bucket days; and in March

A NEW SPECIES OF Microgale (LIPOTYPHLA, TENRECIDAE) FROM ISOLATED FOREST IN SW MADAGASCAR 161

1998 in the Analavelona Forest, 198 pit-fall bucket days (Raxworthy

et al., 1994; Goodman & Rasoloarison, 1997; Goodman, unpub-

lished). During the same periods, a combination of Sherman and

National Live traps were used for a total of 1,088 trap nights in the

Zombitse Forest, 955 trap nights in the Vohibasia Forest, and 535

trap nights in the Analavelona Forest. The only individual of M.

nasoloi taken in one of these devices in the Vohibasia Forest was in

a Sherman Live trap baited with a mixture of peanut butter and

ground corn flour placed about 1.5 m off the ground, and set about

10 m into the forest from the edge of an old road surrounded by forest

habitat. The single individual of this species obtained in the

Analavelona Forest was in a pit-fall device placed within 25 m of the

forest edge. Given the general efficiency of these two trapping

techniques in capturing a wide variety of non-volant small mam-

mals, including terrestrial and semi-arboreal lipotyphlans, it appears

that M. nasoloi is uncommon or difficult to trap with these devices.

Presumably this species also occurs in at least the nearby Zombitse

Forest and perhaps other smaller forest satellites that until their

recent fragmentation were part of an extensive area of transitional

forest. It was not found in the Isoky-Vohimena Forest (22°41.0'S,

44°49 .8'E), lying between Zombitse and the PN de |’ Isalo which was

inventoried in late January 1996.

Natural history

The lipotyphlan fauna of Madagascar is much more diverse in

humid areas of the island and only a few species have been recorded

in the drier west and southwest. Other than those species mentioned

above for the Zombitse-Vohibasia and Analavelona forests, three

others have been reported in dry areas of the island. Microgale

brevicaudata is known from the northwest possibly as far south as

Morondava or Toliara (MacPhee, 1987; Raxworthy & Nussbaum,

1994; Ganzhorn et al., 1996); M. pusilla Major, 1896a from the

Mahafaly Plateau in the extreme southwest, although this material

recovered from ow] pellets may date from a period in recent geologi-

cal times when this region was more mesic (MacPhee, 1986); and a

long-tailed Microgale associated with the longicaudata group from

near Morondava (Ade, 1996).

Little biological data may be gleaned from the capture of the two

individuals of M. nasoloi. The Vohibasia animal was a pregnant

female with two embryos in the left and one in the right oviduct; the

embryos measuring 10 mm in crown to rump length. On the basis of

embryo size, the female was near parturition at the time of capture in

mid-January. In contrast to the data available for species of Microgale

recorded from eastern humid forest, no quantitative information on

the reproductive season of small lipotyphlans is available from the

southwestern portion of the island. Nevertheless, given that in the

eastern humid forest a considerable number of Microgale species

give birth during the early portion of the rainy season, which

normally commences in late November and early December, a mid-

January date for parturition would coincide with the beginning of the

rainy season in southwestern Madagascar which tends to occur later

than in the east (Donque, 1975).

The individual from Analavelona was a male with small abdomi-

nal testes measuring 3 x 2 mm and non-convoluted epididymides.

Unfortunately, the skull is not available to assess the age of the

individual using dental characters, but on the basis of reproductive

condition this animal was probably a juvenile. Further evidence to

support this supposition is that the male is smaller than the adult

female in several external measurements and body mass, all charac-

ters that tend to vary with age. The pit-fall bucket in which the male

was captured contained the chewed remnants of beetles and cock-

roaches, which it presumably fed upon before being removed from

the trap.

The Vohibasia specimen was trapped 1.5 m above the ground ona

vine running from the soil surface to the mid-canopy at an angle of

about 15° (Fig. 6), suggesting that it must be at least competent at

scrambling along supports. Anatomically however, it does not exhibit

the features normally associated with arboreality in other members of

the genus, since the relatively short tail and hindfoot suggest a greater

affinity for a mainly terrestrial lifestyle. In the most extreme cases, M.

longicaudata Thomas, 1882 and M. principula Thomas, 1926 have

very long, naked-tipped tails approximately twice as long as head and

body length, long hindfeet, and are demonstrably able to make use of

slender supports above the ground (Goodman & Jenkins, 1998).

Caution should be exercised in attributing morphological adaptations

to particular lifestyles, since Echinops, which lacks an external tail is

nevertheless an adept climber.

The thesis expounded by Eisenberg & Gould (1970), that species

of Microgale may be divided into different locomotory classes

based on differences in tail and hindfoot length relative to head and

body length, was criticised by MacPhee (1987) because of lack of

ecological evidence. Recent direct observation, plus mainly circum-

stantial evidence from trap locations, suggest that many species of

Microgale are generalists equally at home on the ground as scram-

bling amongst lower levels of the understorey; while a few also use

additional ecological niches, suchas the long-tailed M. longicaudata

and M. principula which are adept at exploiting thinner supports

above ground level.

Microgale nasoloi exhibits some features — pale pelage, promi-

nent pinnae, short hindfoot relative to head and body length, skull

with a broad bimaxillary region, narrow interorbital constriction,

flat and broad braincase with pronounced superior articular facets

and marked lambdoid crest, well developed anterior dentition and

anteroposteriorly compressed M3 — which in combination are unique

to this species of Microgale. Many of these features are, however,

also present in the Malagasy geogaline tenrec, Geogale aurita,

while several are reminiscent of the suite of external, cranial and

dental characters which Hutterer (1986) used to define Afrosorex as

a subgenus of Crocidura (Lipotyphla: Soricidae). Species assigned

to Afrosorex inhabit savanna or forest-fringe areas and the pale

dorsal pelage coloration and prominent pinnae, shown also by

Geogale and M. nasoloi, are presumably adaptations to semi-xeric

conditions. The parallelism in dental features is possibly also an

example of similarities in dietary adaptations. One of the other three

species of Microgale known to occur in dry habitats is M.

brevicaudata, and this species also shows some features converging

on M. nasoloi, Geogale and Afrosorex. Externally all of these taxa

have prominent ears and short hindfeet, while all but M. nasoloi

have a markedly short tail, however M. brevicaudata shows none of

the craniodental features shared by M. nasoloi, Geogale, and

Afrosorex. This suggests that these shared external features are more

plastic than the cranial features and are thus more readily influenced

by the dry conditions of savanna or forest fringe habitats, or that

species such as M. brevicaudata have been adapting to dry or to less

extreme conditions for a shorter evolutionary period than others

such as M. nasoloi and Geogale.

Biogeography

Just a few kilometers from the Vohibasia Forest there is the

paleontological site of Ampoza, which has yielded a remarkable

amount of subfossil material that provides insight into environmen-

tal change in southwestern Madagascar over the past few millennia.

On the basis of current data derived from a pollen core at

Andolonomby (75 km SW from Analavelona and 140 km SW from

Fig. 6 Exact position of trap in the Vohibasia Forest that captured the

holotype specimen of Microgale nasoloi. The trap was placed about 1.5

m off the ground and the trap opening was facing the direction of the

canopy and it is most likely that the animal was descending the vine

when captured. Note the thick woody understorey of the forest.

(Photograph by S. M. Goodman).

Vohibasia), these climatic shifts involved a mesic period starting

before 5000 years Before Present (BP) and an arid period between

3500 and 2500 years BP (Burney, 1993). These proposed shifts are

mirrored in changes of species representation and habitat types of

subfossils excavated from sites in southwestern Madagascar

(Goodman & Rakotozafy, 1997) including Ampoza (Goodman, in

press). Radiocarbon dates available from Ampoza include an AMS

date of 1350 + 60 BP from a bone of Hypogeomys antimena A.

Grandidier, 1869, an endemic large rodent that no longer occurs in

the region (Goodman & Rakotondravony, 1996). Further, bone

remains of extinct giant tortoises from the site have been dated to

1910 + 120 BP (Mahé & Sordat, 1972) and 2035 + 35 BP (Burleigh

& Arnold, 1986). Although these radiocarbon dates are more recent

than Burney’s proposed period of aridification, the important point

for this discussion is that over the past few millennia there has been

significant change in the environment of the Vohibasia and

Analavelona region as reflected by the fauna.

Over the past few years a number of studies have tried to correlate

aspects of the speciation of certain Malagasy vertebrates with

vicariant events derived from information on shifts in vegetational

P.D. JENKINS AND S.M. GOODMAN

tiff

Fig. 7 Photograph of the live individual of the holotype of Microgale

nasoloi (FMNH 156187). (Photograph by J. Durbin).

communities during the Quaternary. These paleoecological extrapo-

lations are derived almost exclusively from palynological data

dating from the Holocene. In many cases several of the hypotheses

advanced seem to explain patterns of the distribution of certain taxa,

particularly those living in montane zones of the east (Carleton &

Goodman, 1996, 1998). A similar argument in the case of Microgale

nasoloi may be formulated as follows: during the recent geological

past when the region was more mesic, the distinctly more humid

forest currently restricted to the upper reaches of the Analavelona

Massif would have been more extensive, consequently, M. nasoloi

would have had a broader distribution. As the climate became drier

and the humid forest retreated towards the summital area of

Analavelona, the distribution of this animal also contracted, leaving

remnant populations at sites with suitable habitat to support it, such

as the Vohibasia Forest.

For M. nasoloi there appears to be a conflict between aspects of

morphological adaptations, namely a species adapted to semi-xeric

conditions and the above scenario associated with a more mesic

Holocene in southwestern Madagascar. Given these adaptations it is

possible that the opposite sequence took place — as more mesic forest

dominated the landscape this species was pushed into drier areas of

the southwestern Madagascar, and only after becoming more arid

was it able to colonize or recolonize this region. On the basis of very

limited information it appears that this species is forest-dwelling and

A NEW SPECIES OF Microgale (LIPOTYPHLA, TENRECIDAE) FROM ISOLATED FOREST IN SW MADAGASCAR 163

currently restricted to the forests of Analavelona and Vohibasia.

However no intensive small mammal surveys, particularly with pit-

fall traps, have been conducted in spiny bush areas of southwestern

Madagascar or the PN de! ’'Isalo and this species might have a much

broader distribution than currently known. Analavelona is a form of

mist-oasis and almost certainly a Pleistocene (or earlier) refuge for

humid forest-dwelling animals (Raxworthy & Nussbaum, 1997),

while the Vohibasia Forest shows transitional aspects between the

humid forests of the east and the deciduous forests of the west. Given

the ecological variation in this region during the Holocene and

recent times, a single coherent explanation for the distribution of this

species is not obvious. It exists in the most mesic portions of

southwestern Madagascar and is unknown from spiny bush. Perhaps

during historical periods when there was more forest cover in the

region its distribution was more widespread.

In recent years several studies have examined the phylogeny of

reputed Malagasy vertebrate adaptive radiations, often using bio-

chemical characters. Using models of genetic clocks these studies

indicate that much of the mammalian intrageneric speciation took

place during the Pliocene (Jansa et al., in press). No information is

available on the paleoecology of southwestern Madagascar dating

from the Pliocene and most of the Pleistocene. If indeed the period

in which Microgale nasoloi speciated falls within this same epoch

and was the result of some vicariant event such as a shift in

vegetational structure, we are currently unable to propose models to

put its modern distribution into any geographical context.

ACKNOWLEDGMENTS. This species was collected during a field expedi-

tion to the Vohibasia Forest sponsored by World Wide Fund for Nature

(WWE), Madagascar, to gather information on the region to help justify the

delineation of a new national park. For aid in numerous ways associated with

this mission we are grateful to Koto Bernard, Joanna Durbin, and Olivier

Langrand. Rodin Rasoloarison collaborated in the small mammal survey at

Vohibasia and played a crucial role in the discovery of this new animal.

For permits to conduct this research and the collection of specimens we are

grateful to officials of Direction des Eaux et Foréts and Association National

pour la Gestion des Aires Protégées. We thank Daniel Rakotondravony for

access to material in the collection of the Département de Biologie Animale,

Université d’ Antananarivo. The field projects were funded by grants from

NORAD to WWE and The John D. and Catherine T. MacArthur Foundation

to the Field Museum of Natural History. Bill Stanley and John Phelps helped

in numerous ways with the movement of specimens between Chicago and

London. Nathalie Messmer and Pierre Jules Rakotomalaza provided infor-

mation on their botanical studies in the Analavelona Forest. Photographs of

prepared specimens were taken by Phillip Crabb, Photographic Unit, The

Natural History Museum. We are grateful to Link Olson, University of

Chicago and Sara Churchfield, Kings College, University of London for

helpful comments and constructive criticism of the manuscript.

REFERENCES

Ade, M. 1996. Morphological observations on a Microgale specimen (Insectivora,

Tenrecidae) from western Madagascar pp. 251-255. In J. U. Ganzhorn & J.-P. Sorg

(eds.) Ecology and economy of a tropical dry forest in Madagascar. Primate Report

(46-1).

Burleigh, R. & E. N. Arnold. 1986. Age and dietary differences of recently extinct

Indian Ocean tortoises (Geochelone s. lat.) revealed by carbon isotope analysis.

Proceedings of the Royal Society of London (B) 227: 137-144.

Burney, D. A. 1993. Late Holocene environmental changes in arid southwestern

Madagascar. Quaternary Research 40: 98-106.

Butler, P.M. & M. Greenwood. 1979. Soricidae (Mammalia) from the early Pleistocene

of Olduvai Gorge, Tanzania. Zoological Journal of the Linnean Society 67: 329-379.

Carleton, M. D. & S. M. Goodman. 1996. Systematic studies of Madagascar’s

endemic rodents (Muroidea: Nesomyinae): a new genus and species from the central

highlands pp. 231—256. In S. M. Goodman (ed.), A floral and faunal inventory of the

eastern slopes of the Réserve Naturelle Intégrale d’ Andringitra, Madagascar: with

reference to elevational variation. Fieldiana: Zoology n.s. (85).

1998. New taxa of Nesomyine rodents (Muroidea: Muridae) from Madagascar’s

northern highlands, with taxonomic comments on previously described forms pp.

163-200. In S. M. Goodman (ed.), A floral and faunal inventory of the Réserve

Spéciale d’ Anjanaharibe-Sud, Madagascar: with reference to elevational variation.

Fieldiana: Zoology n.s. (90).

Coquerel, C. 1848. Note sur une espéce nouvelle de musaraigne trouvée 4 Madagascar.

Annales des Sciences Naturelles, Zoologie 9: 193-198.

Donque, G. 1975. Contribution géographique a l'étude du climat de Madagascar.

Nouvelle Imprimerie des Arts Graphiques, Antananarivo.

Du Puy, B., J. P. Abraham & A. J. Cooke. 1994. Les plantes pp. 15-29. In S. M.

Goodman & O. Langrand (eds.), Inventaire biologique, Forét de Zombitse. Recherches

pour le Développement, série Sciences biologiques, no. spécial. Centre d’ Information

et de Documentation Scientifique et Technique, Antananarivo.

Eisenberg, J.F. & E. Gould. 1970. The tenrecs: a study in mammalian behavior and

evolution. Smithsonian Contributions to Zoology (27): 1-138.

FTM. 1979. Besavoa (feuille E-56). Carte topographique au 1:100 000. Foiben-

Taosarintanin’i Madagasikara, Antananarivo.

Ganzhorn, J. U., S. Sommer, J.-P. Abraham, M. Ade, B. M. Raharivololona, E. R.

Rakotovao, C. Rakotondrasoa & R. Randriamarosoa. 1996. Mammals of the

Kirindy Forest with special emphasis on Hypogeomys antimena and the effects of

logging on the small mammal fauna pp. 215-232. In J. U. Ganzhorn & J.-P. Sorg (eds.),

Ecology and economy of a tropical dry forest in Madagascar. Primate Report (46-1).

Goodman, S. M. (in press). Holocene bird subfossils from the sites of Ampasambazimba,

Antsirabe and Ampoza, Madagascar. In N. Adams & R. Slotow (eds.), Proceedings

of the 22nd International Ornithological Congress. University of Natal, Durban.

—— & J. U. Ganzhorn 1994. Les petits mammiféres pp. 58-63. In S. M. Goodman &

O. Langrand (eds.), Inventaire biologique, Forét de Zombitse. Recherches pour le

Développement, Série Sciences biologiques, No. Spécial. Centre d’ Information et de

Documentation Scientifique et Technique, Antananarivo.

& P. D. Jenkins 1998. The insectivores of the Réserve Spéciale d’ Anjanaharibe-

Sud, Madagascar pp. 139-161. In S. M. Goodman (ed.), A floral and faunal

inventory of the Réserve Spéciale d’ Anjanaharibe-Sud, Madagascar: with reference

to elevational variation. Fieldiana: Zoology n.s. (90).

& D. Rakotondravony 1996. The Holocene distribution of Hypogeomys (Roden-

tia: Muridae: Nesomyinae) on Madagascar pp. 283-293. In W. R. Lourengo (ed.),

Biogéographie de Madagascar. ORSTOM, Paris.

& L. M. A. Rakotozafy 1997. Subfossil birds from coastal sites in western and

southwestern Madagascar: A paleoenvironmental reconstruction pp. 257—279. In S.

M. Goodman & B. D. Patterson (eds.), Natural change and human impact in

Madagascar. Smithsonian Institution Press, Washington, D.C.

— & R. Rasoloarison. 1997. Les petits mammiféres pp. 144-155. In O. Langrand &

S. M. Goodman, S. M. (eds.), Inventaire biologique Forét de Vohibasia et d’Isoky-

Vohimena. Recherches pour le Développement, Série Sciences biologiques (12).

Centre d’ Information et de Documentation Scientifique et Technique, Antananarivo.

, C. J. Raxworthy, and P. D. Jenkins. 1996. Insectivore ecology in the Réserve

Naturelle Intégrale d’Andringitra, Madagascar pp. 218-230. In S. M. Goodman

(ed.), A floral and faunal inventory of the eastern slopes of the Réserve Naturelle

Intégrale d’Andringitra, Madagascar: with reference to elevational variation.

Fieldiana: Zoology n.s. (85).

Grandidier, A. 1869. Description de quelques animaux nouveaux découverts, pendant

l'année 1869, sur la cOte ouest de Madagascar Revue et Magasin de Zoologie (2) 21:

337-342.

Grandidier, G. 1899. Description d’une nouvelle espéce d’Insectivore provenant de

Madagascar. Bulletin Muséum National d'Histoire Naturelle 5(7): 349.

1934. Deux nouveaux mammiféres insectivores de Madagascar Microgale

drouhardi et M. parvula. Bulletin Muséum National d’ Histoire Naturelle (2) 6: 474—

477.

Humbert, H. & G. Cours Darne. 1965. Carte internationale du tapis végétal et des

conditions écologiques. 1 coupure spéciale au 1/1,000,000. Mangoky-Cap Ste.

Marie. Travaux de la Section Scientifique et Technique de |’Institut Francais de

Pondichéry (hors série).

Hutterer, R. 1986. African shrews allied to Crocidura fischeri: taxonomy, distribution

and relationships. Cimbebesia (A) 8: 23-35.

Jansa, S. A., S. M. Goodman & P. K. Tucker. (in press). Molecular phylogeny and

biogeography of the native rodents of Madagascar (Muridae, Nesomyinae): a test of

the single-origin hypothesis. Cladisitics.

Jenkins, P. D. 1992. Description of anew species of Microgale (Insectivora: Tenrecidae)

from eastern Madagascar. Bulletin of the British Museum Natural History (Zoology)

58: 53-59.

1993. A new species of Microgale (Insectivora: Tenrecidae) from eastern Mada-

gascar with an unusual dentition. American Museum Novitates (3067): 1-11.

,S. M. Goodman & C. J. Raxworthy. 1996. The shrew tenrecs (Microgale) of the

Réserve Naturelle Intégrale d’Andringitra, Madagascar pp. 191-217. In S. M.

Goodman (ed.), A floral and faunal inventory of the eastern slopes of the Réserve

164

Naturelle Intégrale d’ Andringitra, Madagascar: with reference to elevational varia-

tion. Fieldiana: Zoology n.s. (85).

, C. J. Raxworthy & R. A. Nussbaum. 1997. A new species of Microgale

(Insectivora, Tenrecidae), with comments on the status of four other taxa of shrew

tenrecs. Bulletin of the Natural History Museum London (Zoology) 63: 1-12.

Koechlin, J., J.-L. Guillaumet & P. Morat. 1974. Flore et végétation de Madagascar.

J. Cramer, Vaduz.

Langrand, O. & S. M. Goodman (eds.), 1997. Inventaire biologique Forét de

Vohibasia et d’Isoky-Vohimena. Recherches pour le Développement, Série Sciences

biologiques (12). Centre d’Information et de Documentation Scientifique et Tech-

nique, Antananarivo.

Linnaeus, C. 1758. Systema Naturae. 10th edition. Holmiae.

MacPhee, R. D. E. 1981. Auditory regions of Primates and eutherian insectivores.

Morphology, ontogeny and character analysis. Contributions to Primatology (18): i-

xv, 1-282.

1986. Environment, extinction, and Holocene vertebrate localities in southern

Madagascar. National Geographic Research 2: 441-455.

1987. The shrew tenrecs of Madagascar: systematic revision and holocene

distribution of Microgale (Tenrecidae, Insectivora). American Museum Novitates

(2889): 1-45.

Mahé, J. & M. Sourdat. 1972. Sur l’extinction des Vertébrés subfossiles et

Varidification du climat dans le Sud-Ouest de Madagascar. Bulletin de la Société

Géologique de France 14: 295-309.

Major, C. I. Forsyth 1896a. Descriptions of four additional new mammals from

Madagascar. Annals and Magazine of Natural History (6) 18: 461-463.

1896b. Diagnoses of four additional new mammals from Madagascar. Annals and

Magazine of Natural History (6) 18: 319-325.

Martin, W. 1838. On a new genus of insectivorous Mammalia. Proceedings of the

Zoological Society of London: 17-19.

McDowell, S. B. 1958. The greater Antillean insectivores. Bulletin of the American

Museum of Natural History 115 (3): 117-214.

Meester, J. 1963. A systematic revision of the shrew genus Crocidura in southern

Africa. Transvaal Museum Memoir (13): 1-127.

Mills, J. R. E. 1966. The functional occlusion of the teeth of Insectivora. Journal of the

Linnean Society (Zoology) 47: 1-25.

Milne Edwards, A. 1885. Description d’une nouvelle espéce de rongeur provenant de

Madagascar. Annales des Sciences Naturelles, Zoologie et Paléontologie (6) 20

Article 1, bis: 1.

P.D. JENKINS AND S.M. GOODMAN

& A. Grandidier. 1872. Description d’un nouveau mammifére insectivore de

Madagascar (Geogale aurita). Annales des Sciences Naturelles, Zoologie (5) 15,

Article 19; 1-5.

— & 1898. Description d’une espéce nouvelle de Muridé provenant de

Madagascar. Bulletin de Muséum National d’Histoire Naturelle (1) 4: 179-

181.

Morat, P. 1973. Les savanes du sud-ouest de Madagascar. Mémoires ORSTOM

(68).

Pétignat, H., P. J. Rakotomalaza & S. Pétignat. 1997. Composition botanique et

diversité spécifique des foréts de Vohibasia, d’ Anjoho, et d’Isoky-Vohimena pp. 53—

103. In O. Langrand & S. M. Goodman (eds.), Inventaire biologique Forét de

Vohibasia et d’Isoky-Vohimena,. Recherches pour le Développement, Série Sciences

biologiques (12). Centre d’Information et de Documentation Scientifique et Tech-

nique, Antananarivo.

Raxworthy, C.J. & R. A. Nussbaum. 1994. A rainforest survey of amphibians,

reptiles and small mammals at Montagne d’ Ambre, Madagascar. Biological Conser-

vation 69: 65-73.

& 1997. Biogeographic patterns of reptiles in eastern Madagascar pp. 124—

141. InS.M. Goodman & B. D. Patterson (eds.), Natural change and human impact

in Madagascar. Smithsonian Institution Press, Washington, D.C.

, J.-B. Ramanamanjato & A. Raselimanana. 1994. Les reptiles et les amphib-

ians pp. 41-57. In S. M. Goodman, and O. Langrand (eds.), Inventaire biologique,

Forét de Zombitse, Recherches pour le Développement, Série Sciences biologiques,

No. Spécial. Centre d’Information et de Documentation Scientifique et Technique,

Antananarivo.

Salomon, J.-N. 1993. La déforestation a Madagascar une dynamique inquiétante.

Publication présentée a |’ Université d’Hiver — Aupelf-Uref, mai 1993. Université

d’ Antananarivo. Probleme de |’environnement en milieu tropical dans les iles de

louest de l’Océan Indien.

Schreber, J. C. D. yon. 1778. Die Saiigethiere in Abbildungen nach der Natur mit

Beschreibungen. Volume 3. Leipzig.

Swindler, D. R. 1976. Dentition of living primates. London: Academic Press. 308pp.

Thomas, [M. R.] O. 1882. Description of anew genus and two new species of Insectivora

from Madagascar. Journal of the Linnean Society (Zoology) 16: 319-322.

1884. Description of a new species of Microgale. Annals and Magazine of

Natural History 14: 337-338.

1926. On some small mammals from Madagascar. Annals and Magazine of

Natural History (9) 17: 250-252.

Bull. nat. Hist. Mus. Lond. (Zool.) 65(2): 165-171

Issued 25 November 1999

Modes of ear reduction in iguanian lizards

(Reptilia, Iguania); different paths to similar

ends

E.N. ARNOLD

Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD

Synopsis. New observations are presented on interspecific variation in ear structure in Phrynocephalus (Agamidae) and the

Chamaeleonidae. The tympanum has probably been obscured at least fourteen times in the [guania and more extensive ear

reduction has occurred independently at least once in each of five separate clades. Combining information on ear reduction with

estimated phylogenies of the groups concerned demonstrates that the process has been initiated in at least two quite different ways

in the Iguania. Modifications to the ear are congruent with hypotheses of phylogeny based on other characters in Tympanocryptis,

the Cophotis-Lyriocephalus-Ceratophora clade, phrynosomatid sand lizards, and to a large extent in the Chamaeleonidae. In

Phrynocephalus there is evidence that some modifications show partial reversal in one or more lineages.

INTRODUCTION

Different lineages of organisms often evolve a number of similar

traits independently, but the order in which these are assembled may

often be different, even in ecological analogues, especially if the

taxa concerned are not closely related (Arnold, 1994). This phenom-

enon of equipotentiality, where more or less the same overall

condition is reached by different routes, will be demonstrated in the

external and middle ear of iguanian lizards, using some new ana-

tomical observations and recent information on the phylogeny of

this assemblage. Reduction of the external and middle ears can be

shown to have occurred a number of times but by at least two

primary initial routes, the various changes making up the process

taking place in different sequences.

Versluys (1898) and Mertens (1971) listed cases where the tym-

panum is obscured in the [guania and more extensive ear reduction

in the group has been surveyed by Smith (1938). More recently,

Wever (1978) discussed selected instances of ear modification in

greater detail and gave information on the ability of such altered

organs to transmit sound. The present account corrects some errors

in Smith’s otherwise useful paper and describes the wide variety of

previously unreported ear conditions found in the genus

Phrynocephalus and some more modest differences among chame-

leons.

MATERIAL EXAMINED

Material examined forms part of the collection of the Natural

History Museum, London and a list of specimens checked is depos-

ited in the Reptile Section there.

NOMENCLATURE

Various changes in iguanian nomenclature have been suggested

recently and, to avoid confusion, usage in this paper will be specified

here. The use of Phrynosomatidae for what were previously infor-

mally called sceloporine iguanids (Savage, 1958), which has been

put forward by Frost and Etheridge (1989), is accepted. On the other

hand, these authors’ use of Chamaeleonidae is not followed. They

employ the name for the whole of the Acrodonta, which comprises

Chamaeleonidae in its usual sense plus what has generally been

called Agamidae, including the Uromastycidae (Borsuk-Bialynicka

& Moody, 1984).

Moody (1980) allocated the wide range of lizards which had long

usually been referred to the genus Agama to a number of separate

genera: Stellio, Agama, Xenagama, Pseudotrapelus and Trapelus.

This course was followed by several authors, but the name Ste/lio is

unavailable (Stejneger, 1933) and the group it was used to denote by

Moody is paraphyletic, comprising distinct Palaearctic and mainly

African assemblages (Joger, 1991) of which the former is probably

a clade and the members of the latter more closely related to such

taxa as Agama, Pseudotrapelus and Trapelus (personal observa-

tions). Leviton, Anderson, Adler & Minton (1992) argue for the use

of Laudakia Gray, 1845 for the Palaearctic forms, a course followed

here. The more recent suggestion (Henle, 1995), that Laudakia

should be confined to some members of this assemblage and the rest

placed in Placoderma Blyth, 1854, requires more thorough assess-

ment of the relationships of these lizards. The name Acanthocercus

Fitzinger, 1843 is available for the remainder of the forms that

Moody allocated to Stellio (see Schatti & Gasperetti, 1994; Henle,

1995; Baig & Bohme, 1997).

DISTRIBUTION OF EAR REDUCTION IN THE

IGUANIA

Basic structure of the unreduced Iguanian middle ear is shown in

Fig. 1. In extreme cases of reduction, the tympanic area is covered

by the anterior slip of the depressor mandibulae, the tympanum

itself is absent and the columella becomes more robust. The distal

part of the extracolumella may virtually disappear while at the same

time its attachments to surrounding structures are thickened and

sometimes ossified. These attachments are the internal or quadrate

process, connecting to the lower quadrate bone, and the dorsal

process which may connect to the paroccipital process, the interca-

lary ligament, or both.

At least some reduction of the ear occurs within the following

apparently holophyletic groups of the Iguania.

166

squamosal

extracolumella depressor

mandibulae

muscle

quadrate

mandible

ee ae a

E.N. ARNOLD

Pars superior

foot plate

extracolumella

eral columella

Pars inferior process

middle ear

cavity

quadrate

tympanum

Fig. 1 General structure of the ear in Iguania. a. Lateral view of left ear, tympanum stippled. b. Transverse section of left ear. Figures based on those of

Baird (1970).

Australian agamids

(Fig. 2)

Among Australian agamids of Group 3 (Moody, 1980), ear modifi-

cation has occurred independently in Ctenophorus maculosus

(Mitchell, 1948) and in all the species of Tympanocryptis Peters,

1863, except T: adelaidensis and T. diemensis (data from Cogger,

1992). In Ctenophorus maculosus and the Tympanocryptis parviceps

Storr, 1964 group the ear is covered with scaly skin but the tympa-

num is present just beneath it (Greer, 1989). In the Tympanocryptis

lineata group (species examined: T. lineata Peters, 1863, T: intima

Mitchell, 1948 and T: cephalus Giinther, 1867) further reduction has

occurred. The anterior slip of the m. depressor mandibulae, has

moved forwards beneath the skin to cover the tympanic area, the

columella is more robust, no clear tympanum exists, the

extracolumella is reduced to a small projection, and the dorsal and

internal processes are robust and sometimes ossified. The middle ear

opens broadly into the buccal cavity in T. lineata and T. intima, but

more narrowly in T. cephalus.

Arboreal agamids of the Oriental region

(Fig. 2)

Among mainly arboreal agamids of the Oriental region which

constitute Group 4 (Moody, 1980), a fully exposed tympanum is

lacking in some or all members of the following apparent clades

(relationships based on the weighted and unweighted Wagner tree

analyses of Moody, 1980) 1. Gonocephalus Kaup, 1805 (partly

obscured in G. miotympanum (Giinther, 1872)); 2. Japalura Gray,

1853 (some species); 3. Phoxophrys Hubrecht, 1881, 4. Otocryptis

Wagler, 1830; 5. Draco Linnaeus, 1758 (some species); 6.

Ptycholaemus Peters, 1864; 7. Aphionotis Peters, 1864, Ceratophora

Gray, 1834, Cophotis Peters, 1861 and Lyriocephalus Merrem,

1820; and 8. Oriocalotes Giinther, 1864 (some individuals).

The tympanum consequently may have become obscured at least

eight times in the Oriental assemblage (although Phoxophrys and

Otocryptis could represent a single origin if reversal occurred in

Sitana, the apparent sister group of the latter genus). In groups

where members vary in the degree to which the tympanum is

obscured, such as Draco, Japalura and Oriocalotes, it is apparent

that covering of the external ear has taken place by development of

scales on the tympanic surface (Fig. 5). Although most of the

Oriental taxa with hidden tympana lack the extensive modifica-

tions found in some Tympanocryptis, there may be less extreme

changes. Draco for instance has a thick columella, the stem of the

extracolumella is angled relative to this, and the air-filled space in

the middle ear is restricted; there is also a substantial loss of

sensitivity (Wever, 1978)

Only in the clade made up of Aphaniotis, Cophotis, Lyriocephalus

and Ceratophora has the process of ear modification gone further.

The relationships of this group (based on Moody, 1980) are shown

in Fig. 2. In this assemblage, the basal Aphionotis has the tympanum

covered (Fig. 5c), but little other change is apparent, apart from the

columella being robust and the exposure of the extracolumella on

the tympanum large (checked in A. acutirostris Modigliani, 1889, A.

fusca (Peters, 1864) and A. ornata Lidth de Jeude, 1893). In the

sister genera Cophotis and Lyriocephalus, the tympanum has disap-

peared and this area is covered by the anterior slip of the m.

depressor mandibulae. The pars superior of the extracolumella is

absent, the pars inferior is small and projects laterally, and the dorsal

and internal processes are robust and ossified, the former attaching

substantially to the paroccipital process. The quadrate itself is more

or less straight and without an auditory cup, while the middle ear

cavity extends laterally as far as the tympanic area and has a quite

large opening to the buccal cavity. In Ceratophora, the ear is

essentially similar (illustrated by Wever, 1978) but there are no

openings from the buccal cavity to a distinct middle ear cavity

(checked on C. aspera Giinther, 1864, C. stoddarti Gray, 1834 and

C. tennentii Giinther, 1861).

Smith (1938) erroneously attributed a highly modified middle ear

structure to Aphaniotis and also incorrectly described the middle ear

openings to the buccal cavity of this genus, Cophotis and

Lyriocephalus as being strongly reduced.

EAR REDUCTION IN IGUANIAN LIZARDS

Tympanocryptis Oriental agamids

T. cephalus Ceratophora

T. lineata Lyriocephalus

T. intima Cophotis

T. parviceps Aphianotis

2b 2b

T. adelaidensis Primitive oriental

T. diemensis agamids

Fig. 2 Pattern of ear reduction in Tympanocryptis (Agamidae).

and in the clade made up of Aphaniotis, Lyriocephalus, Cophotis and

Ceratophora (Agamidae).

Abbreviations: 1. depressor mandibulae moves forwards, a - slightly, b.

extensively. 2. Tympanum covered, largely -a, entirely - b; 3. columella

robust. 4. tympanum disappears. 5. buccal opening to the middle ear

reduced, a - somewhat, b - strongly, c - very small or absent. 6. Pars

inferior of extracolumella reduced, a - somewhat, b - strongly or absent.

Cophosaurus Holbrookia

1a 1b

Fig. 4 Pattern of ear reduction in phrynosomatid sand lizards

(Phrynosomatidae). For abbreviations see Fig. 2.

P. vlangali

P. theobaldi

P. roborowski P. axillaris

6a 6a

5b 5b

Most species

P. arabicus

P. maculatus

P. mystaceus

Bufoniceps

Trapelus

Fig. 3 Pattern of ear reduction in Phrynocephalus and its relatives

(Agamidae). For abbreviations see Fig. 2.

167

168

E.N. ARNOLD

Fig. 5 Stages in reduction of the external ear in Oriental agamids. a. tympanum superficial and exposed, Japalura dymondi, BMNH 1914.3.2.2.;

tympanum indicated by a depression but covered with scales, Japalura polgyonata ishikagiensis, BMNH 1913.3.10.9; tympanic area scarcely sunk and

covered with unmodified skin, Aphaniotis fusca, BMNH 1886.12.28.12-13.

Phrynocephalus and its relatives

(Fig. 3)

Moody (1980), on the basis of his morphological study of the

Agamidae, regarded Phrynocephalus as the sister group of Laudakia

plus Acanthocercus and a relationship to Laudakia has also been

supported by immunological evidence (Joger, 1991). However, a

more detailed anatomical investigation (in progress) suggests that

Phrynocephalus is the sister group of Bufoniceps Arnold, 1992 (a

new generic allocation for Phrynocephalus laungwalaensis Sharma,

1978) and successively more distant relatives are Trapelus,

Pseudotrapelus, various African taxa the relationships of which are

yet to be fully resolved including Agama, Xenagama and species

assigned to Acanthocercus, and then Laudakia (Fig. 3) This hypoth-

esis of relationships is used in the following reconstruction of the

history of earreduction in the group. However, evenif Phrynocephalus

plus Bufoniceps is regarded as the sister group of Laudakia, only

evidence for the initial changes in stage 1 below would be lost.

An estimate of Phrynocephalus phylogeny based on morphology

(Arnold, 1999) suggests that successive branches on the main

lineage are: P. mystaceus; P. maculatus; P. arabicus; the P.

interscapularis group (P. interscapularis, P. sogdianus, P. ornatus,

P. clarkorum, P. luteoguttatus and P. euptilopus); P. scutellatus; P.

golubevi: P. reticulatus; P. raddei; there is then a large clade made up

of most of the remaining species. Within the latter assemblage, little

robust phylogenetic structure is apparent but P. roborowski, P.

theobaldi and P. vlangali are clearly closely related to each other and

perhaps more distantly to P. forsythi.

1. Insome Trapelus, the anterior slip of the m. depressor mandibulae

moves anteriorly to partly obscure the tympanum, producing a

short meatus with a small opening (Fig. 6b; at the same time the

bar-like, superficial part of the extracolumella becomes more

horizontal.

2. In Bufoniceps, the tympanum is directed more posteriorly, the m.

depressor mandibulae moves further forward and the meatus and

its surface opening become very narrow (Fig. 6c), so that its

depth is several times the width of the latter.

3. In all Phrynocephalus, the tympanic area is entirely covered by

skin (Fig. 6d) and substantially by the m. depressor mandibulae.

In P. mystaceus, there 1s still a well defined tympanum incorpo-

rating a extracolumella which lacks the pars superior, but the pars

inferior is large and overlaps the conch of the quadrate. The

dorsal process is long and joins the intercalary cartilage, and the

internal process is quite slender. The buccal opening to the

middle ear is large and extends from the back of the basisphenoid

process well beyond the spheno-occipital tubercle of the basi-

occipital bone; its greatest dimension is over 25% of the head

length in small specimens.

EAR REDUCTION IN IGUANIAN LIZARDS

169

Fig. 6 Stages in reduction of external ear in the clade containing Phrynocephalus. a. Tympanum superficial and fully exposed, Pseudotrapelus sinaitus

(BMNH 1953.1.7.9); b. tympanum sunk and external opening of meatus so formed reduced, Trapelus agilis (BMNH 94.11.13.4); c. tympanum deeply

sunk and meatus and external opening very narrow, Bufoniceps laungwalaensis (BMNH 1975.1592); d. meatus totally closed Phrynocephalus maculatus

(BMNH 1973.2038).

4. In P. maculatus the tympanum is reduced to a delicate membrane

and, while smaller than in P. mystaceus, the extracolumella still

overlies the quadrate; the buccal opening to the middle ear is

reduced in size, its greatest dimension being about 15—20% of the

head length. P. arabicus is similar but the buccal opening is rather

smaller.

5. In most of the other species of Phrynocephalus which form a

large terminal clade, the extracolumella is very small or absent

and, if present, does not overlap the quadrate or only slightly. The

buccal opening to the middle ear is also minute or absent.

6. The only exceptions to this arrangement within the large terminal

clade of Phrynocephalus are P. roborowski, P. theobaldi, P.

vlangali and P. axillaris. These are generally similar to P.

maculatus and P. arabicus, but the entrance to the middle ear is

smaller, not extending beyond the spheno-occipital tubercle of

the basi-occipital bone, the greatest dimension being about 10—

14% of the head length. Relationships within Phrynocephalus

suggest that the condition found in these species results from

evolutionary reversal with the extracolumella increasing in size

and the buccal entrance of the middle ear re-evolving or at least

enlarging. Reversal may have occurred twice: in the common

ancestor of the first three species and perhaps independently in P.

axillaris.

Some variation also exists within Phrynocephalus in the extent to

which the anterior slip of the m. depressor mandibulae extends over

the quadrate bone and whether the dorsal and internal processes are

ossified, although this does not constitute a regular phylogenetic

pattern.

Chameleons

In chameleons, the skin over the quadrate region is more or less like

that covering surrounding areas, the tympanum has disappeared and

the m. depressor mandibulae runs close to the quadrate which is

straight; the columella is short, and the extracolumella elongate,

with a superior ligament attached to it.

Variation exists, for instance in the form of the pars inferior of the

extracolumella and the extent to which this is embedded in the m.

depressor mandibulae (Wever, 1968). There is an anterior process

extending to the flattened posterior section of the pterygoid in

Chamaeleo quilenis Bocage, 1866. C. senegalensis Daudin, 1802

and C. chamaeleon (Linnaeus, 1758) (Wever, 1978) and in C. dilepis

Leach, 1819 and Bradypodion ventrale (Gray, 1845) (personal

observations). This is lacking in Chamaeleo elliotti Giinther, 1895,

C. fischeri tavetanus Steindachner, 1891, C. hoehnelii Steindachner,

1891 and C. jacksoni Boulenger, 1896 (Wever, 1968), in the

Madagascan C. brevicornis Ginther, 1879 and C. lateralis Gray,

1831 (referred to Calumna Gray, 1865 and Furcifer Fitzinger, 1843

respectively by Klaver & Bohme, 1986), and in the dwarf

Rhampholeon brevicaudata (Matschie, 1892) and Brookesia stumpfii

Bottger, 1894 (personal observations).

170

Among the same species, the African forms assigned to Chamaeleo

Laurenti, 1763 have small but well developed buccal openings into

the middle ear, but these are less obvious although present in the two

large Madagascan forms examined. In Bradypodion ventrale there

are indentations where the openings would normally be but the

openings themselves are absent. This also true of the Rhampholeon

Giinther, 1874 and Brookesia Gray 1865 studied in which there are

not even indentations.

Ear reduction in the Phrynosomatidae

(Fig. 4)

Relationships within the Phrynosomatidae are discussed by De

Queiroz (1992) and ear structure of various members of the group is

described by Earle (1961a, b, c; 1962), Wever(1978) and Montanucci

(1987).

In Phrynosoma there is stiff skin over the tympanum and some-

times this is very like that surrounding it, but middle ear structure is

basically normal. Uma has an essentially unmodified ear, but in

Callisaurus the columella is more robust and contacts the inner edge

of the quadrate bone, while the extracolumella is more heavily built,

directed backwards and has much stronger dorsal and internal

processes; the quadrate is also somewhat modified. In Holbrookia

and Cophosaurus, there is no ear opening, the tympanum is absent

and the columella is even more robust attaching to the quadrate via

a short, broad internal process. Cophosaurus has the tympanic area

partly covered by the m. depressor mandibulae and the quadrate 1s

more or less straight instead of cup-shaped. In Holbrookia, the

extracolumella is very reduced, covering of the tympanum by

muscles is greater than in Cophosaurus but modification of the

quadrate rather less.

PATTERNS OF MODIFICATION

In summary, a limited degree of external and middle ear reduction,

including covering of the tympanum by unmodified skin, has prob-

ably occurred at least fourteen times in the Iguania. More extensive

modification has taken place in Tympanocryptis, the Cophotis-

Lyriocephalus-Ceratophora clade, Phrynocephalus, the

Chamaeleonidae and the Callisaurus-Holbrookia-Cophosaurus

clade. In all these groups, different species exhibit markedly differ-

ent degrees of modification. When these varied conditions are

plotted on phylogenies of the groups concerned (Figs 2-4), it is

possible to get some idea of the order in which particular features of

the modified ears appeared. To be able to reconstruct a complete

sequence on a lineage, the origin of each new feature must be

separated from those of others by side-branches, otherwise, recon-

struction will be impossible or incomplete (Arnold, 1994). In the

Chamaeleonidae only two basic degrees of modification exist and

only three in Tympanocryptis, in Aphionotis-Cophotis-

Lyriocephalus-Ceratophora, and in Callisaurus-Holbrookia-

Cophosaurus. In the clade containing Phrynocephalus, on the other

hand, there are at least six successive conditions.

It is apparent that the sequence of ear modification has been

different in some groups even though the end results have substan-

tial similarity. Thus, In the Oriental agamids, and Ctenophorus and

Tympanocryptis, the tympanum was first obscured by becoming

scaly (Fig. 5) and only then did other changes take place, such as the

m. depressor mandibulae moving forwards to cover the tympanic

area and the columella becoming more robust. In contrast, more

E.N. ARNOLD

basal members of the clade containing Phrynocephalus show that

movement of the depressor mandibulae muscle took place first,

creating and then narrowing a meatus (Fig. 6) and it was only when

this process was complete that the tympanum was entirely cut off

from external contact. In phrynosomatids, the earliest change in-

volved the columella and extracolumella becoming more robust,

rather than the tympanum becoming obscured. Complete closure of

the buccal opening is the final stage in the groups where it occurs

but, in the Callisaurus-Holbrookia-Cophosaurus clade, has not

taken place, even though the ear is otherwise highly modified.

The reasons for the extensive ear modification found in some

iguanians are uncertain. The ground-dwelling forms that exhibit

these conditions occur in arid areas and many of them burrow

directly into loose sand or earth. In this situation, covering or

modifying the primitively delicate tympanum and associated middle

ear structures may protect them from damage. Again, a more robust

columella with direct attachment to the quadrate may be more

efficient at transmitting low amplitude vibrations generated on or in

the substrate by predators, prey or conspecifics. Ability to detect

such vibrations sometimes has clear benefits, for instance in the

sand-burrowing Scincus scincus (Hetherington, 1989). However

these possible performance advantages seem unlikely to apply to the

various tree dwelling forms that exhibit reduction of the external and

middle ears. It might be expected that the differences, in the order in

which specific modifications of the ear appear, result from different

selective regimes or different sequences of these. However, differ-

ences in order of modification even occur between ground-dwelling

forms, in which selective regimes are likely to be similar.

USE OF THE OUTER AND MIDDLE EARS IN

THE SYSTEMATICS OF THE IGUANIA

Although loss and reduction features are often said to be of low

value in phylogeny reconstruction (see for instance Hecht and

Edwards, 1977), changes in the outer and middle ear of the Iguania

do not always fit this preconception. Obscuring of the tympanum

has occurred many times, but loss of more structure is often congru-

ent with changes in other characters within groups. Thus ear

alterations do not conflict with phylogenies based on other features

in Tympanocryptis, the Aphaniotis-Cophotis-Lyriocepalus-

Ceratophora clade and in the phrynosomatid sand-lizard group.

Similarly, there is some congruence with classifications of chamele-

ons based on lung and hemipenial structure (Klaver & Bohme,

1986). For instance within Chamaeleo the development of a ptery-

goid connection to the columella is confined to the subgenus

Chamaeleo. However, loss of a buccal opening to the middle ear

occurs in the Brookesia-Rhampholeon group but is also found in

Bradypodion which may be more closely related to other larger

chameleons (Klaver & Bohme, 1986). Although many changes in

the ear on the Phrynocephalus lineage are congruent with the

phylogeny, this group is exceptional in showing reversal in some ear

features.

REFERENCES

Arnold, E. N. 1992. The Rajasthan toad-headed lizard, Phrynocephalus laungwalaensis

(Reptilia: Agamidae), represents a new genus. Journal of Herpetology 26: 467-472.

, 1994. Do ecological analogues assemble their common features in the same

order? An investigation of regularities in evolution using sand-dwelling lizards as

examples. Philosophical Transactions of the Royal Society of London B. 344: 277—

290.

EAR REDUCTION IN IGUANIAN LIZARDS

——, 1999. Phylogenetic relationships of Toad-headed lizards (Phrynocephalus,

Agamidae) based on morphology. Bulletin of the Natural History Museum, London

(Zoology series) 65: 1-13.

Baig, K. J. & Bohme, W. 1997. Partition of the ‘stellio’ group of Agama into two

distinct genera: Acanthocercus Fitzinger 1843, and Laudakia Gray, 1845 (Sauria:

Agamidae). Herpetologia Bonnensis 1997; 21-25.

Baird, I. L. 1970. The anatomy of the reptilian ear. In C. Gans & T. S. Parsons (eds)

Biology of the Reptilia 2. Academic Press. Pp. 193-275.

Borsuk-Bialynicka, M. & Moody, S. M. 1984. Priscagaminae, a new subfamily of the

Agamidae (Sauria) from the late Cretaceous of the Gobi Desert. Acta Palaeontologica

Polonica 29: 51-81.

Cogger, H. G. 1992. Reptiles and Amphibians of Australia. Ithaca, New York: Reed

Books & Cornell University Press.

De Queiroz, K. 1992. Phylogenetic relationships and rates of allozyme evolution

among the lineages of sceloporine sand lizards. Biological Journal of the Linnean

Society 45: 333-362.

Earle, A. M. 1961a. The middle ear of Holbrookia maculata maculata, the Northern

earless lizard. Copeia 1961: 68-74.

——,, 1961b. An additional note on the ear of Holbrookia maculata. Copeia 1961:

355.

——,, 196lc. The middle ear of Holbrookia and Callisaurus. Copeia 1961: 405-410.

——,, 1962. The middle ear of the genus Uma compared to those of other sand lizards.

Copeial1962: 185-188.

Frost, D. R. & Etheridge, R. 1989. A phylogenetic analysis and taxonomy of iguanian

lizards (Reptilia: Squamata). University of Kansas Publications. Museum of Natural

History 81: 1-65.

Greer, A. E. 1989. The Biology and Evolution of Australian Lizards. Chipping Norton,

New South Wales: Surrey Beatty.

Hecht, M. K. & Edwards, J. L. 1977. The methodology of phylogenetic inferrence

above the species level. In M. K. Hecht, P. C. Goody & B. M. Hecht (eds) Major

Patterns in Vertebrate Evolution. New York and London: Plenum Press.

Henle, K. 1995. A brief review of the origin and use of ‘stellio’ in herpetology and a

171

comment on the nomenclature and taxonomy of agamids of the genus Agama (sensu

lato) (Squamata: Sauria: Agamidae). Herpetozoa 8: 3-9.

Hetherington, T. E. 1989. Use of vibratory cues for detection of insect prey by the

sandswimming lizard Scincus scincus. Animal Behaviour 37: 290-297.

Joger, U. 1991. A molecular phylogeny of the agamid lizards. Copeia 1991: 616-622.

Klaver, C. & Bohme, W. 1986. Phylogeny and classification if the Chamaeleonidae

(Sauria) with special reference to the hemipenis morphology. Bonner Zoologische

Monographien 22: |1-64.

Leviton, A. E., Anderson, S. C., Adler, K. & Minton, S. A. 1992. Handbook to Middle

East Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles.

Mertens, R. 1971. Die Riickbildung des Tympanum bei Reptilien und ihre Bezeihung

zur Lebenweise. Senckenbergiana Biologica 52: 177-191.

Montanucci, R. R. 1987. A phylogenetic study of the horned lizards, genus Phrynosoma,

based on skeletal and external morphology. Contributions to Science. Los Angeles

County Museum 390: 1-36.

Moody, S. M. 1980. Phylogenetic and historical biogeographical relationships of the

genera in the family Agamidae (Reptilia: Lacertilia). Ph.D. thesis, University of

Michigan.

Savage, J. M. 1958. The iguanid lizard genera Urosaurus and Uta, with remarks on

related groups. Zoologica, New York 43: 41-54.

Schatti, B. & Gasperetti, J. 1994. A contribution to the herpetofauna of South-west

Arabia. Fauna of Saudi Arabia 14: 348-423.

Smith, M. A. 1938. Evolutionary changes in the middle ear of certain agamid and

iguanid lizards. Proceedings of the Zoological Society of London B 108: 543-549.

Stejneger, 1933. In Smith, M. A. Some notes on the monitors. Journal of the Bombay

Natural History Society 35: 615-619.

Versluys, J. 1898. Die mittlere und aussere Ohrsphare der Lacertilia und

Rhynchocephalia. Zoologische Jahrbucher, Abteilung fur Anatomie 12: 161-406.

Wever, E. G. 1968. The ear of the chameleon: Chamaeleo senegalensis and Chamaeleo

quilensis. Journal of Experimental Biology 168: 423-436.

, 1978. The Reptile Ear, its Structure and Function. Princeton: Princeton Univer-

sity Press.

GUIDE FOR AUTHORS

Aims and scope. The Bulletin of the British Museum (Natural

History) Zoology, was established specifically to accommodate

manuscripts relevant to the Collections in the Department of Zool-

ogy. It provides an outlet for the publication of taxonomic papers

which, because of their length, prove difficult to publish elsewhere.

Preference is given to original contributions in English whose

contents are based on the Collections, or the description of speci-

mens which are being donated to enhance them. Acceptance of

manuscripts is at the discretion of the Editor, on the understanding

that they have not been submitted or published elsewhere and

become the copyright of the Trustees of the Natural History Mu-

seum. All submissions will be reviewed by at least two referees.

Submission of manuscripts. Initially three clear, complete cop-

ies should be submitted in the style and format of the Bulletin. The

text must be typed double-spaced throughout, including references,

tables and legends to figures, on one side of A4 paper with 2.5 cm

margins. All pages should be numbered consecutively, beginning

with the title page as p. 1. SI units should be used where appropriate.

Whenever possible a copy of the text, once the paper has been

accepted, should also be provided on floppy disc (see below). Discs

should only be sent after final acceptance, as papers generally need

revision after refereeing. If it is impossible to provide an appropriate

disc please ensure that the final typescript is clearly printed.

Authors are requested to ensure that their manuscripts are in final

format, because corrections at proof stage may be charged to the

author. Additions at proof stage will not normally be allowed. Page

proofs only will be sent.

Word-processor discs. _ Please follow these instructions.

1. Ensure that the disc you send contains only the final version of

the paper and is identical to the typescript.

2. Label the disc with the author’s name, title of the paper and

the word-processor programme used. Indicate whether IBM or

Apple Mac (IBM preferred).

3. Supply the file in the word-processor format; if there is a

facility to save in ASCII please submit the file in ASCII as well.

4. Specify any unusual non-keyboard characters on the front

page of the hard copy.

5. Do not right-justify the text.

6. Do not set a left-hand margin.

7. Make sure you distinguish numerals from letters, e.g. zero (0)

from O; one (1) from | (el) and I.

8. Distinguish hyphen, en rule (longer than a hyphen, used

without a space at each end to signify ‘and’ or ‘to’, e.g. the Harrison—

Nelson technique, 91-95%, and increasingly used with a space at

each end parenthetically), and em rule (longer than an en rule, used

with a space at each end parenthetically) by: hyphen, two hyphens

and three hyphens, respectively. Be consistent with rule used paren-

thetically.

9. Use two carriage returns to indicate beginnings of paragraphs.

10. Be consistent with the presentation of each grade of heading

(see Text below).

Title. The title page should be arranged with the full title; name(s)

of author(s) without academic titles; institutional address(es); sug-

gested running title; address for correspondence.

Synopsis. Each paper should have an abstract not exceeding 200

words. This should summarise the main results and conclusions of

the study, together with such other information to make it suitable

for publication in abstracting journals without change. References

must not be included in the abstract.

Text. All papers should have an Introduction, Acknowledge-

ments (where applicable) and References; Materials and Methods

should be included unless inappropriate. Other major headings are

left to the author’s discretion and the requirements of the paper,

subject to the Editors’ approval. Three levels of text headings and

sub-headings should be followed. All should be ranged left and be in

upper and lower case. Supra-generic systematic headings only

should be in capitals; generic and specific names are to be in italics,

underlined. Authorities for species names should be cited only in the

first instance. Footnotes should be avoided if at all possible.

References. References should be listed alphabetically. Authori-

ties for species names should not be included under References,

unless clarification is relevant. The author’s name, in bold and lower

case except for the initial letter, should immediately be followed by

the date after a single space. Where an author is listed more than

once, the second and subsequent entries should be denoted by a long

dash. These entries should be in date order. Joint authorship papers

follow the entries for the first author and an ‘&’ should be used

instead of ‘and’ to connect joint authors. Journal titles should be

entered in full. Examples: (i) Journals: England, K.W. 1987. Certain

Actinaria (Cnidaria, Anthozoa) from the Red Sea and tropical Indo-

Pacific Ocean. Bulletin of the British Museum (Natural History),

Zoology 53: 206-292. (ii) Books: Jeon, K.W. 1973. The Biology of

Amoeba. 628 p. Academic Press, New York & London. (iii) Articles

from books: Hartman, W.D. 1981. Form and distribution of silica in

sponges. pp. 453-493. In: Simpson, T.L. & Volcani, B.E. (eds)

Silicon and Siliceous Structures in Biological Systems. Springer-

Verlag, New York.

Tables. Each table should be typed on a separate sheet designed to

extend across a single or double column width of a Journal page. It

should have a brief specific title, be self-explanatory and be supple-

mentary to the text. Limited space in the Journal means that only

modest listing of primary data may be accepted. Lengthy material,

such as non-essential locality lists, tables of measurements or details

of mathematical derivations should be deposited in the Biological

Data Collection of the Department of Library Services, The Natural

History Museum, and reference should be made to them in the text.

Illustrations

DRAWINGS — Figures should be designed to go across single (84 mm

wide) or double (174 mm wide) column width of the Journal page,

type area 235 x 174 mm. Drawings should be in black on white stiff

card with a line weight and lettering suitable for the same reduction

throughout, ideally not more than 40%. After reduction the smallest

lettering should be not less than 10 pt (3 mm). Tracing paper should

ideally be avoided because of the possibility of shadows when

scanned. All artwork must have bulletin, author and figure number

included, outside of the image area, and must be free of pencil, glue

or tape marks.

PHOTOGRAPHS — All photographs should be prepared to the final size

of reproduction, mounted upon stiff card and labelled with press-on

lettering (eg Letraset). They can be mounted on white or black

background; a black background must be evenly black all over; any

background must be free of all pencil and glue marks within the

image area. All figures should be numbered consecutively as a

single series. Legends, brief and precise, must indicate scale and

explain symbols and letters. Photos, when components of figure-

plates should be abutted, trimmed as regular rectangles or close

trimmed up to edge of specimen. Joins etc. can be removed at the

scanning stage but at extra cost. Cropping instructions, if any, should

be indicated on an overlay or marked on a photocopy of the figure.

SIZE — Maximum size of artwork for use of flatbed scanners is A3.

Larger artwork has to be reduced photographically prior to scan-

ning, therefore adding to expense.

Symbols in text. Male and female symbols within the text should

be flagged within curly brackets to enable setter to do a swift global

search.

Reprints. 25 reprints will be provided free of charge per paper.

Orders for additional reprints can be submitted to the publisher on

the form provided with the proofs. Later orders cannot be accepted.