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Full text of "Bulletin of the Natural History Museum Zoology"

ISSN 0968-0470 



Bulletin of 

The Natural History 

Museum 






Zoology Series 



3' NOV 1999 

4 TED 




VOLUME 65 NUMBER 2 25 NOVEMBER 1999 



The Bulletin of The Natural History Museum (formerly: Bulletin of the British Museum 
(Natural History) ), instituted in 1949, is issued in four scientific series, Botany, 
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World List abbreviation: Bull. nat. Hist. Mus. Lond. (Zool.) 
© The Natural History Museum, 1999 



Zoology Series 
ISSN 0968-0470 Vol. 65, No. 2, pp. 73-171 

The Natural History Museum 

Cromwell Road 

London SW7 5BD Issued 25 November 1999 

Typeset by Ann Buchan (Typesetters), Middlesex 

Printed in Great Britain by Henry Ling Ltd., at the Dorset Press, Dorchester, Dorset 



Bull. nat. Hist. Mus. Loncl. (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 

DAVID THISTLE* 

Department of Oceanography, Florida State University, Tallahassee, FL 32306— 4320, USA 

RONY HUYS 

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



H'- 1 ^rT 



3" NOV 1993 

iD 



CONTENTS 

Introduction 74 

Materials and Methods 74 

Systematics 74 

Family Harpacticidae Dana, 1846 74 

Genus Zausodes C.B. Wilson, 1932 74 

Zausodes arenicolus C.B. Wilson, 1932 75 

Zausodes septimus Lang, 1965 81 

Genus Neozausodes gen. nov 8 1 

Neozausodes areolatus (Geddes, 1968a) comb, nov 84 

Neozausodes limigenus (Jakobi, 1954) comb, nov 89 

Neozausodes paranaguaensis (Jakobi, 1954) comb, nov 89 

Neozausodes stammeri (Jakobi, 1954) comb, nov 91 

Neozausodes sextus (Lang, 1965) comb, nov 91 

Neozausodes shulenbergeri sp. nov 91 

Genus Mucropedia gen. nov 96 

Mucropedia cookorum sp. nov 96 

Mucropedia kirstenae sp. nov 107 

Genus Archizausodes gen. nov 1 13 

Archizausodes biarticulatus (Ito, 1979) comb, nov 1 13 

Phylogeny 1 13 

Selection of outgroup 1 13 

Morphological characters 1 16 

Data matrix and analysis 1 19 

Results and discussion 119 

Status of Zausodes ductus Krishnaswamy, 1954 121 

Acknowledgements 122 

References 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 Ito, 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 ductus 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 

© The Natural History Museum, 1999 



74 



L. BOUCK, D. THISTLE AND R. HUYS 



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 is 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 etal, 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 2 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 (Shirayamae/a/., 1993) or Cobb slide frames 



(Westheide & Purschke, 1988). Drawings were prepared with a 
camera lucida on a 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)-l(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 the9P5. 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. , 1 996). 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. Antennule cf 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. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



75 



P2o" enp-2 with or without apophysis, inner seta not modified; enp- 
3 with 1 apical seta (inner one lost), outer spine not fused to segment. 
P3cf enp-2 outer distal corner not attenuated. 
Swimming leg setal formula: 



exopod 



endopod 



P2 


0.1.223 


0.1.221 [9] 
0.1.211 [cf] 


P3 


0.1.323 


1.0.221 


P4 


0.1.323 


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 1 seta lost in Z. septimus). 

Sexual dimorphism in rostrum, antennule, P2 endopod, P5, P6, 
genital segmentation and size. 



Type species. 
monotypy). 

Other species. 



Zausodes arenicolus C.B. Wilson, 1932 (by 



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 lcfdissected 
for examination. According to the USNM catalogue files the 
holotypeo* has gone missing since at least 1 983 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(4 9 9,4o*cf)in 
alcohol; from type locality; coll. C.B. Wilson, 15 August 1927; 
BMNH 1948.9.10.37. 

Gulf of Mexico: 29°5 1 'N, 84°3 1 '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 
99 9and 3cfcfin ethanol (BMNH 1999.176-187) and 29 9and 
2o"o"on slides (BMNH 1999.188-191). Deposited at the 
Smithsonian, Washington, D.C are 9 9 9 and 2o" o"in ethanol (USNM 
288445^146) and 1 9 and 2o"o" 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 urn (x = 0.499, n = 4); 
without rostrum and caudal rami: 394 um (x = 0.456, n = 4). Body 
(Figs 1 A-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 \-<\ 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 1A-B, 2C-D) approximately as long as wide, 
with 7 setae: setae I — III bare, setae IV-V bipinnate, seta VI bipinnate, 
dorsal seta (VII) carried on a biarticulate socle. Gelatinous string 
(Figs 1 A-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 1 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-[l + 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 1 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. 2 A; 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 
1 -segmented exopod and endopod; basis produced transversely, 
with proximal spinular row and 4 bipinnate setae; endopod longer 
than exopod, with 1 bare and 1 pinnate lateral seta and 6 apical setae; 
exopod with 1 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 1 bare inner seta, 1 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 1 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. 



76 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 1 7xtusod.es arenicolus C.B. Wilson, 1932 ( 9 ). A, Habitus, lateral view; B, habitus, dorsal view; C, rostrum. Scale bars = 20 \x.m. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



77 




Fig. 2 Zausodes arenicolus C.B. Wilson, 1932 ( 9 ). A, Antenna; B, antennule; C, urosome (excluding P5-bearing somite), dorsal view; D, urosome 
(excluding P5-bearing somite), ventral view; Scale bars = 20 urn. 



78 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 3 Zausodes arenicolus C.B. Wilson, 1932 ( 9 ). A, Mandible; B, maxilla; C, maxillule; D, maxilliped. Scale bars = 20 |im. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



79 




Fig. 4 Zausodes arenicolus C.B. Wilson, 1932 ( 9 ). A, P2; B, P3. Scale bars = 20 \im. 



80 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 5 Zausodes arenicolus C.B. Wilson, 1932 ( 9 ). A, P5 exopod, posterior view; B, P4; C, PI (arrow indicating rudimentary seta); D, P5, anterior view. 
Scale bars = 20 \im. 



SYSTEMATICS AND PHYLOGENY OF Z4 USODES 



81 



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- 1 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 inr.jr 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 5A,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 1 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 1 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 urn (x = 0.379 um, n = 4); 
without rostrum and caudal rami: 294 urn (x = 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, P5, 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-[l], 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 1 outer, distally pinnate seta and 1 inner, bipinnate seta; outer 
basal seta slender and arising from cylindrical process; with spinules 



around articulation with exopods. Exopod as in 9 except 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 9 . 

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 PI 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 ah, 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, 1 965 

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, 1 997). Coull 
(1971a) 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 9 (particularly segments 3-4 are dis- 
tinctly shorter in the Panama females), (3) the length of PI 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 ( 1 968a) regarded Z areolatus as morpho- 
logically closest to Z sextus. As a result 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 (cf ). A, Habitus, dorsal view; B, habitus, lateral view; C, antennule, fifth and sixth segments, anterior 
view; D, antennule, dorsal view. Scale bars = 20 |J.m. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



83 



A 



B 




Fig. 7 Zausodes arenicolus C.B. Wilson, 1932 (cf ). A, Urosome, dorsal view; B, urosome, ventral view; C, P5 exopod, posterior view; D, P5, anterior 
view; E, P2 endopod. Scale bars = 20 \\m. 



84 



L. BOUCK, D. THISTLE AND R. HUYS 



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. Antennule cf 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- ind"of 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. P2d"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. P3cfenp-2 outer distal corner not 
attenuated. 

Swimming leg setal formula: 





exopod 


endopod 




P2 


0.1.223 


0.1.221 or 0.1.121 


[9] 






0.1.211 


[(fsextus] 






0.311 


[cf areolatus] 






0.1.111 


[cfcf 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, nov.; Z. stammeri Jakobi, 
1954 = /V. lawmen' (Jakobi, 1954);Z sextusLzng, 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 19 and 
1 cf dissected 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 (2d" cf, 
3 9 9) from Exuma Cays, Great Guana Cay, between White Point 
and Black Point, 24°04'25"N, 76°23'45"W; 3^ 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 pm (n = 3); without rostrum and caudal rami: 



x = 561 um (n = 3). Body (Figs 8B-C, 9B-C) dorsoventrally 
flattened. Body width: x = 3 14 um (n = 3). Integumental surface (e.g. 
Al, rostrum, urosome) with areolated ornamentation/sculpturing 
(not illustrated). Sensillae present dorsally and dorsolateral^ 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-A 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 (VII) carried on a Particulate 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 1 and 2 longest; first 
segment widest with spinules; fourth segment with an aesthetasc 
(50 um 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 1 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 1 pinnate, 1 short bare, and 1 long bare seta; distal 
armature comprising 1 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 1 bare and 1 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 10E-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. 1 0D). Syncoxa with a pinnate seta and numerous 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



85 




Fig. 8 Neozausodes areolatus (Geddes, 1968a) comb. nov. ( 9 ). A, Antennule; B, habitus, dorsal view (somewhat distorted); C, habitus, lateral view. 
Scale bars = 50 pm. 



86 



L. BOUCK, D. THISTLE AND R. HUYS 




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 \im. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



87 




Fig. 10 Neozausodes areolatus (Geddes, 1968a) comb. nov. ( 9 ). A, Mandible; B, PI; C, maxillule; D, maxilliped; E, maxilla; F, maxillary endites. Scale 
bars = 20 |J.m. 



88 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 11 Neozausodes areolatus (Geddes, 1968a) comb. nov. ( 9 ). A, P2; B, P3; C, P4; D, P5. Scale bars = 20 |im. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



89 



spinular rows as indicated in Fig. 1 OD; 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. 

PI (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- 1 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. 1 ID) 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 1 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 urn (n = 2); without rostrum and caudal rami: x = 454 um (n 
= 2). Body width: x = 264 |im (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. 1 2B ) 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-[l], 3-[9], 4-[9], 5-[8 + (1 + ae) + 4 modified], 6- 
[6 + acrothek]. 

P2 (Fig. 12D) as in 9 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), PI 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; Bafa 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. 

Type LOCALITY. Brazil, Parana State; Bafa 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 



90 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 12 Neozausodes areolatus (Geddes, 1968a) comb. nov. (cf ). 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 |im. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



91 



former Zausodes complex displays such kind of sexual dimorphism, 
we regard this observation as extremely doubtful. The first exopod 
segment of legs 2-A 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. 

TYPE locality. 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 
( 1 98 1 ) [ecology]. Zausodes arenicolus sensu Varon & Thistle ( 1 988 ) 
[ecology]. 

Type locality. Gulf of Mexico: 29°5 1 'N, 84°3 1 "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 1 50 m to the north; see Foy & Thistle 
(1991 ) for additional description. 

Material examined. 

The Natural History Museum: holotype9in alcohol (BMNH 
1999. 192); allotypic paratypecfin alcohol (BMNH 1999. 193); other 
paratypesare 1 9 methanol (BMNH 1999. 194) and 2 9 9and2cfcfon 
slides (BMNH 1999.195-198). 

National Museum of Natural History (Smithsonian Institution. 
Washington, D.C.): additional paratypes represented by 2 9 9 and 
lcfin alcohol (USNM 288448-449) and 29 9 and 2a"cfon 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 urn (x = 451 urn, n = 4): 
without rostrum and caudal rami: 411 urn (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 
dorsolateral^ 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 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 partially ex- 
posed in dorsal aspect; with ventral pore near posterior margin; anal 
operculum and pseudoperculum present. Caudal rami (Figs 13C-D, 
1 6A,C) approximately as long as wide, with 7 setae: setae I — III bare, 
setae IV-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. 1 3 A) 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 1 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 1 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 + 1 unipinnate + (1 + ae)], 5-[l + 1 unipinnate], 6-[6 + 2 
pinnate], 7-[5 + acrothek]. 

Antenna (Fig. 1 3B). 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. 1 long and 1 short seta; distal armature comprising 1 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 1 -segmented with 1 lateral short seta and 1 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 1 bare and 1 pinnate lateral setae 
and 6 apical setae; exopod with 1 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 1 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 1 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. 

PI (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. ( 9 ). A, Rostrum; B, antenna; C, habitus, dorsal view; D, habitus, lateral view. Scale bars = 20 urn. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



93 




Fig. 14 Neozausodes shulenbergeri sp. nov. ( 9 ). A, Antennule (disarticulated); B, antennule (armature omitted); C, maxilla; D, maxillule; E, mandible; F, 
maxilliped. Scale bars = 10 |Jm. 



94 



L. BOUCK, D. THISTLE AND R. HUYS 










Fig. 15 Neozausodes shulenbergeri sp. nov. ( 9 ). A, P2; B, P3; C, PI ; D, P5. Scale bars = 20 |im. 



SYSTEM ATICS AND PHYLOGENY OF ZA USODES 



95 




Fig. 16 Neozausodes shulenbergeri sp. nov. ( 9 ). A, Urosome (excluding P5-bearing somite), dorsal view; B, P4; C, urosome (excluding P5-bearing 
somite), ventral view. Scale bars = 20 \im. 



96 



L. BOUCK, D. THISTLE AND R. HUYS 



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, 1 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 : 4 1 1 |im (x = 398 p.m, n = 4) ; without 
rostrum and caudal rami: 367 urn (x = 362 urn, n = 4). Body width: 
1 89 urn (x = 1 87 urn, 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. 18 A) 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 urn long), 3 modified elements, and anterior distal corner 
produced into blunt apophysis; with armature formula 1-[1], 2-[l], 
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 1 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 1 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. 



P6 (Fig. 1 8C) 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 PI endopod and the P5 
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 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. Antennulecfwithout 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 9 enp-2 without inner seta. P4 exp-3 with 2 outer spines 
in 9 and 3 outer spines incf . P4 enp-3 (or enp-2 when 2-segmented) 
with 2 inner setae in both sexes. P2d"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. P3 cf enp-2 outer distal 
corner attenuated. 

Swimming leg setal formula: 





exopod 


endopod 


P2 


0.1.223 


0.1.221 [9] 
0.1.211 [Cf] 


P3 


0.1.323 


1.0.221 


P4 


0.1.322 [9] 
0.1.323 [cf] 


1.0.221 or 1.221 



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. 

Type LOCALITY. Gulf of Mexico: 29°40.63'N, 84°22.80'W, north- 
ern Gulf of Mexico, 18m depth, unvegetated medium sand; see 
Thistle et al. (1995) for additional description. 

Material examined. 

The Natural History Museum: holotype9in alcohol (BMNH 
1999. 199); allotypic paratypecf in alcohol (BMNH 1999.200); other 
paratypes are 29 9 and lcTin ethanol (BMNH 1999.201-203) and 
29 9 and 2d"cfon slides (BMNH 1999.204-207). 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



97 




Fig. 17 Neozausodes shulenbergeri sp. nov. ((f). A, Habitus, dorsal view; B, habitus, lateral view; C, P2 endopod; D, rostrum. Scale bars = 10 um. 



98 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 18 Neozausodes shulenbergeri sp. nov. (cf). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding PS- 
bearing somite), ventral view; D, P5. Scale bars = 20 |im. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



99 



National Museum of Natural History (Smithsonian Institution, 
Washington, D.C): additional paratypes represented by 3 9 9 and 
2a"cfin alcohol (USNM 288452^153) and 19and lcfon slides 

(USNM 2888450^51). 

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 urn, n = 4); 
without rostrum and caudal rami: 257 um (x = 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^ 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 I V-V bipinnate, seta VI bipinnate. 
dorsal seta (VII) carried on a Particulate socle. Gelatinous string 
extending posteriorly from each caudal ramus present in some 
specimens. 

Rostrum (Fig. 1 9C) 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 1 and 2 longest; 
first segment widest with spinules; fourth segment with an aesthetasc 
(50 um long); apical acrothek probably consisting of 2 setae and 1 
aesthetasc, however, we were unable to distinguish which elements 
were setae and which was an aesthetasc; with setal formula l-[ 1 ], 2- 
[10], 3-[9], 4-[4 + (1 + ae)], 5-[2], 6-[4], 7-[4], 8-[4 + acrothek]. 

Antenna (Fig. 21 A). Coxa short and unomamented; 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 1 
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 1 lateral seta and 1 bipinnate distal seta and 
exp-2 with 2 distal setae. 

Labrum well developed, not medially incised. 

Mandible ( Fig. 2 1 B ) . 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 1 inner seta and 3 distal setae. 



Maxilla (Fig. 2 1 E). Syncoxa with 3 endites; praecoxal endite with 
4 setae; coxal endites each with 2 bare setae and 1 pinnate seta; 
allobasis with claw, 1 pinnate and 2 bare setae; endopod 1 -seg- 
mented with 5 bare setae. 

Maxilliped(Fig. 2 ID). Syncoxa with a bipinnate seta and numer- 
ous spinular rows as indicated in Fig. 2 ID; basis with a row of fine 
spinules and seta at distal palmar margin; endopod represented by 
acutely recurved claw with a proximal accessory seta. 

PI (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- 1 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- 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 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 1 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 1 inner. 1 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 u.m, n = 4). Body width: 
1 19 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 umlong); with armature formula l-[l],2-[l],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. (9). A, habitus, dorsal view; B, habitus, lateral view; C, rostrum. Scale bars = 20 p.m. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



101 




Fig. 20 Mucropedia cookorum sp. nov. ( 9 ). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing 
somite), ventral view. Scale bars = 20 |im. 



102 



L. BOUCK, D. THISTLE AND R. HUYS 







Fig. 21 Mucropedia cookorum sp. nov. ( 9 ). A, Antenna; B, mandible; C, maxillule; D, maxiliped; E, maxilla. Scale bars = 20 \im. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



103 




Fig. 22 Mucropedia cookorum sp. nov. A, 9P2; B, 9P3; C, 9P1; D,cfP2 endopod; E,cfP3 endopod, second segment. Scale bars = 20 ^m. 



104 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 23 Mucropedia cookorum sp. nov. A, 9 P5 exopod, posterior; B, 9 P5, anterior; C, 9 P4; D,cf P5 exopod, posterior; E,cfP5, anterior; F,cf P4 exopod, 
third segment. Scale bars = 20 |om. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



105 



.w 




Fig. 24 Mucropedia cookorum sp. nov. (cf ). A, Habitus, dorsal view; B, habitus, lateral view; C, rostrum. Scale bars = 20 \xm. 



106 



L. BOUCK, D. THISTLE AND R. HUYS 







Fig. 25 Mucropedia cookorum sp. nov. (cf). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing 
somite), ventral view. Scale bars = 20 |im. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



107 



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 9 , and with fewer spinular rows. 

P6 (Fig. 25C) symmetrical; with distal seta; located more laterally 
than in 9. 

ETYMOLOGY. Named in memory of Roy Cook and in honour of 
Jessie Cook, the first author's grandparents. 

Mucropedia kirstenae sp. nov. 

Type LOCALITY. 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: holotype9in alcohol (BMNH 
1999.208); allotypic paratypecfin alcohol (BMNH 1999.209); other 
paratypes are 19and lcfin ethanol (BMNH 1999.210-211) and 
29 9and 2o"cfon slides (BMNH 1999.212-215). 

National Museum of Natural History (Smithsonian Institution, 
Washington, D.C.): additional paratypes represented by 2 9 9and 
2cfcfin alcohol (USNM 288456-457) and 19 and lcfon 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 urn (x = 320 urn, 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 1-5 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 3-5 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 Particulate 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: l-[l],2-[10],3-[9],4-[4 + (l+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 



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 1 seta, 1 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 1 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 1 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 1 bare seta and 

2 pinnate setae; distal coxal endite with 2 bare setae and 1 pinnate 
seta; allobasis with claw, 1 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. 

PI (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 1 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. 



108 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 26 Mucropedia kirstenae sp. nov. ( 9 ). A, Habitus, lateral view; B, habitus, dorsal view; C, rostrum. Scale bars = 20 



urn. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



109 




Fig. 27 Mucropedia kirstenae sp. nov. ( 9 ). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing 
somite), ventral view. Scale bars = 20 |im. 



110 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 28 Mucropedia kirstenae sp. nov. ( 9 ). A, Antenna; B, mandible; C, maxillule; D, maxilliped; E, maxilla. Scale bars = 20 |im. 



SYSTEMATICS AND PHYLOGENY OF ZAUSODES 



111 




Fig. 29 Mucropedia kirstenae sp. nov. A,cfP2 endopod; B, 9 P2; C, 9 P3; D,cf P3 endopod, second segment; E, PI . Scale bars = 20 |im. 



112 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 30 Mucropedia kirstenae sp. nov. A, 9 P4; B, 9 P5 exopod, posterior view; C, 9 P5, anterior view; D,cf P4 exopod, third segment; E,cf P5 exopod, 
posterior view; F,cfP5, anterior view. Scale bars = 20 |im. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



113 



Male. Body length: measured from anterior margin of rostrum to 
posterior margin of caudal rami: 253 urn (x = 249 urn, n = 4); without 
rostrum and caudal rami: 220 urn (x = 217 um, n = 4). Body width: 
1 3 1 um (x = 1 34 um, n = 4). Not all sensillae shown in habitus views 
(Figs 31 A-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-[l], 3-[9], 4-[9], 5- 
[8 + (l +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 9 , and with fewer spinular rows. 

P6 (Fig. 32C) symmetrical; with distal seta; located more laterally 
than in 9. 

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. Antennulecfwithout 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 9 enp-2 with inner seta. P4 exp-3 with 3 outer spines in both 
sexes. P4 enp-2 with 2 inner setae in both sexes. P2cfenp-2 without 
distinct apophysis, inner seta not modified; enp-3 with 1 apical seta 
(inner one lost), outer spine fused to segment. P3c?enp-2 outer distal 
corner not attenuated. 



Swimming leg setal formula: 



exopod 



endopod 



P2 

P3 
P4 



0.1.223 

0.1.323 
0.1.323 



0.1.221 [9] 
0.1.211 [cf] 
1.1.221 
1.221 



P5 exopod elongate-oval in both sexes. P5 endopodal lobe 9 not 
developed; distal 3 inner setae rudimentary. 

Sexual dimorphism in rostrum, antennule, P2 endopod, P5, P6, 
genital segmentation and size. 

TYPE SPECIES. Zausodes biarticulatus Ito, 1979 = Archizausodes 
biarticulatus (Ito, 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 (Ito, 1979) comb. nov. 

TYPE LOCALITY. 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 PI, the transversely prolonged basis of 
P4, and the reduction of particular setae on the exopod and 
baseoendopod of 9 P5. 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 Ito 
have been added to the latter subfamily since (Noodt, 1954; Ito, 
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 PI exp-1, a well developed maxilliped and 2 setae on 
thed"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. 



114 



L. BOUCK, D. THISTLE AND R. HUYS 




Fig. 31 Mucropedia kirstenae sp. nov. (cf ). A, Habitus, lateral view; B, habitus, dorsal view; C, rostrum. Scale bars = 20 |im. 



SYSTEM ATICS AND PHYLOGENY OF ZA USODES 



115 




Fig. 32 Mucropedia kirstenae sp. nov. (cf ). A, Antennule; B, urosome (excluding P5-bearing somite), dorsal view; C, urosome (excluding P5-bearing 
somite), ventral view. Scale bars = 20 um. 



116 



L. BOUCK, D. THISTLE AND R. HUYS 



A first indication of the artificiality of Lang's subdivision was 
given by Ito (1979) who noted the similarity between the shape of 
the PI exopod of Z. biarticulatus and that of the genus Perissocope. 
Ito did not assign his species to Perissocope because it lacked the 
proximally-born inner seta on PI 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 9 with fused segments 7 and 8 (representing ancestral 
segments XXIV and XXV) forming compound double segment 
(see below: character 1); 

3. armature of PI 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 off! 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 ( 1 987). 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 



2 posterior setae. Comparison of ontogenetic studies of harpacticid 
genera possessing 9-segmented antennules such as Tigriopus (Ito, 
1970) and Harpacticus (Ito, 1971, 1976; Ito & 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 9 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 9 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 (Ito, 1980) 
and Harpacticus (e.g. Ito, 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 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



117 



Table 1 Segmentation of 9antennule (Al) 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. adiastaltits Wells have 
been corrected (see text). 







Seg 


mentation 






Armature 












Al 


A2 


A2 


P2 


P: 




P4 


arenicolus 




8 


1 


2 


0.1.223 


0.1.221 


0.1.323 


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 


2 


(2+2) 


0.1.223 


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 


0.1.323 


1.1.221 


cookorum 


[9] 
[cf] 


8 


2 


(2+2) 


0.1.223 


0.1.221 


0.1.323 


1.0.221 


0.1.322 
0.1.323 


1.221 


kirstenae 


[9] 
[cf] 


8 


2 


(2+2) 


0.1.223 


0.1.221 


0.1.323 


1.0.221 


0.1.322 
0.1.323 


1.0.221 


limigenus 




7 


1 


2 


0.1.223 


0.1.121 


0.1.323 


1.0.221 


0.1.323 


1.121 


paranaguaens 


is 


7 


1 


2 


0.1.223 


0.1.120 


0.1.323 


1.0.221 


0.1.323 


1.121 


septimus 




8 


1 


2 


0.1.223 


0.1.221 


0.1.323 


1.0.221 


0.1.323 


1.121 


sextus 




7 


1 


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 


1.121 


stammeri 




7 


1 


2 


0.1.223 


0.1.121 


0.1.323 


1.0.221 


0.1.323 


1.121 


Perissocope 






















adiastaltus 




7 


3 


(2+0+3) 


0.1.223* 


0.1.221 


0.1.323 


1.1.321 


0.1.323 


1.1.121 


biarticulatus 




8 


3 


(1+0+3) 


1.1.223 


0.1.221 


1.1.323 


1.1.321 


1.1.322 


1.1.221 



* 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 
Tighopus 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 et 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. Ito (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 PI exp-3 

The distal exopod segment of PI 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 (Ito, 1970, 1977; Ito & 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 PI enp-1 

Harpacticidae typically possess a well developed inner seta on the 
proximal endopod segment of PI. 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 1 seta on this segment (Fig. 15 A; 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. 



9 

10 
11 
12 
13 
14 
15 
16 
17 
18 
19 
20 
21 
22 
23 
24 
25 



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 9 segment 6 (or homologous portion in 6- or 7-segmented antennule) without enlarged spines [with 2 enlarged pectinate or pinnate spines] 

Antennule 9 with all elements naked (except for pinnate spines referred to in character 3) [with pinnate or plumose setae on segments 1-6] 

Antennary exopod 3-segmented [state 1: 2-segmented; state 2: 1 -segmented] 

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] 

Maxilla with 5 setae on praecoxal endite [state 1: 4 setae; state 2: 3 setae] 

PI exp-3 with 2 geniculate (hinged) and 3 simple claws [with 2 geniculate and 2 simple claws] 

PI enp-1 with long inner seta [without] 

P2 enp-3 with 2 inner setae [with 1 inner seta] 

P3 enp-2 with inner seta [without] 

P3 enp-3 with 3 inner setae [with 2 inner setae] 

P4 exp-3 with 3 outer spines in 9 [with 2 outer spines in 9 , 3 incf ] 

P4 endopod 3-segmented [2-segmented; enp-2 and -3 fused] 

P4 enp-2 (or homologous portion in 2-segmented endopod) with inner seta [without inner seta] 

P4 enp-3 (or homologous portion in 2-segmented endopod) with 2 inner setae [with 1 inner seta] 

P5 exopod oval or elongate in both sexes [round] 

P5 9 endopodal lobe expressed [completely lost] 

P5 9 endopodal lobe inner seta not distinctly shorter than other endopodal elements [rudimentary] 

P5 9 endopodal lobe 3rd and 4th setae well developed [much shorter than others] 

Antennule cf segment 3 without transformed elements [with modified spine] 

P2 enp-2cf with apophysis [secondarily lost] 

P2 enp-2cf inner element setiform, not sexually dimorphic [modified into stout spine, distinctly shorter than in 9 ] 

P2 enp-3 outer spine articulating with segment [fused to segment] 

P3 enp-2cf outer distal coiner not attenuated [attenuated] 



Table 3 Character data matrix. Characters listed in Table 2 are scored using the multistate system: = ancestral (plesiomorphic) state, 1 = derived 
(apomorphic) state, 2 = further derived state, ? = missing data, indicating that the character state is either unknown or unconfirmed. 



Character 


1 


2 


3 


4 


5 


6 


7 


8 


9 


10 


11 


12 


13 


14 


15 


16 


17 


18 


19 


20 


21 


22 


23 


24 


25 


arenicolus 











1 


2 


2 


1 





















1 











1 

















areolatus 


1 


1 


1 





2 


2 


2 




















1 


1 











1 













biarticulatus 














1 


1 


1 



























1 


1 













1 





cookorum 














1 


1 


1 













1 












1 


1 










1 


1 


1 


kirstenae 














1 


1 


1 













1 













1 


1 










1 


1 


1 


limigenus 


1 


1 


1 


? 


2 


2 


7 






1 













1 


1 











7 




7 


? 


7 


paranaguaensis 


1 


1 


1 


? 


2 


2 


? 






1 













1 


1 











7 




7 


7 


7 


Septimus 











1 


2 


2 


1 




















1 











1 
















sextus 


1 


1 


1 





2 


2 


2 




















1 


1 











1 













shulenbergeri 


1 


1 


1 





2 


2 


2 






1 













1 


1 











1 













stammeri 


1 


1 


1 


7 


2 


2 


7 






1 













1 


1 











7 


7 


7 


7 


7 


PERISSOCOPE 







































































1 


1 


cinctus 


1 











2 


2 


7 


1 


1 


























1 


? 


7 


? 


7 


7 


? 


7 



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 speciesof 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- 



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. 1 1C), 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 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



119 



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 9 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 9 endopodal lobe 

Species belonging to Perissocope and the Zausodes complex typi- 
cally have 5 well developed setae on the P5 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 (Ito, 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 
I 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 antennulecf 

Male antennules in the Harpact icidae 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. It is represented by a strong spine which is situated dorsal ly 
near the distal margin of the segment (Figs 1 2F, 1 8 A). 

(22-23) Modification P2 enp-2 cf 

The male P2 endopod is of high significance in understanding the 
phylogeny of the Harpacticidae (Ito, 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 
a similar apophysis on the male P2 endopod (e.g. Gee & Huys, 1 99 1 ; 
Huys & Gee, 1993, 1996). Within the Perissocope- Zausodes'' 
lineage the apophysis is clearly in a state of reduction. The genus 



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 thecf(character 23 in Table 3; Figs 22D, 29A). 

(24) Modification P2 enp-3 cf 

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 (Ito, 1984). In some species such as H. 
furcatus Lang the outer spine is represented by a rudimentary setule 
(Ito & 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 Ito (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 cf 

Distinct sexual dimorphism on the P3 endopod is rare in the 
Harpacticidae. Differences in surface ornamentation between the 
sexes are occasionally found in Harpacticus (Ito, 1976; Ito & 
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 a mucroniform 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: = the ancestral state, 1 = 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 



A 



24,25 



18,19,22,24 



6 a , 7 a , 8, 9, 12, 15 



1L 13,23,25 



4,20 



5,6 b , U, 16 



1,2, 3, T, 14, 17,21,22 



T.L. = 36 

CI. = 0.778 
f-value = 138 



14 



14 



14,22 



10 



PERISSOCOPE 

biarticulatus I Archizausodes gen. nov. 

kirstenae 



cookorum 

septimus 

arenicolus 

sextus 

areolatus 

limigenus 

paranaguaens is 

shulenbergeri 

stammeri 



Mucropedia gen. nov. 



Zausodes 



Neozausodes gen. nov. 



B 



5, 6 D , 11 16 



4,20 



4,20 



14,22 



1,2,3,7°, 17,21 



f-value=118 



10 



arenicolus 

septimus 

sextus 

areolatus 

limigenus 

paranaguaens is 

shulenbergeri 

stammeri 



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. 



SYSTEM ATICS AND PHYLOGENY OF ZAUSODES 



121 



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 ( 1 38), 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 PI. 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-c\ade and the sextus-c\ade. The former accommodates 
the type species and Z septimus and is characterized by the pres- 
ence of ornate setae on the 9 antennule and by the reduction of 
particular setae on the 9 P5 baseoendopod. Both species have re- 
tained primitive antennule characters such as the 8-segmented 
condition in the 9 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 9 antennule and on segment 3 of thed"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. 

Ito (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 



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. nov.) 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 P5 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 PI 
exopod is only 2-segmented and sexually dimorphic, the male 
having only 2 claws and 1 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 [21 1] 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. Ito'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 
the9P5 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 P5 of A. biarticulatus (cf. Ito, 
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 



L. BOUCK, D. THISTLE AND R. HUYS 



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 N000 14-95-1-0750 to 
D.T. 



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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 fur Meereskunde an der Universitat Kiel, 
Dusternhrooker Weg 20, D 24105 Kiel, Germany 

THORSTEN WALTER 

Marine Pathology Group, Department of Fisheries Biology, Institut fiir Meereskunde an der Universitat Kiel, 
Dusternhrooker Weg 20, D 24105 Kiel, Germany 

SYNOPSIS. During a study of Nybelinia material deposited at The Natural History Museum, London, Nybelinia southwelli sp. 
nov. was discovered amongst material identified and described as Tetrarhynchus perideraeus Shipley & Hornell, 1906 from 
Rhina ancylostoma and Nebriusfemtgineus from Sri Lanka. The new species belongs to the subgroup IIBa of Palm et al. ( 1 997). 
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 et 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 N. 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. 



© The Natural History Museum, 1999 



124 



H.W. PALM AND T. WALTER 



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 ( 1 995 , 1 997 ) 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 T. 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 ( 1 942. Figs 
98-100). Similarly, the type material of T. 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 etal., 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. 

Synonymy. 

N. perideraeus (Shipley & Hornell, 
1929a, b, 1930) 



(Figs l-3c) 



1906) of Southwell (1924, 



Material described. Holotype, BMNH 1977.1 1.4.7, J. Pearson 
leg., 30.9. 1 925, 1 adult from Rhina ancylostoma Bloch & Schneider, 
1801 (=Rhynchobatus anchylostomus) Sri Lanka (Ceylon); Paratype, 
BMNH 1977.11.4.8-9, J. Pearson /eg., 30.09.1925, 1 adult from 
Nebrius ferrugineus (Lesson, 1830) {-Gingly mo stoma 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 




Fig. 1 Scolex of Nybelinia southwelli sp. nov. from Nebrius ferrugineus. 
Scale bar=150 urn. 

bothridialis is 945 (1 134); 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: l).The tentacles are long and 
slender and diminish in size towards the tip; TW basal=46-5 1 (5 1- 
56), TW metabasal 33-38. A basal tentacular swelling is not present. 
The tentacle sheaths are sinuous or spirally coiled; TSW 66-70 (5 1- 
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(iii)) 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= 1 8-20 
(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. nov. 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 1 977. 1 1 . 1 1 .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 NYBEL1N1A SPECIES 
2a 



2b 





2c 




iii 



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 urn. 

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 1 30th 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, 25^4-2 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 N. 
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 1 and 1 2 um, 
and shape. 

The present material illustrates that the material belongs to 
Nybelinia subgroup IIBa 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 1 6. Similarly, the metabasal hooks of the holotype 
were larger. This observation can be interpreted as a record of 
morphological variability for N. 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 2 1 09 and 2 1 1 1 ; 3 adults 
from the small intestine of Glyphis gangeticus (Miiller & 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), pv=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=35^10. 

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— 1 1.5. On the antibothridial surface, the hooks are 



126 



H.W. PALM AND T. WALTER 





3c 



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 urn and scale bar c=l 10 urn. 



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— 1 1.8; 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, N. 
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 A 7 , 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 



127 




Fig. 4 Scolex of Nybelinia perideraeus sp. nov. from Glyphis gangeticus. 

Scale bar=150 urn. 



tentacular hooks by Shipley & Hornell (1906) and Pintner (1930) 
were not unambiguous, he added with his own illustrations given in 
figs 97- 1 00 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 urn, 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 lOum 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 II 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. 




5a 



5b 







> 9 «» 




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 pwnosomum (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 

MATERIAL EXAMINED. Type VNHM 2095, 1 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 




Fig. 6 Mature proglottid of Nybelinia perideraeus. Scale bar=100 um. 




Fig. 7 Scolex of Kotorella pronosoma (Nybelinia herdmani) from 
Himantura imbricata. Scale bar=150 um. 



N. herdmani are summarised in Table 1 . In addition to these data, the 
following characters were observed: The 4 bothridia of TV. 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=l 3.5-14.5, 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- 
7. 

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 35^18. The 
size of ovoid testes varies depending on number of proglottid 
(anterior proglottids: 37^-7; median proglottids: 53-64; posterior 






DESCRIPTION OF THREE NYBELIN1A SPECIES 

8a 



129 




I 




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 urn 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 
oiN. 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 l/3 rd 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 l/3 rd smaller (hooks size between 5-8 
um). 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 um (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 ( 1 989) 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= 1 00 urn. 



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 / 
Year 



Euzet & Radujkovic 
(1989) 



Shipley & Hornell 
(1906) 



Pintner 
(1930) 



Present study 



n 


2 


Scolex length: 


650 


Scolex width 1 


- 


Pars bothridialis 


380 


Pars vaginalis 


550 


Pars bulbosa 


110 


Bulb length 


100 


Bulb width 


60 


Velum 


140 


Bulb length/bulb width 


1,6: 1 


pbo/pv/pb.. 


3,5 : 5 : 1 


Tentacle length 


250-275 


Tentacle width 


12-15 



3 /4 

1000 



80-100 
Short 



900 (880) 2 — 1000 

600 (570-630) 
615(590-640) 
155(150-160) 
160(140-180) 

110(90-130) 

160(140-180) 

1,5: 1 

3,9 : 4,0 : 1 



980 (900-1060) 
374 (297-450) 
610 (570-650) 
615 (590-640) 
192(188-195) 
170(160-180) 
100(90-110) 
160(140-180) 

1,7: 1 

3,2 : 3,2 : 1 

308 (260-357) 

16-29 



1 Maximum width 

2 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 etal., 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 Tentacularia 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 



131 



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, acladistic 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 (TV. 
nipponica: 1 .35-2.9; N.karachii: 1.25-2.5 (Yamaguti, 1952, Kurshid 
& Bilqees, 1 988)), scolex width (N. beveridgei: 2. 1-3. 1 ; A 7 , 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 l/3 rd 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 et 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. 



REFERENCES 



Beveridge, I. & Campbell, R.A. 1 996. New records and descriptions of trypanorhynch 

cestodes from Australian fishes. Records of the South Australian Museum 29: 1-22. 
.Campbell, R.A. & I'uliii. II. 1999. Preliminary cladistic analysis of genera of the 

cestode order Trypanorhyncha Diesing. 1863. Systematic Parasitology 42: 29^19. 
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 Tetrarhynques. (2'contribution). Definition des genres 

(suite). Memoires de la Societe Zoologique de France 29: 139-216. 

1942. Etudes critiques sur les Tetrarhynques du Museum de Paris. Archives du 

Museum national d'Histoire Naturelle 19: 1^466. 

1960. Sur une collection de Tetrarhynques homeacanthes de la famille des 

Tentaculariidae recoltees principalement dans la region de Dakar. Bulletin de 
I'!. F.A.N. . Serie 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). Annates de Parasitologic Humaine 
el Comparee 64: 420-425. 

Jones, M. & Beveridge, I. 1998. Nybelinia queenslandensis sp. nov. (Cestoda: 
Trypanorhyncha) parasitic in Carcharhinus melanoplerus. from Australia, with 
observation on the fine structure of the scolex including the rhyncheal system. Folia 
Parasitologic^ 45: 295-3 1 1 . 

Khurshid, N. & Bilqees, F.M. 1988. Nybelinia Icarachii new species from the fish 
Cybium gutlalum of Karachi coast. Pakistan Journal of Zoology 20: 239-242. 

Palm, H.W. 1995. Llntersuchungen zur Systematik von Russelbandwurmern (Cestoda: 
Trypanorhyncha) ausatlantischenFischen. Berichtcausdein 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. 

, Mtiller, H. & Petersen, F. 1993. Otobothrium penetrans (Cestoda; 

Trypanorhyncha) in the flesh of belonid fish from Philippine waters. International 

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 Monographic der Tetrarhynchoideen. 

Sitzungsberichle der Kai.wrlich.en Akademie der Wissenschaften Wien, mathematisch- 

naturwissenschaftliche Klasse. Abteilung I. 122: 171-253. 
1930. Wenigbekanntes und Unbekanntes von Russelbandwurmern. 

Sitzungsberichle der Kaiserlichen . \ kademie der Wissenschaften Wien. malhemalisch- 

naturwissenschafllichen 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. 1 996. 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, 
II. Acta Medicinae Okavama 8: 1-76. 



Bull. nat. Hist. Mus. Land. (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 fur 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 1 7 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 & Bilqees, 1979) comb, nov.; H. estigmena 
(Dollfus, 1960) comb, nov.; H. heteromorphi sp. nov.; H. minima sp. nov.; H. robusta (Linton, 1890) comb, nov.; H. yamagutii 
(Dollfus, 1960) comb, nov.; Mixonybelinia beveridgei (Palm, Walter. Schwerdtfeger & Reimer, 1997) comb. nov. and M. 
southwelli (Palm & Walter. 1 999) comb. nov.. Tentacularia scoliodoni is transferred to the genus Nybelinia. Nine new locality and 
1 5 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 et 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, 1 906) 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- 



© The Natural History Museum, 1999 



134 



H.W. PALM 



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 (Ml 30-6)) were 
borrowed. Similarly, deposited Nybelinia species were studied in 
the Museum 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=46-5 1 . 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 th row towards the basal part of the tentacle. The size of the hooks 
also diminish slightly towards the apical end of the tentacles. The 



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. 
( 1 997) 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). N. 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 IAb 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 N. 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 1982.4.6.37^15, 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 leg., 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 with a 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 



135 





Fig. 1 Nybelinia aequidentata isolated from Lepturacanthus savala. 
Scolex. Scale bar=500 |am. 



Fig. 2 N. aequidentata. Homeomorphous metabasal armature. Scale 
bar=25 |im. 



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 



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 A 7 , 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 A', 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 1 1 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 N. africana. Mature segment. Scale bar=60 um. 





Fig. 4 Nybelinia jayapaulazariahi from Harpodon nehereus. Scolex. 
Scale bar=50um. 



Fig. 5 N. jayapaulazariahi. Homeomorphous metabasal armature with 
slender hooks, metabasal hook as given in Reimer (1980), figure 4 
(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-l 1.2; 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 urn) 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. 11-1 2, R. Bray leg., 03. 12. 1986, 
2 postlarvae from the branchial chamber of Arnoglossus imperialis, 
Cirolana 76-78 m, 49°50'5"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°50'5"N, 3°44'3"W, 
76-78 m. 

DESCRIPTION. Nybelinia 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 (112-1 17), nm;BR=2.6:l, 
2.4:1, 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=l 1.0-1 3.0, 



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 ( 1 942), the scolex 
form as well as the form and arrangement of the tentacular hooks 
correspond with drawings of A 7 , lingualis found in Sepia fdliouxi, S. 
officinalis and Mullus barbatus (see Dollfus, 1942, Figs 88-91). 
According to Dollfus (1942), the bulbs are typically short (about 
300-400 urn 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); pv=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=51-56. 
The tentacle sheaths are straight and the TSW without invaginated 
tentacles is nearly half as small (TSW=23-28) than with invaginated 
tentacles (TS W=42^16). 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. 1 1 ) 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, N. 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=l 1-12) are smaller than 
observed for the present specimens. N. lingualis corresponds with a 
similar basal armature (see above) and scolex proportions as de- 
scribed for specimens ofN. 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 



H.W. PALM 





Fig. 6 Nybelinia lingualis from Torquigener pleurogramma. Scolex. 
Scale bar=100 |im. 



Fig. 7 iV. lingualis from T. pleurogramma. Homeomorphous basal 
armature consisting of rounded hooks without anterior extension of the 
basal plate. Scale bar=10 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) 



Material examined. Holotype and paratype, BMNH 1 976. 1 .7.9, 
Hecht leg., 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=15 12, 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:l, 
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=ll-13);hsr=6-7. 



Additional material. SL=3270; SW=1020; pbo=1134; 
pv=l 172; 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=ll-13; B=ll— 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 
( 1 960) 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 



139 




Fig. 8 N. tingualis from T. pleurogramma. Homeomorphou.s metabasal 

armature. Scale bar=10 urn. 
Fig. 9 N. lingualis from T. pleurogramma. Homeomorphous apical 

armature. Scale bar=10 urn. 



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 Isurus 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=1 8.4-23.5; 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=l 1.7-13.3 (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. 10 Nybelinia riseri. Scolex from Trachyurus felicipes. Scale 
bar=100 |jm. 



Fig. 11 N. riseri. Homeomorphous basal armature consisting of rounded 
hooks without anterior extension of the basal plate. Scale bar=15 \xm. 



140 



H.W. PALM 



12 





Fig. 12 Nybelinia sakanariae sp. nov. Scolex from Xiphiurus capensis. 
Scale bar=150 |im. 



Fig. 13 N. sakanariae sp. nov. from X. capensis Homeomorphous basal 
and metabasal armature. Scale bar=20 urn. 



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 IAa of 
Palm etal.{\ 997) 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 A 7 , anthicosum and N. palliata, deposited at the 
U.S. National Parasite Collection, Beltsville, revealed differences in 
oncotaxy. N. strongyla has a much larger TW=55 and SL=2300 and 
larger hooks, and N. riseri has smaller hooks together with a larger 
TW and a different scolex form (Dollfus, 1960). N. sphyrnae and A 7 . 
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. 



8. Nybelinia scoliodoni (Vijayalakshmi, Vijayalakshmi & 
Gangadharam, 1996) comb. nov. (Tentacularia scoliodoni) 

(Figs 16-17) 

Material examined. BMNH 1976. 1 1 .5.42^13, R. van der Elst 
leg., 1 adult from the gut of Carcharhinus limbatus, South Africa. 
Additional material: NHMV 2111, A.E. Shipley leg., 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 



141 





Fig. 14 Nybelinia schmidti sp. nov. Scolex from Isurus glaucus. Scale 
bar=100|im. 



Fig. 15 N. schmidti sp. nov. Homeomorphous basal and metabasal 
armature. Scale bar=10 urn. 



and a distinctive basal armature is present (Fig. 17). The basal 
armature consists of about 1 1 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-l 1 in the basal and L=30, B=3 in the 
metabasal armature as given by Vijayalakshmi et 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 etal. (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 



limbatus is a new host for N. scoliodoni. Under the co-type material 
of Nybelinia perideraeus (Shipley & Hornell. 1906), slide No. 12f, 
an adult N. 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. scoliodoni has 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 ofN. 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 N. 
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 



H.W. PALM 



16 





Fig. 16 Nybelinia scoliodoni. Scolex from Carcharhimts limbatus. Scale 
bar=50 p.m. 



Fig. 17 N. scoliodoni. Homeomorphous basal and metabasal armature 
consisting of rose-thorn shaped and falcate hooks. Scale bar=20 urn. 




Fig. 18 N. indica. Homeomorphous basal and metabasal armature 
1992). Scale bar=20 urn. 



9. Nybelinia sp. 

Material examined. BMNH 1979.9.13.94, leg. R. vanderElst, 
2 postlarvae from the kidney of Coryphaena hippurus, Cape Vidal, 
South Africa. 

DESCRIPTION. The following measurements were taken: SL=1 172, 
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. riseri 
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 



143 



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=40^8, 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 & Bilqees, 
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 et al. 
(1997). 

10. Heteronybelinia elongata (Shah & Bilqees, 1979) 
comb. nov. (Figs 19-25) 

Material examined. Types BMNH 1989.5. 18.5, Shah & Bilqees 
leg., 1979, 2 postlarvae from Pellona elongata, Pakistan; BMNH 
1980.6.23.13, A. Roy leg., 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 & Bilqees, 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 aTW 
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 



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= 1 1 .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= 24-27.2. 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-l 1.2 (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 N. 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 N. 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 II Aa in Palm et 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. It is recommended that the type material of species 
in subgroup IIAa described by Dollfus (1960) be compared with N. 
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 1976.11.5.42^3, 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 leg; 11.05.1984, 1 adult 
from Carcharhinus leucas, Richards Bay, South Africa; BMNH 



144 




H.W. PALM 



20 




Fig. 19 Heteronybelinia elongata. Scolex from Pellona elongata. Scale 
bar=200 um. 




Fig. 20 H. elongata. Scolex from Lepturacanthus savala. Scale bar=100 
|im. 







Fig. 21 H. elongata. Scolex from L. savala. Scale bar=100 um. 



Fig. 22 H. elongata from L. savala.. Muscular ring around tentacle 
sheath. Scale bar=50 ujn. 



TENTACULARIID TRYPANORHYNCHS FROM THE NHM 



145 



24 



23 






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, 1 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, 1 134, 1000; SW=700, 
nm, 493; pbo=700, 642; 500; pv=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); 
BR=3.5:1, 3.2:1; 3.5:1; SP=1.6:1. 1:1, 1.9:1.4:1, 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= 10.4-1 2, 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 th proglottid: 55-60 
x 475-185; 100 th : 185-210 x 560-585; 150 th : 360-420 x 755-780; 
190 th : 670-730 x 840-900). 80-90 testes in a single layer, 33-55 
(between 100 th and 150 th 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 um. 



146 

27 



H.W. PALM 



28 



30 




^ 

* 

m 
^ 






Fig. 27 H. estigmena from C. limbatus. Heteromorphous basal armature, 

bothridial surface. Scale bar=10 urn. 
Fig. 28 H. estigmena from C. limbatus. Heteromorphous metabasal 

armature, antibothridial surface. Scale bar=10 urn. 



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 IIAa 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 10-1 1 urn (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 



29 





Fig. 29 Heteronybelinia alloiotica from Carcharhinus limbatus. 

Heteromorphous basal armature, bothridial surface. Scale bar=10 um. 
Fig. 30 H. alloiotica. Heteromorphous metabasal armature, antibothridial 

surface. Scale bar=10 urn. 

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 . 197 1 , Cirolana, Atlantic Ocean off Morocco, 33°43'N, 8°38'W, 
222-236 m. 1 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 leg., 16.5.78, 2 adults from the 
stomach of Sphyrna mokarran. South Africa; Additional material: 
BMNH 1968.2.14.30-31, Gooding leg., 2 adults from Sphyrna 
blochii, Singapore. 



TENTACULARIID TRYPANORHYNCHS FROM THE NHM 



147 





33 




Fig. 31 Heteronybelinia heteromorphi sp. nov.. Scolex from Sphyrna makorran. Scale bar=100 pm. 

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. 33 H. heteromorphi sp. nov. from S. makorran. Heteromorphous basal armature, bothridial (left) and antibothridial (right) surfaces. Scale bar=15 um. 



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; pv=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 
(368^127); BW=154 (134-163), 181 (174-187), 158 (137-175), 
176 (173-179); BR=2.8:1, 2.2:1, 2.1:1, 2.3:1; 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=ll-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 (25-4-0 in diameter) and 
vitellaria (10-15); other internal structures not seen. 

Remarks. The present specimens belong to subgroup IIAa (Palm 
etal., 1997), with a heteromorphous armature and hooks increasing 
in size towards the metabasal part of the tentacle. The large hook size 



148 



H.W. PALM 





Fig. 35 H. minima sp. nov.. Scolex from Polynemus paradiseus. Scale 
bar=100 urn. 



Fig. 34 Heteronybelinia minima sp. nov.. Scolex from Harpodon 
nehereus. Scale bar=50 |im. 

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//, 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. 




37 





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 



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 urn. 
Fig. 37 H. minima sp. nov., hooks on bothridial surface. Scale bar=15 

urn. 
Fig. 38 H. minima sp. nov., hooks on antibothridial surface. Scale 

bar=15 um. 



TENTACULARIID TRYPANORHYNCHS FROM THE NHM 



149 



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. paradiseus 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 3<MU) 

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 leg., 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 



hook size in the metabasal armature ranged between L=l 1.7-12.5; 
B=7.2-9.2 (bothridial) and L=l 3.0-14.0; 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 A 7 , 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 urn (antibothridial). The general hook form 
remains rose-thorn shaped along the tentacles. Thus, the present 
specimen belongs into subgroup IIAa of Palm et al. (1997). 

15. Heteronybelinia yamagutii (Dollfus, 1960) nov. comb. 

(Fig. 42^4) 

Material examined. BMNH 1976.1 1.5.41, R. van der Elst leg. , 
1 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 300^120 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 



39 






Fig. 39 Heteronybelinia robusta. Scolex from Carcharhinus limbatus. Scale bar=100 um. 

Fig. 40 H. robusta Heteromorphous metabasal armature, bothridial (right hand side) and antibothridial (left hand side) surfaces. Scale bar=10um. 

Fig. 41 H. 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 



151 



43 






Fig. 42-44 H. yamagutii. Strobila 4-5 cm (42) and 7-8 cm (43) behind 
scolex, and last proglottids (44). Scale bar=500(jm. 



BMNH 1997.3.24.1, 1997.3.24.2, 1997.3.24.3^, 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, 1 977. 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 



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 et 
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 et 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, 
1 995). 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 1 6 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 
IIAa (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 tentaculariids 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 



H.W. PALM 



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), N. 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. nov., 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), TV. tenuis (Linton, 1890), 
Nybelinia sp. 

c Size of basal hooks larger than metabasal hooks 

N. basimegacantha Carvajal, Campbell & Cornford, 1976 



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 (Vijayalakshmi, 
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, I960)) 

A Without characteristic basal armature 

a Size of basal hooks smaller than metabasal hooks 

H. alloiotica (Dollfus, 1960), H. cadenati (Dollfus, 1960), 
H. e/oftgata(Shah&Bilqees, \919),H. est/gmena (Dollfus, 
1960),//. eureia (Dollfus, 1960),//. heteromorphisp. nov., 
H. karachii (Khurshid & Bilqees, 1988), H. minima sp. 
nov., H.punctatissima (Dollfus, 1960),//. 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 
IAa by Palm etal. (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 



153 



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 etal. (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. I 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 fur Meereskunde Kiel and The Natural History 
Museum, London. 



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Bull. not. Hist. Mus. Lond. (Zool.) 65(2): 155-164 



Issued 25 November 1999 



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 Protegees, B.P. 738, Antananarivo (101), Madagascar. 

SYNOPSIS. A new species of Microgale is described on the basis of two specimens collected in southwestern Madagascar. This 
species occurs in the Pare 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 espece de Microgale est decrite sur la base de deux specimens collectes dans le sud-ouest de 
Madagascar. Cette espece est presente dans le Pare National de Zombitse-Vohibasi a 780 m dans les forets seches caducifoliees 
ainsi que dans l'habitat montagneux de la Foret d' Analavelona a 1050 m, dont les plantes sont une composition d'especes de Test 
(humide) et de l'ouest (seche). Cette nouvelle espece presente plusieurs modifications craniennes distinctes qui semblent etre le 
resultat de 1' adaptation a des zones de conditions semi-xerophiles. Des donnees considerables sont disponibles sur la region du 
sud-ouest de Madagascar sur les changements climatiques durant le Holocene. La biogeographie de ce nouveau Microgale est 
examinee a la lumiere de ces vicissitudes environnementales. 



INTRODUCTION 



MATERIALS AND METHODS 



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 to the Analavelona Forest in early 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. 



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 right 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. 



© The Natural History Museum. 1999 



156 



P.D. JENKINS AND S.M. GOODMAN 




Town & Site 
Ay/ Coast and River 
A f National Road 
1 Protected Area 



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 [Foret de Vohibasia], 59 km 
northeast of Sakaraha, Province de Toliara, southwestern Madagas- 
car, 22°27.5'S, 44°50.5'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 [Foret 
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 Departement de Biologie Animale, 
Universite 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 



M. cowani 



M. nasoloi 
Vohibasia 
FMNH 156187 


M. nasoloi 
Analavelona 
FMNH 161575 


81 




70 


53 




62 


13 




14 


16 




16 


14.0 




5.9 



Character 
HB 

TL 

HF 

E 

Wt 

Condylo-incisive length 
Upper toothrow length 
Rostral breadth 
Interorbital breadth 
Braincase breadth 
Braincase height 



75.00 ±4.47 
66-82(10) 
35.64 ±2.84 
30-41 (11) 
12.55 ±0.49 
12-13(11) 
11.82 ± 1.11 
10-13(11) 
11.0 ±0.89 
10-12.5 (6) 
20.87 ± 0.66 
19.9-22.0(12) 
9.31 ±0.33 
8.7-10.0(12) 
3.53 ±0.16 
3.3-3.8(12) 
5.10± 0.14 
4.9-5.4(12) 
8.83 ± 0.25 
8.5-9.2(12) 
5.66 ±0.1 8 
5.4-6.1 (12) 



77.78 ± 5.64 
68-85(12) 
65.44 ±3.00 
61-71 (11) 
16.03 ±0.60 
15-17(12) 
14.19 ± 1.42 
12-17(12) 
13.75 ±0.90 
12.5-15.5(8) 
22.38 ±0.44 
21.4-23.0(12) 
10.73 ±0.19 
10.4-11.0(12) 
2.47 ± 0.85 
2.3-2.6(12) 
5.23 ±0.15 
5.0-5.6(12) 
10.07 ±0.18 
9.8-10.3(12) 
6.59 ±0.14 
6.4-6.8(12) 



23.2 

10.2 

3.1 

4.3 

9.2 

4.9 



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 II to P2 sub-parallel; anterior incisive foramina very large, 
posterior incisive foramina lie between anterior region of canines; 
mesopterygoid 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 



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 (1 1 ) robust, pro-odont, greater in crown 
height than C, distostyle well developed; short diastema between II 
and 12; 12 robust, approximately equal in crown height to C, anterior 
accessory cusp and distostyle well developed; 13 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 13, 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 Ml to M3; M3 anteroposteriorly 
compressed, bucco-lingually elongated. First lower incisor (il) 
large, subequal in crown height to i2, 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 i3, two roots present; p3 small, slightly greater in 
crown height than p2, with small paraconid and hypoconid; p4, ml 
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 Pare 
Botanique et Zoologique de Tsimbazaza, Antananarivo. Nasolo was 



158 



P.D. JENKINS AND S.M. GOODMAN 





| 




1 I 

E 


i— 



Fig. 2 Dorsal view of skin of Microgale nasoloi (FMNH 156187) 



1 £ 




■i 1 /^« 
P^ ^ ■••Hi 

^^^^^^^ IB' 

■ dm mi- ■■->.., __ _ ^^-: _' ,v j^MM 


ranm 


Inlmmml : ' v? ™ 



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 




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 II 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 12 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 i3 small, 
unlike M. soricoides which has i 1 larger than i2. 

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 



Fig. 4 Dentition of Microgale nasoloi (FMNH 156187). Buccal view of 
left II - 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= lOinM. 
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- 



Ecology 

Vohibasia ( 1 5,500 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 et 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 (Petignat 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 (Tenrec 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 ('Foret basse sclerophylle'), 
surrounding areas of low-lying forests to the east (e.g. Zombitse- 
Vohibasia) as dry dense forest ('foret dense seche') and to the west 
as Didiereaceae and Euphorbia bush ('Didiereacees et Euphorbia 
haut fourre'). 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 95-1 10 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 ai, 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 



1 998 in the Analavelona Forest, 1 98 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 
1 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 ITsalo 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 owl 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 3x2 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 on a 
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, such as 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 



162 



P.D. JENKINS AND S.M. GOODMAN 





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 (Mahe & 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 



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, TENREC1DAE) 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 Flsalo 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 
(WWF), 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 Forets and Association National 
pour la Gestion des Aires Protegees. We thank Daniel Rakotondravony for 
access to material in the collection of the Departement de Biologie Animate. 
Universite d' Antananarivo. The field projects were funded by grants from 
NORAD to WWF 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. 



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Bull. not. Hist. Mus. Land. (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 Iguania 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 phy logeny 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, 1 994). 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 Iguania 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. 



put forward by Frost and Etheridge ( 1 989), 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 ( 1 980) 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 Stellio is 
unavailable (Stejneger, 1 933) 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&B6hme, 1997). 



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 



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. 



© The Natural History Museum. 1999 



166 



E.N. ARNOLD 



squamosal 



extracolumella 




depressor 
mandibulae 
muscle 



quadrate 



pars superior 

extracolumella 

pars inferior 

tympanum 



foot plate 




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, 1 948 and T. cephalus Gunther, 1 867) 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 (Gunther, 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 Gunther, 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, 1 889, 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 Gunther, 1 864, C. stoddarti Gray, 1 834 and 
C. tennentii Gunther, 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 



167 



X. cephalus 



Ceratophora 



X. lineata 
T. intima. 



5b 



6b 
4 
3 

1ab 



5c 



Lvriocephalus 
Cophotis ^ 



L parviceps . 






2b 



T. adelaidensis 
T. diemensis. 



6b 

4 

1b 



Aphianotis - 



3 
2b 



Primitive oriental 
agamids- 



P. vlanaali 




P. theobaldi 




P. roborowski 


P. axillaris 


6a \ 


/6a 


5b \ 


/ 5b 



Most species. 



6b 
5c 



P arabicus ^ 
P maculatus. 



Fig. 2 Pattern of ear reduction in Tympanocryptis (Agamidae). 

and in the clade made up of Aphaniotis, Lyriocephalus, Cophotis and 
Ceratophora (Agamidae). 

Abbreviations: l . 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. 



5a 

4 



P mystaceus 



2b 



Bufoniceps - 



Cophosaurus 



Holbrookia 




Trapelus - 



4 
2b 



Callisaurus- 



3 

2a 

lb 



1a 



Fig. 3 Pattern of ear reduction in Phiynocephalus and its relatives 
(Agamidae). For abbreviations see Fig. 2. 



Fig. 4 Pattern of ear reduction in phrynosomatid sand lizards 
(Phrynosomatidae). For abbreviations see Fig. 2. 



168 



E.N. ARNOLD 



a 





b 









. 


















-''^iJSfcfa 




^§2*P^iP 


fe. m ^— r 






ifc.'^v — 


, *^ t -^ 




^^^ i^^^ 





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, even if 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. interscapulars, 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 . In some 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 is 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 






d 



Fig. 6 Stages in reduction of external ear in the clade containing Phrynocephalus. a. Tympanum superficial and fully exposed, Pseudoirapelus sinaitus 
(BMNH 1953.1.7.9); b. tympanum sunk and external opening of meatus so formed reduced, Trapelus agilis (BMNH 94.1 1.13.4); 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 Giinther, 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, 1 892) and Brookesia stumpfii 
Bottger, 1894 (personal observations). 



170 



E.N. ARNOLD 



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 
GLinther, 1 874 and Brookesia Gray 1 865 studied in which there are 
not even indentations. 

Ear reduction in the Phrynosomatidae 

(Fig. 4) 

Relationships within the Phrynosomatidae are discussed by De 
Queiroz ( 1 992) 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 is 
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 



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 Brooke sia-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. 



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earless lizard. Copeia 1961: 68-74. 
, 1961b. An additional note on the ear of Holbrookia maculata. Copeia 1961: 

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, 1961c. The middle ear of Holbrookia and Callisaurus. Copeia 1961: 405-410. 

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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. 



CONTENTS 



73 Systematics and phylogeny of Zausodes C.B. Wilson, 1 932 (Copepoda, Harpacticoida, 

Harpacticidae), including three new species from the northern Gulf of Mexico. 

L Bouck, D. Thistle and R. Huys 
1 23 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) 

H.W. Palm and T.Walter 
1 33 Nybelinia Poche, 1 926, Heteronybelinia gen. nov. and Mixonybelinia gen. nov. (Cestoda, 

Trypanorhyncha) The Natural History Museum, London 

H.W. Palm 
155 A new species of Microgale (Lipotyphla.Tenrecidae) from isolated forest in southwestern 

Madagascar 

PD. Jenkins and S.M. Goodman 
165 Modes of ear reduction in iguanian lizards (Reptilia, Iguania); different paths to similar ends 

EM Arnold 



ZOOLOGY SERIES 

Vol. 65, No. 2, November 1999