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Zoosystematics
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ISSN 1435-1935 Zoosyst. Evol. 93 (1) 2017, 1-188

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Zoosystematics and Evolution

A Bulletin of Zoology since 1898

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Zoosystematics
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93 ( 1 ) 2017

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Zoosystematics and Evolution

A Bulletin of Zoology since 1898

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Zoosystematics and Evolution

2017. Volume 93. 1 Issues

ISSN: 1435-1935 (print), 1860-0743 (online)
Abbreviated keys title: Zoosyst. Evol.

In Focus

The cover picture shows a female of Nothobranchius
insularis sp. n. from eastern Tanzania.

See paper of Costa WJEM Redescription of Nothobranchius
lucius and description of a new species from Mafia Island,
eastern Tanzania (Cyprinodontiformes, Aplocheilidae)

Cover design

Pensoft

Zoosystematics and Evolution

A Bulletin of Zoology since 1898

Content of volume 93 ( 1 ) 2017

Liebherr JK

Bryanites graeffii sp. n. (Coleoptera, Carabidae): museum rediscovery of a relict species
from Samoa 1

Pochai A, Kingtong S, Sukparangsi W, Khachonpisitsak S

The diversity of acorn barnacles (Cirripedia, Balanomorpha) across Thailand’s coasts:
The Andaman Sea and the Gulf of Thailand 13

Costa WJEM

Redescription of Nothobranchius lucius and description of a ne\A/ species from Mafia Island, eastern
Tanzania (Cyprinodontiformes, Aplocheilidae) 35

Albano PG, Bakker PAJ, Janssen R, Eschner A

An illustrated catalogue of Rudolf Sturany’s type specimens in the Naturhistorisches Museum
Wien, Austria (NHMW): Red Sea gastropods 45

Minton RL, Harris PM, North E, Tu DV

Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae) 95

Sandberger-Loua L, Muiier H, Rddel M-0

A review of the reproductive biology of the only known matrotrophic viviparous anuran, the West
African Nimba toad, Nimbaphrynoides occidentalis 105

Salvador RB, Cavallari DC, Simone LRL

Taxonomical study on a sample of land and freshwater snails from caves in central Brazil, with
description of a new species 135

Lambert SM, Mutter CR, Scherz MD

Diamond in the rough: a new species of fossorial diamond frog (Rhombophryne) from Ranomafana
National Park, southeastern Madagascar 143

Branch WR, Haacke W, Pinto PV, Conradie W, Baptista N, Verburgt L, Luis Verissimo L

Loveridge’s Angolan geckos, Afroedura karroica bogerti and Pachydactylus scutatus angolensis (Sauria,
Gekkonidae): new distribution records, comments on type localities and taxonomic status 157

Corgosinho PHC, Schizas NV, Previatteiii D, da Rocha CEF, dos Santos-Silva EN

A new genus of Parastenocarididae (Gopepoda, Harpacticoida) from the Tocantins River basin
(Goias, Brazil), and a phylogenetic analysis of the Parastenocaridinae 167

Abstract & Indexing Information

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BIOSIS Previews® (Thompson ISI)

Cambridge Scientific Abstracts (CSA/CIG)

Web of Science® (Thompson ISI)

Zoological Record™ (Thompson ISI)

Zoosyst. Evol. 93 (1) 2017, 1-11 | DOI 10.3897/zse.93.10802

museum fur naturkunde

Bryanites graeffii sp. n. (Coleoptera, Carabidae): museum rediscovery
of a relict species from Samoa

James K. Liebherr^

1 Cornell University Insect Collection, John H. and Anna B. Comstock Hall, 129 Garden Ave., Cornell University, Ithaca NY 14853-2601 U.S.A.

http://zoobank.org/4B7C702D-F9FC-4038-BE8E-DEC7FCD3D63A

Correspoudiug author; James K. Liebherr (JKL5@cornell.edu)

Received 14 October 2016
Accepted 21 December 2016
Published 5 January 2017

Academic editor:

Martin Husemann

Key Words

anthropogenic extinction
biogeography
brachyptery
Polynesia

Abstract

Bryanites graeffii sp. n. is described from Samoa based on a single male specimen col¬
lected between 1862-1870 that was recently discovered in the Museum national d’His-
toire naturelle, Paris. Cladistic analysis based on 127 morphological characters from 49
exemplars of the carabid beetle tribe Platynini in the Austral-Pacific region, places the
new species as adelphotaxon to Bryanites samoaensis Valentine, type species of the genus
Bryanites Valentine, 1987. Bryanites comprises, along with Vitagonum Moore, 1998 of
Fiji and Ctenognathus Fairmaire, 1843 of New Zealand, a clade that diverged early in
the evolutionary history of Pacific platynine Carabidae. Bryanites graeffii exhibits very
large body size among taxa of Platynini—16.2 mm standardized body length—with the
genus characterized by vestigial fiight wings and metathoracic apomorphies that are asso¬
ciated with fiight-wing loss. Along with Blackburnia Sharp, 1878 of Hawaii, the origins
of Bryanites, Vitagonum, and Ctenognathus are hypothesized to date to the Miocene,
with their radiations beginning long before the origins of the geographically widespread,
fiight-capable species of Metacolpodes Jeannel, 1948 that colonized numerous island
systems across the western Pacific. Given the numerous platynine taxa collected by ex¬
tensive biotic surveys of Samoa during the first quarter of the 20* Century, the absence
of any specimens of B. graeffii since the initial collection of the unique holotype prior to
1871 suggests that this species may be extinct. Such extirpation of large platynine cara¬
bid beetles has also been documented for Hawaii, where the time of extinction of seven
Blackburnia species represented only by subfossil fragments coincides with the time of
human colonization and attendant introduction of the Pacific rat, Rattus exulans (Peale).

Introduction

It is undeniable that natural history museums represent in¬
valuable and irreplaceable archives of biological diversity
on Earth. Firstly these institutions serve as repositories for
many millions of studied and described specimens: i.e. type
specimens and associated subsequent collections of named
species. Secondly museums also hold uncounted, unstud¬
ied specimens that have been collected and processed, but
never adequately examined or understood by a taxonomic
specialist. Predictably, examination of unidentified materi¬
al collected long ago can produce surprising results, espe¬
cially when the historical museum specimens represent the
only evidence we have for existence of that particular spe¬
cies. For example, two Samoan species of flying fox, genus

Pteropus Brisson, 1762 (Chiroptera: Pteropodidae), are
known only from museum specimens collected between
1839 and 1856 (Helgen et al. 2009). In this contribution,
a Samoan carabid beetle specimen collected prior to 1871,
and subsequently deposited in the Paris Natural History
Museum, is shown to represent the only specimen known
of a new species. Moreover, the genus to which the new
species is assigned is known previously only from two spe¬
cies based on two specimens collected in 1924 (Valentine
1987). That the new species is being described only now,
over 140 years after its collection from nature, attests to
the contextual information that is required to interpret bio¬
diversity, for it is not the simple naming of organisms that
occupies systematists, but more importantly, the organized
naming and placing in context of all organisms. A scientific

Copyright James K. Liebherr. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits
unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

Liebherr, J.K.: Bryanites graeffii sp. n.

name presented in isolation from any detailed taxonomic
framework is nearly useless, being suspect as a natural en¬
tity, devoid of biological context provided by knowledge
of its sister group (Hennig 1966), and at best representing
a single datum indexing a gross estimate of biodiversity.

The specimen described in this contribution is a mem¬
ber of the carabid beetle tribe Platynini belonging to the
genus Bryanites Valentine, 1987 (Valentine 1987). This
genus was previously known only from specimens collect¬
ed by E. H. Bryan, Jr., 23-V-1924, at Sala'ilua, SavaiT Is¬
land, Samoa. Though the holotype specimens of Bryanites
samoaensis Valentine and B. barri Valentine are assign¬
able to the Platynini, they are aberrant representatives of
that tribe. In contrast to many platynine carabid beetles,
which as the name suggests are flattened dorsally, the bod¬
ies of Bryanites beetles are fusiform with a broad prono-
tum, their bodies convex dorsally. The two Bryanites spp.
also exhibit patterns of setation on the elytra and pronotum
unusual among platynine taxa. H. E. Andrewes, formerly
at the Natural History Museum, Eondon and a worldwide
authority on Carabidae, placed determination labels on
both specimens subsequently described by Valentine that
read “? Pterostichini gen. nov.” He did this presumably
because the specimens appear superficially like the larg¬
er-bodied, more robust beetles of that tribe, though their
lack of a critical diagnostic feature of most Pterostichi¬
ni—i.e. an externally visible plica, or fold, along the apical
elytral margin—^flts members of the tribe Platynini. An¬
drewes’ tentative, incorrect guess as to tribal membership
is also understandable because the two Bryanites beetles
appear nothing like the other Samoan species of Platynini
that he had previously described (Andrewes 1927).

This paper first traces the provenance of the newly
described Samoan beetle specimen from its collection in
nature to the present day. We cannot be certain why the
specimen avoided description until now. But the docu¬
mented timing of expeditions and subsequent taxonomic
publications coupled with the temporal connections of
the various taxonomists, and how the beetle could have
passed from hand to hand, make a strong case for how
a large carabid beetle from a tropical island could be ig¬
nored for well over a century to be rediscovered within a
natural history museum. In order to be certain how best to
classify the new species, cladistic analysis using morpho¬
logical characters is used to phylogenetically place the
species. After adding the new species to a little-known
clade of Samoan Carabidae, the question regarding the
fate of this lineage in nature is investigated, with parallels
from the platynine carabid beetle fauna of the Hawaiian
Islands suggesting a likely scenario for this species lead¬
ing from the 19th to the 21st Century.

Materials and methods

Taxonomic material. Specimens treated in this contribu¬
tion were borrowed from the Museum national d’Histoire
naturelle, Paris (MNHN), Mdm. Helene Perrin and Dr.

Thierry Deuve curators, and the B. P. Bishop Museum,
Honolulu (BPBM), James Boone collection manag¬
er. Placement of the new species within the context of
platynine phylogeny (Suppl. material 1) utilized an up¬
dated version of the character matrix previously present¬
ed in Eiebherr (2005), with that paper citing institutional
sources that provided specimens for initial matrix de¬
velopment. Taxa included in the analysis are distributed
in the southwest Pacific region, including Australia and
Asia, northeastward through Melanesia and Polynesia to
the Hawaiian Islands.

Several taxa were added to complement the previous
analysis. Colpodes kanak Fauvel (Fauvel 1903) of New
Caledonia was added to the analysis based on examina¬
tion of a female (MNHN) determined by Fauvel in 1906.
Vitagonum apterum Moore of Fiji was added because it,
like Bryanites, represents an aberrant, taxonomically iso¬
lated platynine lineage in the Pacific (Moore 1998). The
male holotype of Bryanites samoaensis serves to repre¬
sent the genus in the analysis. The female holotype of B.
barri Valentine was also studied, and external anatomy of
prothorax and elytra is consistent with Valentine’s (1987)
taxonomic decision placing both species together in the
genus. However the type specimen of B. barri is heavily
damaged. The beetle was extensively disarticulated during
description, demonstrated by Valentine’s illustrations of
an isolated mentum, maxilla, and labium (Valentine 1987:
Fig. 3). The resulting disarticulated structures were then
mounted on two acetate sheets using Canada balsam as a
fixative. Several isolated flecks of mounting medium re¬
main on the sheet without any associated sclerite, suggest¬
ing strongly that flexure of the acetate caused the balsam
to pop off the acetate. This interpretation explains the ab¬
sence of the head capsule, mandibles, and antennae from
the mounting cards. The female ovipositor is also damaged
and the internal reproductive tract not present. Given this
destruction of the specimen, 26 characters of the female
reproductive tract and 11 characters of the head cannot be
scored. Coupling that loss with the inability to score the
21 characters of the male reproductive system from the
female holotype leads to at least 58 of the 127 characters
necessarily being coded as missing. The poor mounting
condition of the remaining sclerites cemented to the spec¬
imen cards limits confidence in assessing microsculpture
covered by the Balsam, adding further uncertainty to the
assessment of character states. This lack of information
precludes a precise placement of this taxon in the analysis,
at the same time seriously reducing resolution in a strict
consensus cladogram when the taxon is included in the
analysis. As B. samoaensis is the type species of Bryanites,
it was decided to limit the focus of the analysis to the ques¬
tion of where the taxon herein classified as B. graeffii fits
phylogenetically relative to an array of fully informative
exemplar specimens. As we have no evidence to overturn
Valentine’s (1987) decision to place B. barri in Bryanites,
that decision is allowed to stand.

Faboratory Techniques. Dissection protocols used
throughout development of the present character matrix

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Zoosyst. Evol. 93 (1) 2017, 1-11

are detailed in Liebherr (2015: 18-20). An ocular ratio
is used to quantify eye size: the maximum width of head
across eyes divided by the minimum breadth of frons be¬
tween eyes. Male genitalia are preserved in polyethylene
vials placed on the specimen pin. Standardized body
length comprises the sum of three measurements: 1, head
length measured from the medioanterior margin of the la-
brum to the cervical ridge; 2, median pronotal length; and
3, elytral length measured from base of elevated scutellar
apex to apex of longer elytron adjacent to the suture.

Character data. The cladistic analysis was based on
127 characters, 26 scored from the female reproductive
tract and gonocoxae (i.e. ovipositor), 21 scored from
male genitalic structures, and 80 derived from external
anatomical structures (Suppl. material 2). Six of the char¬
acters are autapomorphic for a single terminal, however
these were retained as other taxa could not be scored for
these characters, due either to missing female or damaged
specimens. Given additional material these characters
could become potentially synapomorphous.

Cladistic methods. The character matrix was devel¬
oped in WinClada (Nixon 2002) (Suppl. material 2), and
analyzed by Nona (Goloboflf 1999) using the ratchet (Nix¬
on 1999). Results from an initial analysis using 200 itera¬
tions of the ratchet were compared to subsequent analyses
using 1000 ratchet iterations, and then 10,000 ratchet it¬
erations. After each ratchet run all trees were hard col¬
lapsed—i.e. collapsing nodes on trees when they are not
supported under all optimizations—and then non-opti¬
mum (longer) trees were deleted. The strict consensus
was then generated from those remaining hard-collapsed
trees. Identical results at the 200,1000 and 10,000 ratchet
levels permitted the conclusion that all most parsimoni¬
ous trees had been discovered.

Results

Provenance. The specimen rediscovered in the Paris Mu¬
seum (Fig. 1) bears three labels (Fig. 2). The collector/lo¬
cality label specifies that the beetle was collected in Samoa
by “Dr. Graffe.” A second label reads “8284”, and a third
label notes accession by the Paris Museum. “Dr. Graffe” is
no doubt Eduard Graffe, or Graeflfe, a Swiss zoologist and
naturalist who lived in Samoa from 1862-1870 (Graeflfe
1917, Clunie and Snow 1986). Graetfe was employed by
Johann Cesar VI Godeflfroy, a wealthy shipping magnate
in Hamburg who founded the Museum Godeffroy. The
Museum Godeflfroy published a journal, within which
Graeflfe published treatises on Samoan geography and
birds (Graeflfe 1873a, 1873b). He also published on the in¬
vertebrates including the insects oflFiji (Graeflfe 1866). He
maintained contact with scientists in Europe, including the
ornithologists Otto Finsch and Gustav Hartlaub, to whom
he sent a manuscript describing the birds ofl Tonga (Graefl-
fle 1870). After Graeflfe’s return to Hamburg, Eeon Fair-
maire described new species and redescribed numerous
previously described beetle species from Australia, Fiji,

Tonga, and Samoa (Fairmaire 1879a), many deposited in
Museum Godeflfroy. Fairmaire’s (1879a) paper documents
a connection between Graeflfe and Fairmaire via the Mu¬
seum Godeflfroy, and supports the transfer ofl the specimen
described herein to Fairmaire, either by loan or by pur¬
chase, after 1870 but prior to 1879. Fairmaire described
or revised other carabid beetles from Fiji and Tonga (Fair¬
maire 1878, 1879b, 1881a, 1881b), though no more from
Samoa. When his collection passed to the Paris Museum
upon his death in 1906, the “MUSEUM PARIS” accession
label was placed on the specimens (e.g. Fig. 2), with all of
his carabid specimens maintained together in boxes as the
“Fairmaire Collection.” When Erwin and Erwin (1971)
assessed the condition of the Paris Museum carabid beetle
holdings, they cited shelving unit B13, shelves 1-2; “23
boxes of the Fairmaire Collection, misc. carabids in very
poor condition with no or poor labels, ‘a mess’! (p. 10).”
It is within this set of boxes that the specimen described
below was found.

Cladistic Analysis. Subjecting the taxon-character ma¬
trix to Nona (Goloboflf 1999) within the WinClada shell
(Nixon 2002) resulted in 47 hard-collapsed, multiple
equally parsimonious trees (MEPT) ofl 566 step-length un¬
der 200, 1000, or 10,000 iterations ofl the ratchet (Nixon
1999). These trees were constrained to be fully resolved
under all character optimizations; i.e. fast or slow optimi¬
zation. The strict consensus cladogram ofl607 steps (Fig. 3)
was rooted so that the species ofl Lorostema Motschulsky,
1865 comprise outgroups to the other Pacific platynine
taxa. This decision was based on plesiomorphic presence
ofl two testes in male beetles ofl Lorostema spp. versus the
derived monorchid, or single-testis configuration (charac¬
ter 46, Suppl. material 2) in males ofl species ofl Blackbur-
nia Sharp, 1878, Notagonum Darlington, 1952, Colpodes
W. S. MacEeay, 1825, and Metacolpodes Jeannel, 1948
(Will et al. 2005). The cladistic relationships indicate that
the newly described species should be combined as Bry-
anites graeffii sp. n. (Fig. 3). The two Bryanites examples
are members ofl a clade, under all possible MEPTs, that in¬
cludes Vitagonum apterum Moore oflFiji as adelphotaxon.
These two genera are in turn sister group to Ctenognathus
Fairmaire, 1843 oflNew Zealand.

Other relationships inherent in the tree are very similar
to those discussed in Eiebherr (2005, fig. 78), although
the inclusion ofl the two Bryanites spp. plus V. apterum
in this analysis results in the Ctenognathus spp. joining
with those taxa much closer to the root node the clado¬
gram (Fig. 3). Also, Notagonum kanak (Fauvel) comb,
n. is placed such that it must be removed from the genus
Colpodes and newly combined with Notagonum.

Taxonomic challenges remain regarding monophyletic
classification of species in the genera Colpodes and No¬
tagonum, and these must be addressed via a more com¬
prehensive and informative phylogenetic analysis, such
as those that include DNA-molecular characters (e.g.
Maddison 2012). Colpodes is certainly polyphyletic. The
genus is based on Colpodes brunneus (W. S. MacEeay),
placed here as sister species to a second Javan species.

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Liebherr, J.K.: Bryanites graeffii sp. n.

C. latus Louwerens (Fig. 3). A third Javan species, C.
brittoni Louwerens, is also closely related, with beetles
of all three species exhibiting exceedingly protruded
compound eyes and very broad pronotal lateral margins
(Liebherr 1998). Other species combined with Colpodes
in this analysis—from Fiji and Tahiti (Fig. 3)—must be
recombined with different generic names to accommo¬
date the monophyletic taxa Helluocolpodes Liebherr,
2005 and Metacolpodes. Notagonum has been a genus of
convenience since Darlington (1952) proposed it. In his
words, “It must be admitted that it is hard to draw a line
between Colpodes in my partly restricted sense and some
of the forms which I am including in Notagonum, but I am
convinced that when Colpodes is broken up the various
species of Notagonum will properly form at least one and
perhaps more separate genera (Darlington 1952: 129).”

Taxonomy

Bryanites Valentine, 1987

Type species. Bryanites samoaensis Valentine (by original
designation).

Diagnosis. These beetles can be diagnosed from other
Pacific platynine taxa by the much reduced subapical
sinuation of the elytra, with the elytral margins straight
to convex near the apex (Fig. 1). The pronotum is broadly
orbiculate, with the lateral margins convex to only slightly
concave anterad the rounded hind angles. The pronotum
has the basal seta present and situated anterad the rounded
hind angle. The elytra are moderately narrowed basally,
with the basal elytral groove meeting the lateral elytral
depression at an angle; i.e. the humeri are angulate.
The male aedeagus exhibits characters typical of tribe
Platynini (Fig. 4): 1, both parameres are rounded apically,
or conchoid in shape; 2, the right paramere is smaller than
the left, and the aedeagus lies with the right side ventral
in repose; 3, the basal bulb is closed and bears a sagittal
crest; and 4, the internal sac is tubular and unarmored,
with slightly more melanized spicules present apically
near the gonopore.

Beetles of all three Bryanites species are brachypter-
ous, with the wing rudiments narrow and elongate
stenopterous straps, the length of the rudiments more than
4x the rudiment breadth. Beetle size is moderate to large,
ranging from 11.7 mm in B. barri (measurement of Barr
1987) to 16.2 mm in B. graeffii.

Key to the Adults of Bryanites Valentine

1. Beetles of moderate size, standardized body length 11.7-12.5 mm; pronotum quadrisetose both lateral and basal setae

present; parascutellar seta present.2

Larger beetles, standardized body length 16.2 mm; pronotum bisetose, only basal seta present both sides; parascutel¬
lar seta absent. B. graeffii sp. n.

2. Third elytral interval with 6 setae along length, the anterior seta associated with the third stria, the trailing five setae
associated with the second stria; elytral basal groove meeting lateral elytral depression at right angle; pronotum without

any evident laterobasal depressions, at most a slight depression near hind margin (left side of holotype).

. B. samoaensis Valentine

Third elytral interval with 3 setae along length, the anterior seta associated with the third stria, the posterior two setae
associated with the second stria; elytral basal groove meeting lateral elytral depression at acute angle; pronotum with

broad, shallow linear laterobasal depressions extended from hind angles toward center of pronotal disc.

. B. barri Valentine

Bryanites graeffii sp. n.

http://zoobank.org/F82C8023-8E56-4563-AB2E-8A208F41E984
Figs 1, 2,4

Diagnosis. Besides the very large size of this beetle—
standardized body length 16.2 mm—the elytral and
pronotal setation are diagnostic. The elytra lack the
parascutellar seta and any dorsal elytral setae, though
both subapical and apical setae are present in the sev¬
enth stria near the rounded sutural apex. The pronotum
has only the basal seta present, with this seta’s position
0.14x the median pronotal length anterad a transverse
line drawn across the median pronotal base. The prono¬
tal lateral marginal depression is broad and upraised to a
smooth, unbeaded margin. The prosternal process is fiat
between the procoxae, with four to five setae each side
approaching the process apex. Cuticular micro sculpture

is particularly well developed, with the frons and clypeus
bearing distinct, upraised isodiametric sculpticells, and
the vertex covered with more transverse, though equal¬
ly well-developed sculpticells. The pronotal and elytral
discs are covered with very small transverse sculpticells,
the sculpticells’ small size giving the surface a velvety or
velour-like refiection.

Description. Head broad, robust, ocular ratio 1.61; an¬
tennae elongate, as long as distance from antennal socket
to elytral midlength; scape stout, maximal breadth 0.5x
distance from basal constriction to apex; antennomeres
2-3 apparently glabrous, but sparsely covered with very
short microsetae, an apical ring of setae on antennom-
ere 3; antennomere 4 apparently glabrous in basal % of
length, though also with very short microsetae, remainder
of antennomere and antennomeres 5-11 pilose with darker

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Zoosyst. Evol. 93 (1) 2017, 1-11

Figure 1. Male holotype, Bryanites graeffii, dorsal view.

bmnneous, glabrous longitudinal ridge on each anterior
and posterior surface; frontal grooves very shallow, ending
posteriorly anterad the anterior supraorbital seta; posterior
supraorbital setal position behind posterior margin of eye
and 3x as far from eye margin as anterior seta; frons and
clypeus not demarked by suture, surfaces convex, continu¬
ous, only three very shallow transverse wrinkles medially
at position of frontoclypeal suture; labral anterior margin
straight, only slightly incurved medially; mentum tooth
broad, apex flattened medially, mentum setae positioned
posterad curved mentum margin each side of midline;
submentum with two setae each side. Pronotum broad,
maximal width 1.08x median length; lateral margins only
slightly incurved anterad rounded hind angles; broadly
longitudinal laterobasal depressions joined by well-de-
flned transverse depression anterad basal convexity; me¬
dian longitudinal impression very flnely incised, absent on
basal convexity, continuous to beaded front margin; front
angles projected anteriorly, their apex tightly rounded; lat¬
eral marginal depression of equal breadth from midlength
to front angles, about twice as broad in basal half of prono¬
tum; proepistemum smooth, proepimeron very narrow. El¬
ytra flattened overall, sutural intervals upraised at suture in
apical half of length; elytral apex evenly rounded; elytral

SiySEOHIi ?Ai>!S

\Sci/vyi'Cfc!L.

Collection Leon Fairriiairei
, J9C6

Figure 2. Specimen labels associated with holotype specimen
of Bryanites graeffii.

Striae flnely incised, completely smooth, the intervening
intervals nearly flat; humeri narrowed, with elytral basal
groove meeting lateral depression at obtuse-angulate junc¬
ture, i.e., the humerus; seventh stria with two setae near
strial apex; eighth striae with 33-37 lateral elytral setae
more or less continuously distributed along elytral length,
but with greater intersetal distances near midlength. Legs
gracile, elongate; profemur with eight setae along antero-
ventral margin; mesofemur with 8-11 setae along pos-
teroventral margin; metacoxa bisetose, two lateral setae
present anteriorly and posteriorly, median seta absent;
metafemur with eight setae along posteroventral margin,
three setae on anterodorsal surface near apex from 0.7-
0.8x femoral length; metatarsomeres 1-3 convex dorsally,
without evident inner or outer dorsal sulci; metatarsomere
4 lobate apically, length of outer apical lobe 0.4x medi¬
an tarsomere length, length of inner lobe 0.25x median
length; tarsomeres 1-4 with two parallel longitudinal rows
of elongate ventrolateral setae each side of a central space,
the setae of inner rows each side about half as long as se¬
tae of outer rows; metatarsomere 5 apparently with eight
ventrolateral setae, equal in length to tarsomere depth, set
in two longitudinal rows (several setae broken off). The
pronotum and elytra of the type specimen are covered with
a varnish-like substance that can be scraped off with difli-

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Liebherr, J.K.: Bryanites graeffii sp. n.

Lorostema ogurae (Jp)

Lorostema bothriophora (NC+V+T)

Lorostema informalis (NG)

Lorostema subnitens (l+Sunda)

Lorostema alutacea (l+As)*

Lorostema interstitialis (Ph)

Blackburnia posticata (HI)

Blackburnia mandibularis (HI)

Blackburnia costata (HI)

Blackburnia kahili (HI)

Notagonum marginicolle (Au)

>Vitagonum apterum (F)*

Bryanites graefFii sp. n. (Sa)

Bryanites samoaensis (Sa)*
•Ctenognathus otagoensis (NZ)
Ctenognathus bidens (NZ)
Ctenognathus parabilis (NZ)
Notagonum kanak comb. n. (NC)

Notagonum delaruei (V)

Notagonum angulum (NG)

Notagonum externum (NG) *
Notagonum lafertei (Au+NC+V)

607 step-length strict
consensus of 47 trees;
each 566 steps, with
Cl = 0.22, Rl = 0.56

Colpodes brunneus (Jv)*

Colpodes latus (Jv)

Violagonum piceum (V+Sa)

>Violagonum violaceum (Au+NG+So)*

Helluocolpodes helluo (NG)*

Helluocolpodes discicollis (V)

Helluocolpodes mucronis (V)

Helluocolpodes multipunctatus (V)

Helluocolpodes sinister (V)

Helluocolpodes vanemdeni (V)

Colpodes nigratus (F)

Colpodes n sp peckorum (F)

Colpodes xanthocnemus (F)

Colpodes anachoreta (T)

Colpodes eremita (T)

Plicagonum kaindi (NG)

Colpodes n sp opacidermis (F)

Metacolpodes monticola (T)

Metacolpodes buchanani (As)*
Metacolpodes buxtoni (Sa)
Metacolpodes cyaneus (NC)
Metacolpodes pacificus (Sa)
Metacolpodes laetus (Ph)
Metacolpodes laetus (V)
Metacolpodes hopkinsi (Sa)

Metacolpodes truncatellus (F)
Metacolpodes truncatellus (NG)

Figure 3. Strict consensus dado gram of 49 taxa of Pacific platynine carabid beetles. Type species, where included, indicated by as¬
terisks. See text for further explanation of cladistic analysis. Distributional areas of species include; As, Asia; Au, Australia; F, Fiji;
HI, Hawaiian Islands; I, India including Sri Lanka; Jp, Japan; Jv, Java; NC, New Caledonia; NG, New Guinea; NZ, New Zealand;
Ph, Philippine Islands; R, Rapa; Sa, Samoa; So, Solomon Islands; Sunda, Sunda Islands; T, Tahiti and Society Islands; V, Vanuatu.

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Zoosyst. Evol. 93 (1) 2017, 1-11

Figure 4. Male aedeagus, internal sac everted, of Bryanites
graeffii male holotype, right lateral view. Abbreviations in¬
clude; ae, aedeagal median lobe; is, internal sac; Ip, left param-
ere; rp, right paramere.

culty (Fig. 1). The head, ventral surface, legs, and elytral
lateral marginal depression are not so covered, suggesting
that this coating is associated with the specimen in life, not
an artifact of preservation.

Male genitalia. Aedeagal median lobe elongate, evenly
narrowed from midlength to apex extended 4.Ox its dor-
soventral breadth beyond the apex of the ostial opening
(Fig. 4); aedeagal tip slightly expanded, apical surface of
tip tightly rounded; right paramere slightly shorter and
narrower than left; aedeagal internal sac fusiform (flat¬
tened under cover slip), with a fleld of more heavily scle-
rotized spicules distributed apically near gonopore.

Type. Holotype male (MNHN): Dr Gratfe / Samoa //
8284 // MUSEUM PARIS / Samoa / Collection Leon
Fairmaire / 1906 // HOLOTYPE / Bryanites / graeffii /
J.K. Liebherr 2016 (black-margined red label). The type
locality is designated as the mountains near Apia, Upolu
island, based on GraelFe (1917); his autobiography notes
his residing at Apia during his tenure in Samoa. He vis¬
ited other islands in the Fijian and Tongan archipelagos,
but did not mention any visits within Samoa to the islands
of SavaiT or Tutuila. Moreover, the following passage for
the year 1869, after he had published his popular book
describing a trip to Viti Levu (Graetfe 1868), suggests
the time period during which he could have collected the
specimen here described as Bryanites graeffii. “Es wurde
nun wieder tiichtig geforscht und zog ich fast taglich mit
meinem Gewehr in die Waldungen des Apiaberges, Vo¬
gel und grosse Fledermause, Pteropus samoaensis Peale
erlegend, Insekten und Landschnecken, sowie Pflanzen
sammelnd (Graetfe 1917: 31) [It was now again time for
me to diligently conduct research, going almost daily
with my rifle into the woods of the Apia mountains to
gather birds and big bats, Pteropus samoaensis Peale, in¬
sects and snails, as well as plants].” A collection made in
1869 would have had to wait only a year before Graetfe
left Samoa to return to Hamburg, allowing safe preser¬
vation of a specimen held in the humid tropical Paciflc.
In an ironic coincidence, Apia is also the type locality of
the extinct flying fox, Pteropus allenorum Helgen, Hel-
gen and Wilson, 2009 (Mammalia: Chiroptera) , known
from a unique holotype collected in 1856 that was recent¬
ly rediscovered in the Academy of Natural Sciences of
Philadelphia (Helgen et al. 2009).

Etymology. The species epithet honors Dr. Eduard Graef-
fe, zoologist and naturalist from Zurich, Switzerland who
collected the type specimen while working in Samoa from
1862-1870 (Clunie & Snow 1986). The species epithet is
formed from Gratfe converted to Latin iconography, and
without the terminal letter. This formation is consistent
with several other honorific epithets for Eduard Gralfe;
e.g. Epeira graeffii Keyserling (Arachnida: Araneidae),
now combined with Phonographa Simon, 1894, Lamel-
lidoris graeffii Bergh (Nudibranchia: Dorididae), and
Pachycephala pectoralis graeffii Hartlaub (Aves: Pachy-
cephalidae).

Nomenclatural note

Based upon the results of the cladistic analysis, Colp-
odes kanak Fauvel is newly combined with the genus
Notagonum Darlington: Notagonum kanak (Fauvel)
comb. n. (Suppl. material 1). This taxonomic decision
is based on N. kanak exhibiting the following charac¬
ter states that place it within the Notagonum grade (Fig.
5, Suppl. material 2): 1, frons with evident isodiametric
microsculpture that is visible through the surface reflec¬
tion; 2, pronotal basal bead visible laterally but effaced
at midline; 3, pronotal laterobasal depressions smooth,
not punctate; 4, pronotal disc with evident transverse mi-

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Liebherr, J.K.: Bryanites graeffii sp. n.

- 1.0 mm

Figure 5. Notagonum kanak female (MNHN), label data:
Ncaledonie / lie d. Pins / f. Faustien // MUSEUM PARIS / Ex.
Coll. M. MAINDRON / Coll. G. BABAUET 1930 // Colpodes
/ kanak / Fauvel dedit 1906 (card mounted, abdomen removed,
female genitalia and reproductive tract in vial on pin).

crosculpture; 5, margins of prosternal process rounded
on posterior face; 6, short elytral sutural tooth present,
subapical tooth absent; 7, metatarsomere 4 with shallow
apicomedial ventral invagination and short lateral lobes,
the outer, or lateral lobe, less than twice the length of the
inner lobe.

Discussion

The results of the cladistic analysis suceeed in the goal
of placing the new species as a member of a Samoan lin¬
eage, Bryanites, that exhibits a close biogeographic re¬
lationship to the Fijian relict, Vitagonum (Moore 1998).
This clade, and its sister group Ctenognathus of New
Zealand, diverged early in the history of Pacific Platynini.
Previously, Liebherr (2005) concluded that the Hawaiian
genus Blackburnia colonized the Hawaiian Island ehain
long before the origins of the present high islands, and
perhaps as long ago as 28 Mya when Kure became the
first in a eonsistently present subaerial chain of islands

generated by the Hawaiian Island volcanic hotspot (Dun¬
can and Clague 1985). In the Samoan Island chain, the
Alexa Bank seamount is hypothesized to have originated
as a subaerial island 22 Ma (McDougall 2010), setting
the earliest date possible for colonization of the Samoan
Islands hotspot volcanic chain by a Bryanites ancestor.
Subaerial origin of the Fijian archipelago is dated to a
similar time—22-25 Ma (Gill and MeDougall 1973,
Whelan et al. 1985)—establishing a maximal time of or¬
igin for the ancestor of Vitagonum. And volcanism along
the Kermadec-Lau-Tonga Ridge system would have en¬
hanced colonization prospects for the ancestor of New
Zealand Ctenognathus 10—15 Mya. Thus all area rela¬
tionships among the early diverging Pacific platynine lin¬
eages, including Bryanites, occupy continental areas or
island chains available for colonization in the Mioeene.
This supports Valentine’s (1987) hypothesis that Bry¬
anites is a relict Samoan lineage.

The question of whether any or all of the Bryanites
speeies are extinct is necessarily open ended. Neverthe¬
less, examination of the circumstances of their collections
taken within the context of other biological surveys of
Samoa paint a grim picture as to the possibility of their
eontinued existence in nature. The single specimen of
Bryanites graeffii was collected prior to 1871 by a nat¬
uralist principally interested in birds and marine inver¬
tebrates (Graetfe 1917). Nonetheless, we know that he
colleeted insects during his trips to Fiji (Graetfe 1868),
and during 1869 near Apia (Graetfe 1917). But only the
one specimen of B. graeffii described herein is known
to have passed to Leon Fairmaire for eventual deposi¬
tion in the Paris Museum. The British Museum survey
of 1924-1925 (Kami and Miller 1998), summarized for
Carabidae by Andrewes (1927), led to description of five
other platynine carabids— Colpodes buxtoni Andrewes,
C. pacificus Andrewes, C. hopkinsi Andrewes, C. piceus
Andrewes, and C. anomalus Andrewes, the first three of
which are now assigned to Metacolpodes (Fig. 3, Suppl.
material 1; Liebherr 2005). Andrewes (1927) also exam¬
ined previously collected taxonomic material, includ¬
ing that from 1905 collections for the Vienna Museum
(Rechinger 1914) and 1912-1913 collections for the Ber¬
lin Museum (Friedrichs 1914).

The Bishop Museum’s Whitney South Seas Expedi¬
tion of 1924, including E. H. Bryan, Jr. as entomologist,
also visited Samoa (Evenhuis 2007). Bryan’s field notes
for 23 May 1924-the date labeled on the two speeimens
later deseribed as Bryanites (Valentine 1987)-included:
“Put away large quantity of specimens collected yester¬
day (Evenhuis 2007: 125).” Some of those “yesterday’s”
specimens were collected when he “Dug several things
from partly rotten bank [sic bark] of large tree:- centi¬
pedes, termites, sowbugs, tree cricket and moderately
large slender fuscous Carabid (Evenhuis 2007: 125).”
Given that the deseription of a “moderately large slen¬
der fuscous Carabid” on Samoa can only fit a Bryanites
beetle, it appears that Bryanites, either the B. barri or B.
samoaensis individual that Bryan collected, was associ-

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Zoosyst. Evol. 93 (1) 2017, 1-11

ated with a downed log covered with rotten bark. Bryan
described the situation within which he was collecting
at that camp as “Two large Ac[h]atinella [^zc] landshells
on Orange tree in banana patch at about 2200’. [Met]
Mr. Beck and returned to hut. Mosquitoes not bad, but
rats after our provisions. Very good collecting at this
elevation (Evenhuis 2007: 125).” Being a field biologist
based on Oahu, Bryan no doubt mistook a native Sa¬
moan Samoana or Eua land snail (Pilsbry 1909-1910,
Cowie 1992) for the precinctive Oahu genus Achatinel-
la, but his sighting of native land snails in proximity to
rats in 1924 suggests that the native elements did not
have long to exist at the site given the presence of inva¬
sive rats. There is both indirect and direct evidence that
rats prey on native brachypterous carabid beetles. De¬
posits in Makauwahi Cave on Kauai include abundant
subfossil fragments of extinct, brachypterous Blackbur-
nia carabid beetles in stratigraphic layers deposited pri¬
or to human colonization and the associated introduc¬
tion of the Pacific rat, Rattus exulans (Peale) (Liebherr
and Porch 2015). Subfossil fragments of those presently
extinct taxa are absent from the stratigraphic column in
deposits laid down from shortly after the time of hu¬
man colonization up to the present. More directly, stom¬
ach contents of alien black rats {Rattus rattus L.) have
been shown to include fragments of a native Hawaiian
Blackburnia beetle species, as well as native katydids,
weevils and spiders (Shiels et al. 2013). The presence
of predatory, climbing, night active rats is uniformly
deleterious to native communities on tropical islands
(Harper and Bunbury 2015), with Samoa not a likely
exception to this rule.

Given these various lines of data, it seems unlike¬
ly that Bryanites beetles currently exist in nature. Only
through the perspicuous collecting by E. H. Bryan, Jr. and
the passing of his two specimens to J. Manson Valentine
could the first two species of this genus be described (Val¬
entine 1987). The subsequent discovery of a single addi¬
tional specimen collected over 140 years ago that traveled
a circuitous route from Samoa, to the Museum Godeflfroy,
to the Paris Museum adds another entry point to study of
the Bryanites radiation. Are we better for knowing about
this evolutionary story even after all known players have
likely left the scene? To the degree that the hotspot vol¬
canic chain of Samoa supported a very unique radiation
of platynine Carabidae, as did Hawaii, we have learned
that the Blackburnia radiation of Hawaii had an analog
in Samoa, with Samoan species inhabiting the islands of
SavaiT and Upolu. We have characterized a large-bodied,
distinctive species that may turn up in Samoan subfossil
deposits, much like the large-bodied subfossil Blackbur¬
nia spp. of Kauai (Eiebherr and Porch 2015). And should
these or any other Bryanites beetles have survived forest
conversion, and the plagues of rats and other invasive
species so that they may be collected during a future bi¬
ological survey, that sample will be connected to speci¬
mens held in two other biodiversity hotspots on Earth.

Acknowledgements

The curators at the Bishop Museum, Honolulu, and the
Museum national d’Histoire naturelle, Paris have gra¬
ciously let me work in their collections over the years
with free access to specimens and with a minimum of
distractions. I thank the following for their support of my
curatorial and collection-based research efforts: James
Boone, Neal Evenhuis, Scott E. Miller, Gordon Nishida,
G. Allan Samuelson (Bishop Museum); Thierry Deuve,
Jean Menier, Helene Perrin, Azadeh Tagavian (Paris
Museum). I thank Martin Baehr, Zoologische Staats-
sammlung Miinchen, for sharing his findings regarding
species identities in the Notagonum marginellum-subme-
tallicum-complQx. The underlying research on Hawaiian
platynine beetles was supported by National Science
Foundation grants DEB-9208269, DEB-9806349, and
DEB-0315504.

References

Andrewes HE (1927) Coleoptera, Carabidae. In: Andrewes HE, Austen
EE (Eds) Insects of Samoa and other Samoan Terrestrial Arthropo-
da. Part 4(1). Trustees of the British Museum, Eondon, 14 pp.
Clunie F, Snow PA (1986) Notes to accompany English translation of
“Travels in the interior of the island Vitilevu” by Eduard Graelfe.
Domodomo 4: 130-140.

Cowie RH (1992) Evolution and extinction of Partulidae, endemic
Pacific Island land snails. Philosophical Transactions of the Roy¬
al Society of Eondon B 335: 167-191. https://doi.org/10.1098/
rstb. 1992.0017

Darlington PJ Jr (1952) The carabid beetles of New Guinea part 2. the
Agonini. Bulletin of the Museum of Comparative Zoology 107:
89-252. [4 pis]

Duncan RA, Clague DA (1985) Pacific plate motion recorded by lin¬
ear volcanic chains. In: Nairn AEM, Stehli EG, Uyeda S (Eds) The
Ocean Basins and Margins. Plenum Press, New York, 89-121.
https ://doi.org/l 0.1007/978-1 -4613-2351 -8_3
Erwin TE, Erwin JE (1971) A guide to the ground beetle collection
in the Museum National d’Histoire Naturelle, Paris (Coleoptera:
Carabidae). Smithsonian Institution Duplicating Unit, Washington,
D.C., 22 pp. http://entomology.si.edu/StaffPages/Erwin/T’s%20up-
dated%20pub%20PDFs%2010 Jan2014/015_197 l_GroundBeetle-
Collection_ParisMuseum.pdf

Evenhuis NE (compiler) (2007) Field Notes of E.H. Bryan, Jr. on the
Whitney South Seas Expedition (February-November 1924). Bish¬
op Museum Technical Report 37: 1-334.

Fairmaire E (1878) Diagnoses de Coleopteres des iles Viti, Samoa, Tonga,
etc. Petites Nouvelles Entomologiques 2(210): 286.

Fairmaire E (1879a) Descriptions de Coleopteres nouveaux ou peu con-
nus du Musee Godefffoy. Journal des Museum Godefffoy 14: 80-114.
Fairmaire E (1879b) Diagnoses de Coleopteres Australiens et
Polynesiens. Ee Naturaliste 1(9): 70.

Fairmaire E (1881a) Diagnoses de Coleopteres de la Melanesia. Ee Natu¬
raliste 3(43): 348-349.

Fairmaire E (1881b) Essai sur les Coleopteres des iles Viti (Fidgi). Annales
de la Societe Entomologique de France (ser. 6) 1: 243-318.

zse.pensoft.net

Liebherr, J.K.: Bryanites graeffii sp. n.

Fauvel A (1903) Faune analytique des Coleopteres de la Nou-
velle-Caledonie. Revue d’Entomologie 22: 203-378.

Friedrichs R (1914) \Jher Adoretus vestitus Boh. als Schadling im Sa¬
moa, und seine fruheren Stande. Zeitschrift fiir Wissenschaftliche
Insektenbiologie Berlin 10: 41-47.

Gill JB, McDougall I (1973) Biostratigraphic and geological signifi¬
cance of Miocene-Pliocene volcanism in Fiji. Nature 241: 176-180.
https://doi.org/10.1038/241117a0

Golobolf PA (1999) NONA (NO NAME). Published by the author,
Tucuman, Argentina. http://www.softpedia.com/get/Science-CAD/
NONA.shtml [accessed 16-ix-2016]

Graetfe E (1866) Notizen fiber die Faune der Viti-Inseln. Verhandlun-
gen der Kaiserlich-Konigliche Zoologisch-Botanische Gesellschaft in
Wien 16: 585-596.

Graelfe E (1868) Reisen im Innern der Insel Viti-Eevu. Zfircher and
Furrer, Zfirich, 48 pp. [2 pis]

Graelfe E (1870) Ornithologische Mitteilungen aus Central-Polynesien.
Journal ffir Ornithologie 18(108): 401-420. https://doi.org/10.1007/
BF02259500

Graeflfe E (1873a) Topographic der Schilfer-inseln. Journal des Muse¬
um Godeflfoy 1: 1-32.

Graelfe E (1873b) Vogelbalge aus Huahine. Journal des Museum Go-
defffoy 1: 48-51.

Graeflfe E (1917) Meine Biographic in meinem 80. Eebensjahre ges-
chreiben. Vierteljahrsschrift der Naturforschenden Gesellschaft in
Zfirich 61: 1-39.

Harper GA, Bunbury N (2015) Invasive rats on tropical islands: their popu¬
lation biology and impacts on native species. Global Ecology and Con¬
servation 3: 607-627. http://creativecommons.Org/licenses/by-nc-nd/4.0

Helgen KM, Helgen EE, Wilson DE (2009) Pacific Hying foxes (Mam¬
malia: Chiroptera): two new species of Pteropus from Samoa, prob¬
ably extinct. American Museum Novitates 3646: 1-37.

Hennig W (1966) Phylogenetic Systematics. University of Illinois
Press, Urbana, 263 pp.

Kami KS, Miller SE (1998) Samoan insects and related arthropods: check¬
list and bibliography. Bishop Museum Technical ReportNo. 13,136 pp.

Eiebherr JK (1998) On Rembus {Colpodes) brunneus MacEeay
(Coleoptera: Carabidae, Platynini): redescription and relation¬
ships. Journal of Natural History 32: 987-1000. https://doi.
org/10.1080/00222939800770511

Eiebherr JK (2005) Platynini (Coleoptera: Carabidae) of Vanuatu: Mio¬
cene diversification on the Melanesian arc. Intertebrate Systematics
19: 263-295. http://dx.doi.org/10.1071/IS04032

Eiebherr JK (2015) The Mecyclothorax beetles (Coleoptera: Carabidae:
Moriomorphini) of Haleakala, Maui: keystone of a hyperdiverse
Hawaiian radiation. ZooKeys 544: 1-407. https://doi.org/10.3897/
zookeys.544.6074

Eiebherr JK, Porch N (2015) Reassembling a lost lowland carabid bee¬
tle assemblage (Coleoptera) from Kauai, Hawaiian Islands. Inver¬
tebrate Systematics 29: 191-213. http://dx.doi.org/10.1071/IS14047

Eorenz W (2005) Systematic list of extant ground beetles of the world
(Insecta: Coleoptera: “Geadephaga”: Trachypachidae and Carabidae
incl. Paussinae, Cicindelinae, Rhysodinae) [2"‘' edn]. Published by
the author, Tutzing, 530 pp.

McDougall I (2010) Age of volcanism and its migration in the Samoa Is¬
lands. Geological Magazine 147: 705-717. https://doi.org/10.1017/
SOO16756810000038

Maddison DR (2012) Phytogeny of Bembidion and related ground bee¬
tles (Coleoptera: Carabidae: Trechinae: Bembidiini: Bembidiina).
Molecular Phylogenetic & Evolution 63: 533-576. http://dx.doi.
org/10.1016/j.ympev.2012.01.015

Moore BP (1998) A new genus and species of flightless Carabidae (Co¬
leoptera) from Fiji. Australian Entomologist 25: 103-106.

Nixon KC (1999) The parsimony ratchet, a new method for
rapid parsimony analysis. Cladistics 15: 407-414. https://doi.
org/10.1111/j. 1096-0031.1999.tb00277.x

Nixon KC (2002) WinClada. Ithaca, NY, Published by the author, http://
www.softpedia.com/get/Science-CAD/WinClada.shtml [accessed
16-ix-2016]

Pilsbry HA (1909-1910) Caecilioides, Glessula and Partulidae. Manual of
Conchology (2"‘' Ser.) 20. Academy of Natural Sciences, Philadelphia,
336 pp. [43 pis]

Rechinger K (1914) Botanische und zoologische Ergebnisse einer wis-
senschaftlichen Forschungsreise nach den Samoainseln, dem Neu-
guinea-Archipel und den Salomoninseln von Marz bis Dezember
1905, V. Teil. Denkschriften der Kaiserlichen Akademie der Wis-
senschaften Wien 89: 443-708.

Shiels AB, Flores CA, Khamsing A, Krushelnycky PD, Mosher SM,
Drake DR (2013) Dietary niche differentiation among three species
of invasive rodents (Rattus rattus, R. exulans, Mus musculus). Bio¬
logical Invasions 15: 1037-1048. doi:10.1007/sl0530-012-0348-0

Valentine JM (1987) Some ancient and zoogeographically significant
carabid beetles from the South Pacific (Coleoptera: Carabidae), with
descriptions of new taxa. Bishop Museum Occasional Papers 27:
73-89.

Whelan PM, Gill JB, Kollman E, Duncan RA, Drake RE (1985) Radio-
metric dating of magmatic stages in Fiji. In: Scholl DW, Vallier TE
(Eds) Geology and offshore resources of Pacific Island arcs - Tonga
Region. Circum-Pacific Council for Energy and Mineral Resources,
Houston, 415-440.

Will KW, Eiebherr JK, Maddison DR, Galian J (2005) Absence
asymmetry: the evolution of monorchid beetles (Insecta: Coleop¬
tera: Carabidae). Journal of Morphology 264: 75-93. https://doi.
org/10.1002/jmor.l0319

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Zoosyst. Evol. 93 (1) 2017, 1-11

Supplementary material 1

Taxonomic checklist

Authors: James K. Liebherr

Data type: Adobe PDF file

Explanation note: Taxa included in cladistic analysis taxo-
nomically placing Bryanites graeffii sp. n. are listed
along with their taxonomic authorities.

Copyright notice: This dataset is made available under
the Open Database License (http://opendatacommons.
org/licenses/odbl/1.0/). The Open Database License
(ODbL) is a license agreement intended to allow us¬
ers to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided
that the original source and author(s) are credited.

Supplementary material 2

Computer file for cladistic analysis

Authors: James K. Liebherr

Data type: Adobe PDF file

Explanation note: The NONA format data file that supports
the cladistic analysis of Bryanites and Pacific Platynini
is provided for export to a plain text editor.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 13-34 | DOI 10.3897/zse.93.10769

4>yEnsPFr.

museum fur naturkunde

The diversity of aeom bamaeles (Cirripedia, Balanomorpha) aeross
Thailand’s eoasts: The Andaman Sea and the Gulf of Thailand

Ashitapol Pochai^ Sutin Kingtong\ Woranop Sukparangsi\ Salinee Khachonpisitsak^

1 Department of Biology, Faculty of Science, Burapha University, Chon Buri, Thailand

http://zoobank.org/9FF0B30A-A535-48DE-B756-BDlC0DFE2B92

Corresponding author; Salinee Khachonpisitsak.ac.VC)

Received 11 October 2016
Accepted 7 December 2016
Published 11 January 2017

Academic editor:

Michael Ohl

Key Words

acorn barnacle

Cirripedia

Balanomorpha

shell morphology

opercular valve

distribution

Thailand

Abstract

The acorn barnacle is a sessile crustacean, inhabiting the intertidal areas of tropical and
temperate regions worldwide. According to current practices on Cirripedia morpholo¬
gy, shell, opercular valves, and arthropodal characters including cirri and mouthparts
are used as a tool for taxonomic classification, and using these characteristics the pres¬
ent study aimed to provide better resolution for the barnacle diversity and geographical
distribution within coastlines of Thailand; the Andaman Sea and the Gulf of Thailand.
A total of ten species belonging to three families (Chthamalidae, Tetraclitidae, and Bal-
anidae) were identified in this study. Subsequently, five species were newly recorded for
the first time from Thailand’s coasts: Newmanella spinosus Chan & Cheang, 2016, Eu-
raphia hembeli Conrad, 1837, Euraphia depressa (Poli, 1795), Tetraclita kuroshioensis
Chan, Tsang & Chu, 2007, and Tetraclita singaporensis Chan, Tsang & Chu, 2007. The
others, already mentioned in previous records, include: Tetraclita squamosa (Bruguiere,
1789), Chthamalus malayensis Pilsbry, 1916, Amphibalanus amphitrite (Darwin, 1854),
Amphibalanus reticulatus (Utinomi, 1967), and Megabalanus tintinnabulum (Linnae¬
us, 1758). Interestingly, acorn barnacles along the Andaman Sea occur abundantly, and
are much higher in number of species (up to 8 species) than those found in the Gulf of
Thailand’s coast (up to 6 species). This biased trend of species’ preferences is possibly
due to the differences in oceanographic nature between two coastlines and the history of
barnacle colonization.

Introduction

Acorn barnacles, a member of marine crustaceans, in¬
habit a diverse array of substrates (e.g. calcareous rock
or limestone, mollusk shells, corals, sponges, mangrove
roots, turtle shells, and whale skins) along intertidal zones
of temperate and tropical coastlines worldwide, as ses¬
sile form throughout their adulthood (Frith et al. 1976;
Sophia Rani et al. 2010; Brickner and Hoeg 2010; Brick-
ner et al. 2010; Chen et al. 2012; Hayashi 2013; Chen et
al. 2014; Yu et al. 2016). It is known as a marine foul¬
ing or biofouling organism and it has been considered
as a problematic or invasive species for oyster farming,
aquaculture, the reforestation of mangrove swamps, and
for the support structures of offshore oil rig platforms
and ship transport (Santhakumaran and Sawant 1991;
Rawangkul et al. 1995; Molnar et al. 2008; Sophia Rani

et al. 2010; Holm 2012). Although the presence of hard
calcareous plates covering acorn barnacles’ bodies lim¬
its abilities to search for food and new habitats, the spe¬
cies are still tremendously successful in occupying the
coastline of tropical and temperate regions due to their
free-swimming and planktonic larval stages: high-feed¬
ing nauplius and non-feeding cyprid. The nauplius larva
develops in successive manner with ecdysis or molting
to shed their exoskeleton and allow growth of larva, a
characteristic used to classify acorn barnacles into Ec-
dysozoa of Protostomia clade. The metamorphosis (set¬
tlement process) alters a cyprid larva to a sessile juvenile
and subsequently an adult form growing inside the ring
of shell plates (4-8 in number depending on the species),
homologous structure to carapace of other crustaceans
(Hoeg and Moller 2006; Maruzzo et al. 2012; Martin
et al. 2014). The sessile body of adult barnacles has six

Copyright Ashitapol Pochai et al. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

pairs of featherly throracic appendages called cirri (legs
or feeding appendages), so named suborder Cirripedia
constituted inside order Sessilia and superorder Thoraci-
ca. With highly suitable habitats and temperature ranges,
diverse forms of acorn barnacles occur along coastlines
in both the Andaman Sea and the Gulf of Thailand. How¬
ever, the taxonomic classification alongside geographical
distribution information of acorn barnacles has received
little attention in Thailand. Here we aim to investigate
taxonomy, shell morphology, and geographical distribu¬
tion by firstly relating the taxonomic key of acorn barna¬
cles to their distribution records along the Andaman Sea
and the Gulf of Thailand coasts to elucidate the diversity
of the species across the coastlines of Thailand.

Material and methods

study sites

Acorn barnacles were collected from the rocky coastal
areas of two distinct geographic regions of Thailand:
the Andaman Sea and the Gulf of Thailand, during May
2015-July2016.

The Andaman Sea located in the eastern part of the
Indian Ocean is bordered by the coastlines of Myanmar,
Thailand, Malaysia, Indonesia and India. In the Andaman
Sea, the tide is semidiurnal. Its water temperature and
salinity range 25.9-30.4°C and 29-33 ppt, respectively
(Limpsaichol et al. 1991). Five sampling sites along the
Andaman Sea coast comprised of (1) Ao Khoei beach,
Khura Buri district, Phang-nga province, (2) Na Tai
beach, Takua Thung district, Phang-nga province, (3)
Kalim beach, Katu district, Phuket province, (4) Ao Yon
beach, Mueang Phuket district, Phuket province, and (5)
Panwa beach, Mueang Phuket district, Phuket province.

The Gulf of Thailand, a semi-enclosed sea, is bordered
by the coastlines of Vietnam, Cambodia, Thailand, and
Malaysia with a connection to the South China Sea in
the south. In the Gulf of Thailand, the tide is mixed di¬
urnal. Its water temperature and salinity range 29-32°C
and 30-33 ppt, respectively (Pollution Control Depart¬
ment 2001). Five sampling sites along the coastline of the
Gulf of Thailand were investigated, comprising (1) Khao
Sam Muk beach, Mueang Chon Buri district. Chon Buri
province, (2) Si Racha beach. Si Racha district. Chon Buri
province, (3) Ko Kham Yai beach, Ko Si Chang district.
Chon Buri province, (4) Ban Krut beach. Bang Saphan
district, Prachuap Khiri Khan province, and (5) Hin Ngam
beach, Sichon district, Nakhon Si Thammarat province.

A synopsis and illustration of all the sampling loca¬
tions are given in Table 1 and Figure 1.

Sampling collection

The barnacles were collected from each station by sur¬
veying along rocky shores of an intertidal zone during
both low and high tides. Whole acorn barnacle individu¬
als were removed from the substratum and immediately
preserved in ethyl alcohol (95%v/v) for further examina-

Table 1. Sampling locations, arranged from north to south.

Locality

Habitat

characteristics

Coordinates

Andaman Sea coast

Ao Khoei

Large boulders on
sandy shores

09°16’44.18”N

98°22’07.01”E

Na Tai

Rocky shores

08°14’15.39”N

98°16’51.22”E

Kalim

Small to large rocks
on sandy shores

07°55’25.47”N

98°15’47.68”E

Ao Yon

Rocky shores

07°52’09.79”N

98°26’08.29”E

Panwa

Large boulders on
sandy shores

07°48’05.09”N

98°24’28.80”E

Gulf of Thailand coast

Khao Sam Muk

Rocky shores

013°18’38.88”N

100°54’07.81”E

Si Racha

Large boulders on
sandy shores

013°10’33.92”N

100°55’33.74”E

Ko Kham Yai

Small rocks on
sandy shores

013°09’59.30”N

100°49T8.00”E

Ban Krut

Rocky shores

011°21’26.07”N

099°34’42.86”E

Hin Ngam

Rocky shores

009°00’00.68”N

099°55’09.45”E

tion. All work was done under certified supervision of
S.K. (Certificate from Institute of Animal for Scientific
Purposes Development-IAD, Royal Thai Government:
Ul-03104-2559).

Morphology analysis

Samples were primarily identified based on their shell
morphology using an Olympus SZ51 stereomicroscope
and was photographed with digital camera. For better
species identification in some families, arthropodal char¬
acters were observed. Soft bodies were removed from the
shells and dissected. Cirri and mouthparts were mounted
onto slides for light microscopy observation and imaging
using digital camera. Taxonomic identification was per¬
formed using keys of Newman and Ross (1976) and Chan
et al. (2009). The general terminology of shell morphol¬
ogy and the important characters used in this paper fol¬
low Chan et al. (2009). All voucher specimens from each
station were deposited in the collection of Laboratory of
Zoology, Department of Biology, Faculty of Science, Bu-
rapha University, Thailand.

Results

Based on shell morphology, total ten species (6 genera) of
acorn barnacles along the coastlines of Thailand in both
the Andaman Sea and the Gulf of Thailand were identi¬
fied and are categorized into three families: Chthamal-
idae (2 subfamilies: Chthamalinae and Euraphiinae),
Tetraclitidae (2 subfamilies: Newmanellinae and Tetra-
clitinae), and Balanidae (2 subfamilies: Amphibalaninae
and Megabalaninae). The descriptions of the identified
barnacles are as follows:

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Zoosyst. Evol. 93 (1) 2017, 13-34

Andaman

Gulf of
ThEiiland

14°00'N

12“00'N

10“00'N

• NT

KL'#'0ay

*PW

98°00'E

08“00'N

lOrOO'E

Andaman

sea

Gulf of
Thailand

Figure 1. Map showing all sampling locations (A) and habitat characteristics (B) of acorn barnacles found along the coastlines of the An¬
daman Sea and the Gulf of Thailand. See Table 1 for acronyms of sampling sites, (modified from http://marinegiscenter.dmcr.go.th/gis/)

Systematic taxonomy

Superorder Thoracica Darwin, 1854
Order Sessilia Lamarck, 1818
Suborder Balanomorpha Pilsbry, 1916
Superfamily Chthamaloidea Darwin, 1854
Family Chthamalidae Pilsbry, 1916
Subfamily Chthamalinae Darwin, 1854

Genus Chthamalus Ranzani, 1817

Type species. Chthamalus stellatus (Poli, 1791)

1 genus, 1 species recorded: Chthamalus malayensis
Pilsbry, 1916.

Chthamalus malayensis Pilsbry, 1916

Figure 2; Tables 2-3

Chthamalus malayensis Pilsbry, 1916: 310-311; Hiro, 1939: 249-251;
Utinomi, 1954: 18; Karande & Palekar, 1963: 231; Pope, 1965: 51-
63; Newman & Ross, 1976: 42; Dong et al., 1980: 125; Ren, 1984:
151-153; Southward et al., 1998: 123.

Chthamalus stellatus’. Hoek, 1913: 267-269.

Chthamalus challenger’. Broch, 1931: 53-55; 1947: 5.

Chthamalus antennatus. Rossq\, 1972: 174, pi. 13, figs. 1-7, pi. 14, fig. 1-5.

Non-type material examined. Andaman Sea: 3 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai

beach, 16.V.2015, A. Pochai (BUU16.CH.CM01-03).
2 specimens, Phuket province, Mueang Phuket dis¬
trict, Ao Yon beach, 15.VII.2015, A. Pochai (BUU16.
CH.CM04-05). 1 specimen, Phuket province, Mueang
Phuket district, Panwa beach, 16.VII.2015, S. Khachon-
pisitsak (BUU16.CH.CM06). 3 specimens, Phuket prov¬
ince, Katu district, Kalim beach, 15.VII.2015, A. Pochai
(BUU16.CH.CM07-09).

Gulf of Thailand: 2 specimens. Chon Buri province,
Ko Si Chang district, Ko Kham Yai beach, 05.VII.2015,
S. Khachonpisitsak (BUU16.CH.CM10-11).

Description. Peduncle absent; body length 3-10 mm;
base membranous. Shell elongated oval/shield-shaped,
shell white to grey with 6 plates (1 carina, 2 carinal latus,
2 latus and 1 rostrum), carina bigger than rostrum, pari-
etes symmetrical, calcareous and solid, radii solid, inner
surface of parietes smooth and white-grey to pale-violet;
orifice kite-shaped. Operculum plates symmetrical, artic¬
ulation of opercular valves deep, scutum and tergum sep¬
arable. Tergum smaller than scutum, tergum higher than
wide, tergum with 4 distinct crests for lateral depressor
muscles. Scutum elongated and triangular, adductor pit
deep. Mandible with 4 teeth, lower margin pectinated,
three large setae at the edge; cirri I with conical spines;
cirri II with multi-cuspidate setae and basal guard.

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Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

Figure 2. Chthamalus malayensis collected from Ka Lim beach, Phuket (BUU16.CH.CM07). A. Dorsal and ventral view of ex¬
ternal shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. External
(upper panel) and internal (lower panel) view of shell plates, D-G. Eight microscopy on mouthparts, D. Close up of cirri I showing
conical spines(^), E. Cirri II, F. Close up on cirri II showing multi-cuspidate setae with basal guard(4'), G. Mandible with four
large teeth. D-G. Scale bars in pm. Abbreviations: c, carina; cl, carinal latus; 1, latus; r, rostrum.

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Zoosyst. Evol. 93 (1) 2017, 13-34

Table 2. Species list and distribution of acorn barnacles found in ten sampling sites along the coastlines of the Andaman Sea and the
Gulf of Thailand. Abbreviations: +, presence; abs, absence. See Table 1 for acronyms of sampling sites.

Sampling sites

Species

Andaman Sea

Gulf of Thailand

Chthamalus malayensis

abs

Euraphia depressa

abs

Euraphia hembeli

abs

Newmanella spinosus

abs

Tetraclita kuroshioensis

abs

Tetraclita singaporensis

abs

Tetraclita squamosa

abs

Amphibalanus amphitrite

Amphibalanus reticulatus

abs

Megabalanus tintinnabulum

abs

Total number of species

Distribution. Chthamalus malayensis is widely distribut¬
ed in the Indo-West Pacific region. It has been previously
recorded in Taiwan, Thailand, China, Philippines, Viet¬
nam, Malaysia, India and Australia (Jones 2004; Tsang et
al. 2008; Tsang et al. 2012). From the previous observa¬
tion, C. malayensis presented in both the Andaman Sea
(Phuket) and the Gulf of Thailand (Si Chang and Samui
Islands) (Tsang et al. 2012). In this study, C. malayensis
were also found in both coastlines: the Andaman Sea (Na
Tai, Kalim, Ao Yon, Panwa) and the Gulf of Thailand (Ko
Kham Yai) (Table 2).

Remarks. Chthamalus malayensis has usually 4 crests for
lateral depressor muscles while Euraphia hembeli and Eu-
raphia depressa contains distinct 10-12 crests at the ter-
gum and 3 small crests, respectively. The size of C. malay¬
ensis ranges from 3-10 mm similar to E. depressa while
that of Euraphia hembeli is much bigger (10-33 mm). In
addition, C. malayensis differs from E. depressa in two
main characters diagnosed in this study: shape of external
shell and jointing pattern of tergum and scutum. The shape
of the external shell of C. malayensis shows a distinct and
rather uniform ribbed surface from the lower region to the
apex; on the other hand, E. depressa exhibits smooth sur¬
face that is never ribbed. Secondly, marked articulation
and sinous jointing of tergum and scutum can be clearly
noticed in C. malayensis while E. depressa shows less ar¬
ticulation. However, these shell morphology is not reliable
tool for species identification among Chthamalids; hence,
we further investigate arthropodal characters. It is clear
that Chthamalus has four teeth on the mandible while
Euraphia has three teeth on the mandible. In addition, to
further identify Chthamalus into the correct species, setae
on cirri I and cirri II were observed. Our specimens of
Chthamalids have conical spines on cirri I and multi-cus¬
pidate setae with basal guard on cirri II (Figure 2F); hence,
our specimens are confirmed as C. malayensis.

Moreover, C. malayensis distributes above the verti¬
cal zonation of Tetraclita population. The overlapping
of habitats can be seen among these species and even C.

malayensis were found to attach to Tetraclita at the over¬
lapping regions of high shore and middle shore.

Subfamily Euraphiinae Newman & Ross, 1976
Genus Euraphia Conrad, 1837

Type species. Euraphia hembeli Conrad, 1837

1 genus, 2 species recorded: Euraphia depressa (Poli,
1795) and Euraphia hembeli Conrad, 1837.

Euraphia depressa (Poli, 1795)

Figure 3; Tables 2-3

Chthamalus depressus Vo\i, 1791

Chthamalus stellatus yar. depressus: Darwin, 1854.

Euraphia depressa: Utinomi (1959); Southward (1964).

Non-type material examined. Gulf of Thailand: 2

specimens. Chon Buri province, Mueang Chon Buri dis¬
trict, Khao Sam Muk beach, 05.VII.2016, W. Sukparang-
si (BUU16.CM.ED01-02).

Description. Peduncle absent; body length 3-10 mm;
base membranous. Shell light brown-yellowish brown
with 6 plates (1 carina, 2 carinal latus, 2 latus and 1 ros¬
trum), shell flatted and thin-walled; parietes symmetrical
and solid, external surface of shell without ribbed, inner
surface of parietes smooth and light brown and white
with small horizontal striations around aperture, parietes
separable, suture distinct and easily parted; orifice rhom-
boidal. Opercular plates symmetrical, tergum smaller
than scutum, scutum and tergum separable jointing be¬
tween tergum and scutum with slightly sinous. Scutum
triangular with slightly curved basal margin, external sur¬
face with shallow and horizontal striations from occlu-
dent margin to tergal margin, occludent margin of scutum
without teeth, tergal margin slightly sinous from interior
view; tergum with 2-3 lateral depressor crests. Mandible
with 3 teeth, lower margin pectinated with 8 setae, three

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Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

Figure 3. Euraphia depressa collected from Khao Sam Muk beach, Chon Burl (BUU16.CH.ED01). A. Dorsal and ventral view of
external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. External
(upper panel) and internal (lower panel) view of shell plates, D-G. Eight microscopy on mouthparts, D. Eabrum, E. Close up on the
teeth of the labrum, F. Mandible with three large teeth, G. Close up on the pectinated lower margin of mandible. D-G. Scale bars in
pm. Abbreviations; c, carina; cl, carinal latus; 1, latus; r, rostrum.

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Zoosyst. Evol. 93 (1) 2017, 13-34

Table 3. Distribution of acorn barnacles on dilferent habitat types of intertidal zone (vertical zonation): low shores/ sublittoral zone
(LS), middle Shores/ littoral zone (MS), and high shores/ supralittoral zone (HS).

Scientific name

Habitat type

Settlement pattern on habitats

Family Chthamalidae

Chthamalus malayensis

Attached to rock platform, shell of Tetracllta spp. and other substrates

Euraphia depressa

Attached to sheltered sites of rock

Euraphia hembeli

Attached to rocky shore exposed to heavy \A/ave action

Family Tetraclitidae

Newmanella spinosus

Attached to rocks on a wave exposed shore

Tetracllta kuroshioensis

Attached to rock platform and sheltered sites of rock

Tetraclita singaporensis

Attached to rock platform and sheltered sites of rock

Tetracllta squamosa

Attached to rock platform and sheltered sites of rock

Family Balanidae

Amphibalanus amphitrite

Attached to rocks on a wave exposed shore, shell of oyster and Asian
Rreen mussel, offshore vessel and various substrates

Amphibalanus reticulatus

Attached to shell of Asian green mussel, oyster, ridged Venus clam and

other substrates

Megabalanus tintinnabulum

Attached to rocky shore exposed to heavy wave action

large setae at the edge; labmm with obvious teeth; caudal
appendage absent.

Distribution. In previous records, Euraphia depres-
sa was found to inhabit along Mediteranean localities,
including Spain (Punta Camero, Punta de la Chullera,
Malago, Salobrena and Calpe), France (Cap Bear, La
Couronne, and Cassis), Italy (Pegli and Lido), Greece
(Amnisso), the Black Sea and Suez canal (Utinomi 1959;
Southward 1964; Achituv and Safriel 1980; Crisp 1981).
In this study, the presence of E. depressa in Khao Sam
Muk station (Chon Buri) in Thailand was unexpected as
it was previously unrecorded along Thailand’s coastal
areas. They were found along rocky shores exposed to
heavy wave action inhabiting sheltered crevices of the
rocky platform and high shore. The abundance of E. de¬
pressa is much less than that of the cosmopolitan barnacle
Amphibalanus amphitrite in the same area of observation.

Remarks. Euraphia depressa (Poli, 1795) was the reas¬
signed name from Chthamalus depressus (Poli, 1795).
According to Southward (1964), Euraphia depressa can
be distinguished from Chthamalus stellatus, based on the
shell morphology showing smooth unribbed shell on the
external surface from younger specimens to more adult
stage and the operculum characters, showing joints be¬
tween tergum and scutum without sinous or slightly
sinous, and smaller tergum. In addition, a barnacle of
the genus Euraphia is distinguished from the genus Ch¬
thamalus based on the number of teeth on mandible and
as described in Southward (1964) our specimens have
mandible with three large teeth and three large setae on
the lower edge (Figure 3F & G) and lacking of caudal
appendages, leading to species identification of our spec¬
imens as Euraphia depressa. However, the number of se¬
tae at the pectinated margin of mandible in our specimens
is different. Only small 5 setae after larger three setae
were found in our specimens while up to 12 setae were
mentioned in Southward (1964).

Euraphia hembeli Conrad, 1837

Figure 4; Tables 2-3

Euraphia hembeli Conrad, 1837: 261.

Non-type material examined. Andaman Sea: 2 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai
beach, 16.V.2015, A. Pochai (BUU16.CH.EH01-02).

Description. Peduncle absent; base membranous; body
length larger than Chthamalus and range from 10-30
mm. Shell brownish grey with 6 plates (1 carina, 2 cari-
nal latus, 2 latus and 1 rostrum), carina bigger than ros¬
trum, carinal latus bigger than latus. External surface of
shell irregularly ribbed around basal margin, inner sur¬
face of parietes smooth and white with dark brown and
pale violet horizontal striations around aperture. Parietes
symmetrical, calcareous and solid, parietes separable, su¬
tures coarsely serrate or with interlocking toothed struc¬
ture. Orifice rhomboidal. Operculum plates symmetrical,
tergum smaller than scutum, tergum and scutum separa¬
ble. Scutum triangular, occludent margin of scutum with
strong teeth. Tergum strongly marked with 10-12 lateral
depressor crests, scutal margin strongly articulated.

Distribution. Barnacles in the genus Euraphia were re¬
corded in several regions including West Africa, the Med¬
iterranean, Hawaii and Southern Japan (Newman and
Ross 1976). Euraphia hembeli was previously recorded
in California around San Diego (Barrett and Freeman
2016). In this study, we report the presence of Euraphia
hembeli distributing along low and middle shore of the
intertidal zone, which was only found at Na Tai station,
the Andaman Sea (Tables 2 and 3). In addition, this is the
first report of its presence in Thailand.

Remarks. Based on the shell and opercular valve morpholo¬
gy (Newman and Ross 1976; Kim and Yamaguchi 1996), two
candidates: Euraphia hembeli Conrad, 1837 and Euraphia

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Figure 4. Euraphia hemheli collected from Na Tai beach, Phang-nga (BUU16.CH.CH01). A. Dorsal and ventral view of external
shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. External (upper
panel) and internal (lower panel) view of shell plates. Abbreviations; c, carina; cl, carinal latus; 1, latus; r, rostrum.

pilsbryi Hiro, 1936 (reassigned as Hexechamaesipho pilsbryi
(Hire, 1936)) show similar patterns of opercular plates to our
collected specimens. Based on Newman and Ross (1976),
description of Euraphia hembeli in Barrett and Freeman
(2016) and Chan et al. (2008), our specimens fit more into
E. hembeli and differ from other Euraphia in its gigantic ap¬
pearance (up to 30 mm) and the presence of strong marked
lateral depressor crests (10-12 in number, less in H. pilsbryi).

Superfamily Tetraclitoidea Gruvel, 1903

Family Tetraclitidae Gruvel, 1903

Subfamily Newmanellinae Ross & Perreault, 1999

Genus Ross, 1969

Type species. Newmanella radiata (Bruguiere, 1789)

1 genus, 1 species recorded: Newmanella spinosus
Chan & Cheang, 2016.

Newmanella spinosus Chan & Cheang, 2016

Figure 5; Tables 2-3

Newmanella spinosus Chan & Cheang, 2016: 212-220, figs 9-15.

Non-type material examined. Andaman Sea: 4 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai
beach, 16.V.2015, A. Pochai (BUU16.TC.NS01-04).

Description. Peduncle absent; base calcareous. Shell
greyish green, shell with 4 plates (1 carina, 2 latus, 1 ros¬
trum); parietes low conical, 3^ rows of irregular pari¬
etal tubes (parietes multiple tubiferous), radii board with
horizontal striation and summit oblique. External surface
with deep longitudinal/radiating lines from base to apex,
internal surface of parietes smooth and white with greyish
green striations close to operculum. Orifice pentagonal,
diamond-shaped. External surface of operculum brown¬
ish grey, internal surface of operculum white. Scutum tri¬
angular, external surface of scutum with horizontal stri¬
ations; tergum high and narrow, tergum with numerous
depressor crests.

Distribution. Newmanella spinosus was previously re¬
corded from low intertidal to subtidal levels on rock
shores along the coastlines of Taiwan and the Philippines
and they were also collected from the surfaces of buoys

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Zoosyst. Evol. 93 (1) 2017, 13-34

Figure 5. Newmanella spinosus collected from Na Tai beach, Phang-nga (BUU16.TC.NS01). A. Dorsal and ventral view of external
shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. External (upper
panel) and internal (lower panel) view of shell plates. Abbreviations; c, carina; 1, latus; r, rostrum.

used in fishing cages in the open sea (Chan and Cheang
2016). In this present study, N. spinosus specifically dis¬
tributes along low shores, and the intertidal zones of Na
Tai beach, Takua Thung District, Phang-nga (the Anda¬
man Sea).

Remarks. N. spinosus is morphologically similar to N.
radiata, based on shell and scutum. The shell of N. spi¬
nosus is green while those of N. radiata is white. In ad¬
dition, lateral scutal depressor muscle crest is shallow in
the scutum of N. radiata, but deep in N. spinosus. The
distribution of N. spinosus is around the North Pacific
Ocean, from Okinawan Japan to Taiwan and the Philip¬
pines (Chan and Cheang 2016). The presence of N. spi¬
nosus in Thailand is surprising in our study, and creates
the first record of this species distributing specifically in
Na Tai beach, Takua Thung district, Phang-nga province.

Subfamily Tetraclitinae Newman & Ross, 1976
Genus Tetraclita Schumacher, 1817

Type species. Tetraclita squamosa (Bruguiere, 1789)

1 genus, 3 species recorded: Tetraclita kuroshioensis Chan,
Tsang & Chu, 2007, Tetraclita singaporensis Chan, Tsang &
Chu, 2007 and Tetraclita squamosa (Bruguiere, 1789).

Tetraclita kuroshioensis Chan, Tsang & Chu, 2007

Figure 6; Suppl. material 1; Tables 2-3

Tetraclita squamosa viridis'. Hire, 1936: 635; 1937: 469; 1939: 271.
Tetraclita squamosa squamosal. Utinomi, 1968: 178.

Tetraclitapacifica Chan et at, 2007b; 88.

Non-type material examined. Andaman Sea: 2 speci¬
mens, Phang-nga province, Khura Buri district, Ao Khoei
beach, 30.VII.2015, A. Pochai (BUU16.TC.TK01-02).
3 specimens, Phang-nga province, Takua Thung dis¬
trict, Na Tai beach, 16.V.2015, A. Pochai (BUU16.
TC.TK03-05). 2 specimens, Phuket province, Mueang
Phuket district, Ao Yon beach, 15.VII.2015, A. Pochai
(BUU16.TC.TK06-07). 3 specimens, Phuket province,
Katu district, Kalim beach, 15.VII.2015, A. Pochai
(BUU16.TC.TK08-10).

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Figure 6. Tetraclita kuroshioensis collected from (BUU16.TC.TK01) from Na Tai beach, Phang-nga. A. Dorsal and ventral view of
external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C-F. Light
microscopy on mouthparts, C. Labrum, D. Close up on the teeth of the labrum, E. Mandible, F. Close up on the lower margin of
mandible. C-F. Scale bars in pm.

Gulf of Thailand: 3 specimens, Prachuap Khiri
Khan province, Bang Saphan district. Ban Krut beach,
06.IX.2015, A. Pochai (BUU16.TC.TK11-13). 3 spec¬
imens, Chon Buri province, Ko Si Chang district, Ko
Kham Yai beach, 05.VII.2015, S. Khachonpisitsak
(BUU16.TC.TK14-16).

Description. Peduncle absent; base membranous; shell
greyish black to purplish-grey with 4 plates (1 carina, 2
latus, 1 rostrum), parietes conical, plates inseparable, 7-8
rows of parietal tubes (parietes multiple tubiferous), exter¬
nal surface with mosaic scales pattern radiating randomly
from base to apex, internal surface of parietes smooth and
white with dark grey striations around aperture. Exter¬
nal surface of operculum mixed grey and yellowish-light

brown, internal surface of operculum greyish-dusky green.
Scutum bigger than tergum, scutum triangular, external
surface of scutum with horizontal striations, occludent mar¬
gin of scutum with obvious shallow and rough teeth, short
articular ridge-basal margin, angle between basal margin
and tergal margin is quite perpendicular. Tergum higher
than wide, basi-scutal angle 158°, tergum with broad spur,
spur angle 30°. Mandible with 4 big teeth, PHooth smaller;
maxillule not notched with 11 setae; labrum with 5 small
teeth on each side; cirri I possessing serrulate setae.

Distribution. Tetraclita kuroshioensis is reassigned the
name from Tetraclita squamosa which were collect¬
ed from Taiwan, and Okinawa and Honsu of Japan, and
Tetraclita pacifica. The distribution of this species occurs

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Zoosyst. Evol. 93 (1) 2017, 13-34

in broad area along north-west Pacific region (Chan et al.
2007a, b; Chan 2009). In this present study, the species
distribution occurs along littoral intertidal zones in both
the Andaman Sea (Ao Yon, Ao Khoei, Na Tai, and Kalim)
and the Gulf of Thailand (Ban Krut and Ko Kham Yai).

Remark. TetracUta kuroshioensis is quite similar to
Tetraclita singaporensis in following characteristics: ter-
gum without beak and with wide spur, scutum with short
articular ridge-basal margin. However, angle between
tergal margin and basal margin of T. kuroshioensis is
more perpendicular (90°) or shaper while that of T. sin¬
gaporensis is curved.

Tetraclita singaporensis Chan, Tsang & Chu, 2007

Figure 7; Suppl. material 2; Tables 2-3

Tetraclita singaporensis Chan, Tsang & Chu, 2007: 52-53, figs 1-3.

Non-type material examined. Andaman Sea: 2 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai
beach, 16.V.2015, A. Pochai (BUU16.TS.TSG01-02).

Description. Peduncle absent; base membranous; shell
purplish-dusky green with 4 plates (1 carina, 2 latus, 1
rostrum), parietes conical, plates inseparable, 5-6 rows of
parietal tubes (parietes multiple tubiferous), external sur¬
face with deep and irregular longitudinal striations from
apex to base and small radiating lines, internal surface of
parietes smooth and white with greyish-green horizontal
striations around aperture. External surface of opercu¬
lum yellowish brown mixed with dusky green, internal
surface of operculum dusky green-purplish and white
around spur of the tergum. Scutum bigger than tergum,
scutum triangular, short articular ridge-basal margin, ex¬
ternal surface of scutum with horizontal striations, occlu-
dent margin of scutum with rough teeth. Tergum higher
than wide, tergum with broad spur and not beaked, spur
angle 30-35°, basi-scutal margin 148-150°. Mandible
with 4 big teeth, 2"^ and 3'^‘^ teeth consisting double teeth,
tooth with small spines, lower margin pectinate with 8
small teeth and obvious double bigger teeth at the edge;
maxillule notched, two large setae above notch, 13-17
setae below notch; labrum with 4-5 large teeth on each
side; cirri I possessing bidenate serrulate setae.

Distribution. Tetracliata singaporensis has been reas¬
signed the name from previously known as Tetraclita
squamosa, which were collected from Singapore. Hence,
the distribution of this species is firstly marked at Singa¬
pore, Indo-West Pacific region (Chan et al. 2007a). In this
present work, the specimens were collected from Na Tai,
Andaman Sea and it distributes in the mid shore.

Remarks. Tetraclita singaporensis differs from Tetraclita
squamosa in that it has tergum without beak and broader
spur, and scutum with short articular ridge-basal margin.

Tetraclita squamosa (Bruguiere, 1789)

Figure 8; Suppl. material 3; Tables 2-3

Balanus squamosa YimgmQXQ, 1789: 170.

Lepas porosa GmeXm, 1791: 3212.

Tetraclita porosa var. viridis: Darwin, 1854: 329; Borradaile, 1900:
799; Gruvel, 1905: 228; Kruger, 1911: 61, pi. 4, fig. 41b; Hoek,
1913:254;

Tetraclita squamosa’. Stebbing, 1910: 570; Barnard, 1924: 90; Oliveira,
1941: 6.

Tetraclita squamosa squamosa'. Pilsbry, 1916: 251; Kolosvary, 1943:
96; Henry, 1957: 33; Stubbings, 1967: 294; Newman & Ross, 1976:
48; Ren & Liu, 1979: 339, pi. 1, figs. 1-11.

Tetraclita squamosa forma viridis’. Broch, 1922: 337; 1931: 116.
Tetraclita porosa perfecta'HWsson-CdiniQW, 1921: 364.

Tetraclita squamosa’. Yamaguchi, 1987: 344; Chan, 2001: 625, fig. 8;
Chan etal., 2007b: 82, fig. 4.

Non-type material examined. Gulf of Thailand: 2

specimens, Nakhon Si Thammarat province, Sichon dis¬
trict, Hin Ngam beach, 04.VII.2015, A. Pochai (BUU16.
TC.TSSOl-02).

Description. Peduncle absent; base membranous; shell
green mixed with brownish grey, shell with 4 plates (1
carina, 2 latus, 1 rostrum); parietes conical, plate fused,
inseparable, 8 rows of parietal tubes (parietes multi¬
ple tubiferous), external surface with longitudinal lines
from base to apex, internal surface of parietes smooth
and white with purplish grey striations close to aperture.
External surface of operculum brownish grey, internal
surface of operculum purplish grey. Scutum larger than
tergum, scutum triangular, long articular ridge-basal mar¬
gin, external surface of scutum with horizontal striations,
occludent margin of scutum with very shallow teeth; ter¬
gum higher than wide, basi-scutal margin 158-160°, ter¬
gum apex obviously beaked, tergum with spur long and
sharp, spur angle 25°. Mandible with 4 big teeth, EHooth
with three small spines, lower margin pectinate; maxil¬
lule notched, two large setae above notch, 11 big setae
below notch and some smaller setae at the edge; labrum
with 4 large teeth on each side; cirri I possessing bidenate
serrulate setae.

Distribution. Tetraclita squamosa is widespread in
tropical and subtropical waters from West Africa, the
Indo-Pacific, the Indian Ocean, Australia, Indonesia and
Singapore (Newman and Ross 1976; Ren and Eiu 1979;
Jones et al. 2000; Chan et al. 2007b). Its distributions in
Thailand were previously recorded in two places: the An¬
daman Islands and the Gulf of Siam (recently called the
Gulf of Thailand) (Jones 2000). In this present study, T.
squamosa has restricted areas of distribution and it was
found specifically at Hin Ngam beach, the Gulf of Thai¬
land coast. Regarding vertical zonation, T. squamosa
found in Thailand occurs on the mid shore.

Remark. As described in Chan et al. 2007a, b, T. squa¬
mosa (southern China) has unique tergum characteristics
including tergum with beak and long spur, and scutum
with long articular ridge-basal margin. Our specimens

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Figure 7. Tetraclita singaporensis collected from (BUU16.TC.TSG02) from Na Tai beach, Phang-nga. A. Dorsal and ventral view of
external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. Lateral
side showing external surface of shell, D. Close up on the external surface of shell, E-H. Light microscopy on mouthparts, E. Labrum,
E. Close up on the teeth of the labrum, G. Mandible, G. Close up on the pectinated lower margin of mandible. E-H. Scale bars in pm.

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Figure 8. Tetraclita squamosa collected from Hin Ngam beach, Nakhon Si Thammarat (BUU16.TC.TS01). A. Dorsal and ventral
view of external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel),
C. External (upper panel) and internal (lower panel) view of shell plates, D. Close up on external surface of shell, E-H. Eight
microscopy on mouthparts, E. Eabrum, E. Close up on the teeth of the labrum, G. Mandible, G. Close up on the pectinated lower
margin of mandible. E-H. Scale bars in pm. Abbreviations; c, carina; 1, latus; r, rostrum.

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from Hin Ngam beach have all of these characteristics;
hence, it is more fitted into T. squamosa (Southern China)
rather than T. squamosa (Singapore), which is reassigned
as T. singaporensis.

Superfamily Balanoidea Leach, 1817
Family Balanidae Leach, 1817
Subfamily Amphibalaninae Pitombo, 2004

Genus Amphibalanus Pitombo, 2004

Type species. Amphibalanus amphitrite (Darwin, 1854)

1 genus, 2 species recorded: Amphibalanus amphitrite
(Darwin, 1854) md Amphibalanus reticulatus (Utinomi,
1967).

Amphibalanus amphitrite (Darwin, 1854)

Figure 9; Tables 2-3

Balanus amphitrite var. communis Darwin, 1854: 240 (in part).

Balanus amphitrite V^oiinQY, 1897: 264; Pilsbry, 1907: 190; 1928: 312.
Balanus amphitrite communis'. Hiro, 1939: 263.

Balanus amphitrite hawaiiensis'. Hiro, 1939: 260.

Amphibalanus amphitrite'. Pitombo, 2004: 263.

Non-type material examined. Andaman Sea: 2 speci¬
mens, Phang-nga province, Khura Buri district, Ao Khoei
beach, 30.VII.2015, A. Pochai (BUU16.BN.AA01-02).
4 specimens, Phang-nga province, Takua Thung dis¬
trict, Na Tai beach, 16.V.2015, A. Pochai (BUU16.
BN.AA03-06). 4 specimens, Phuket province, Mueang
Phuket district, Ao Yon beach, 15.VII.2015, A. Pochai
(BUU16.BN.AA07-10). 3 specimens, Phuket province,
Mueang Phuket district, Panwa beach, 16.VII.2015, S.
Khachonpisitsak (BUU16.BN.AA11-13). 4 specimens,
Phuket province, Katu district, Kalim beach, 15. VII.2015,
A. Pochai (BUU16.BN.AA14-17).

Gulf of Thailand: 2 specimens, Nakhon Si Thammarat
province, Sichon district, Hin Ngam beach, 09.VIII.2015,
A. Pochai (BUU16.BN.AA18-19). 4 specimens, Prach-
uap Khiri Khan province. Bang Saphan district. Ban Krut
beach, 06.IX.2015, A. Pochai (BUU16.BN.AA20-23).
2 specimens. Chon Buri province, Ko Si Chang district,
Ko Kham Yai beach, 05.VII.2015, S. Khachonpisitsak
(BUU16.BN.AA24-25). 4 specimens. Chon Buri prov¬
ince, Si Racha district. Si Racha beach, 04.VII.2015, A.
Pochai (BUU16.BN.AA26-29). 3 specimens. Chon Buri
province, Mueang Chon Buri district, Khao Sam Muk
beach, 05.VII.2015, A. Pochai (BUU16.BN.AA30-32).

Description. Peduncle absent; base calcareous. Shell
white-pale pink with 6 plates (1 carina, 2 carinal latus,
2 latus, 1 rostrum); single rows of parietal tubes (pari-
etes single tubiferous) with transverse septa; radii solid.
External surface with purple longitudinal striations from
apex to base (3^ lines per plate) without horizontal stri-
ation, transverse teeth on suture edges with denticles on
lower regions, internal surface of parietes grey with black
horizontal striations close to operculum. External surface

of operculum brownish grey, internal surface of oper¬
culum grey-white. Scutum bigger than tergum, scutum
triangular, external surface of scutum with curved stria¬
tions; tergum spur board with growth lines.

Distribution. Amphibalanus amphitrite is a common foul¬
ing barnacle and cosmopolitan species distributed along
intertidal zones of coastlines in both the Gulf of Thailand
and the Andaman Sea. It was found in all stations exam¬
ined. The settlement patterns are various (e.g. rocks, shells
of oyster and green mussels, concrete walls of bridges
and harbors, offshore vessels, dock pilling, and mooring
robes). In previous records, this species distributes world¬
wide in both tropical and temperate regions including the
Indo-West Pacific, and Western Australia (Jones 2004;
Chen et al. 2014) and it has been suggested that this wide
range of distribution was due to human-mediated activities
during global trade expansion (Chen et al. 2014).

Remark. The morphology of Amphibalanus amphitrite
is variable from diverse habitats worldwide. Shells ex¬
posed and eroded by heavy wave action showed no pur¬
ple stripes on the external surface. The molecular analysis
has confirmed its genetic differentiation which might be
due to local adaptation and geographical isolation (Chen
et al. 2014). Due to hypothesis on human-mediated ac¬
tivities as the main cause of A. amphitrite A distribution
across the globe, this species is considered as non-native
or introduced species in these examined regions: Hawaii,
California, North Carolina, and the Atlantic coast (Carl¬
ton et al. 2011), whereas it is considered as native in trop¬
ical waters (e.g. Hong Kong, Thailand, Malaysia) sup¬
ported by molecular study (Chen et al. 2014). Despite the
diverse morphology of A. amphitrite, another species in
the same genus Amphibalanus reticulatus exhibits clear
patterns of shell carrying both vertical and longitudinal
striations on the external surface. The separation of set¬
tlement type is distinct between these two species; one is
found mostly on rocky shores exposed to waves and the
other one is found on some mollusk shells.

Amphibalanus reticulatus (Utinomi, 1967)

Figure 10; Tables 2-3

Balanus amphitrite var. communis Darwin, 1854: 240, pi. 5, figs. 2e, h,
1 [type locality: Tachitgatani, Tanabe Bay, Japan],

Balanus amphitrite communis'. Hiro, 1938: 301, figs, la, b; Utinomi,
1956: 52, pi. 26, fig. 11.; 1960: 44, figs. Ic, d, 2c, d.

Balanus reticulatus'. Utinomi, 1967: 216, figs. 9a, b, 10a, b, lla-e, pi. 6,
figs. 7-8; Henry & McLaughlin, 1975: 88, text figs. 11, 18, pi. 7, fig.
d, pi. 8, pi. 9, figs, a, d, e.

Non-type material examined. Andaman Sea: 2 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai
beach, 16.V.2015, A. Pochai (BUU16.BN.AR01-02).

Gnlf of Thailand: 3 specimens. Chon Buri province.
Si Racha district. Si Racha beach, 04.VII.2015, A. Po¬
chai (BUU16.BN.AR03-05). 3 specimens. Chon Buri

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Figure 9. Amphibalanus amphitrite collected from Khao Sam Muk beach, Chon Burl (BUU16.BA.AA30). A. Dorsal and ventral
view of external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel),
C. External (upper panel) and internal (lower panel) view of shell plates. Abbreviations: c, carina; cl, carinal latus; 1, latus; r, rostrum.

province, Mueang Chon Buri district, Khao Sam Muk
beach, 05.Vn.2015, A. Pochai (BUU16.BN.AR06-08).
3 specimens. Chon Buri province, Ko Si Chang district,
Ko Kham Yai beach, 05.VIL2015, S. Khachonpisitsak
(BUU16.BN.AR09-11).

Description. Peduncle absent; base calcareous. Shell
white-pale pink and orange with 6 plates (1 carina, 2
carinal latus, 2 latus, 1 rostrum); single rows of parietal
tubes (parietes single tubiferous) with transverse septa;
radii solid. External surface with longitudinal and hor¬
izontal striations, transverse teeth on suture edges with
denticles on lower regions, internal surface of parietes
white. External surface of operculum white-pale pink and
orange with striations in both tergum and scutum, internal
surface of operculum white. Scutum bigger than tergum,
scutum triangular; tergum spur sharp with growth lines.

Distribution. Amphibalanus reticulatus is widely distrib¬
uted from Japan, the Indo-West Pacific to Australia, of
which the latter is considered as an introduced species
carried by ship transport (Jones 2004). In this study, A.
reticulatus occurred in the intertidal zone along the Anda¬
man Sea and the Gulf of Thailand. These specimens were

found at Si Racha, Khao Sam Muk, Ko Kham Yai (Chon
Buri) and Na Tai (Phang-nga).

Remark. Amphibalanus reticulatus exhibits clear vertical
and horizontal striations while Amphibalanus amphitrite
shows only vertical purple striation in all shell plates. In ad¬
dition, the shapes of shell of A. reticulatus is more columnar
than that of A. amphitrite, which might be due to elongation
of parietes in response to crowding when growing as colo¬
nies. On all examined stations, distinct distribution and set¬
tlement between A. amphitrite and A. reticulatus can be no¬
ticed, in that A. amphitrite were found in almost all kinds of
substrates but^J. reticulatus preferred its attachment on shells
which obviously did not live along the rocky shores and it
might probably inhabit the deeper areas of the sea and were
occasionally carried away into the shores by wave action.

Subfamily Megabalaninae Newman, 1979
Genus Megabalanus Hoek, 1913

Type species. Megabalanus tintinnabulum (Einnaeus, 1758)
1 genus, 1 species recorded: Megabalanus tintinnabu¬
lum Einnaeus, 1758.

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Figure 10. Amphibalanus reticulatus collected from Si Racha beach, Chon Buri (BUU 1 6.BN.ARO 1, A; BUU 1 6.BN.AR 03, B & C).
A. Dorsal and ventral view of external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and
scutum (lower panel), C. External (upper panel) and internal (lower panel) view of shell plates. Abbreviations: c, carina; cl, carinal
latus; 1, latus; r, rostrum.

Megabalanus tintinnabulum (Linnaeus, 1758)

Figure 11; Tables 2-3

Lepas tintinnabulum Linnaeus, 1758: 668.

Balanus tintinnabiihmr. Bruguiere, 1789: 165 (in part); Holthuis &
Heerebout, 1972: 24, pl.l.

Lepas tintinnabulum Wood, 1815: 38, pi. 6, figs. 1, 2.

Balanus tintinnabulum tintinnabulum: Pilsbry, 1916: 55, pi. 10, fig.l-
le; Hiro, 1939: 258, figs. 7a-b; Daniel, 1956: 17, pi. 4, figs. 1-6;
Davadie, 1963: 26, pi.2, fig. 4, pi. 6, figs, la, 2b; Zevina & Tarasov,
1963: 87, fig. 8; Stubbings, 1964: 335.

Balanus tintinnabulum var. tintinnabulum: Oliveira, 1941: 11, text-fig.

1, pi. 2, figs. 1, 2, pi. 4, fig. 1, pi. 5 fig. 3, pi. 8, fig. 6.

Megabalanus tintinnabulum: Newman & Ross, 1976: 68; Lacombe &
Rangel, 1978: 3, fig. 4.

Non-type material examined. Andaman Sea: 3 speci¬
mens, Phang-nga province, Takua Thung district, Na Tai
beach, 16.V.2015, A. Pochai (BUU16.BN.MT01-03).

Description. Peduncle absent; base calcareous. Shell
cylindric or conic with 6 plates (1 carina, 2 carinal la¬
tus, 2 latus, 1 rostrum); parietes reddish to brownish red
usually with longitudinal striations on external surface,
parietes not prominently ribbed and rather smooth, irreg¬

ular shape of parietal tubes (parietes tubiferous), sutural
edges of radii with regular denticles, radii wide with hor¬
izontally striated, radii tubiferous; internal surface of pa¬
rietes pale-purple with horizontal greyish violet striations
around aperture. Orifice subcircular to rhombus. External
surface of operculum white-pale pink and orange with
prominent growth ridges in both tergums and scutums,
internal surface of operculum white. Scutum bigger
than tergum, scutum triangular, adductor ridge of scu¬
tum prominent; tergum with spur, spur furrow of tergum
closed, scutal margin denticulate.

Distribution. Megabalanus tintinnabulum is widely dis¬
tributed across almost all continents and is a well-known
cosmopolitan fouling species. It was previously found
in French Guiana, the United States, Australia, Mexico,
Ecuador, Kuwait, Saudi Arabia, Sweden, France, Neth¬
erlands, Singapore, Indonesia and India (Henry and Mc-
laughlin 1986; Thiyagarajan et al. 1997; Jones et al. 2000;
Jones 2004). Similar to Amphibalanus, it is considered
as an introduced species in several regions and its distri¬
bution has been facilitated via shipping (Jones 2004). In
Thailand, M. tintinnabulum specifically occurs in the low

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Zoosyst. Evol. 93 (1) 2017, 13-34

Figure 11. Megabalanus tintinnahulum collected from Na Tai beach, Phang-nga (BIJU16.BN.MT01). A. Dorsal and ventral view of
external shell, B. External (left panel) and internal (right panel) view of tergum (upper panel) and scutum (lower panel), C. External
(upper panel) and internal (lower panel) view of shell plates. Abbreviations; c, carina; cl, carinal latus; 1, latus; r, rostrum.

shores at Na Tai beach, Phang-nga province (the Anda¬
man Sea). However, it does not appear to be a common
fouling species as seen in some regions. M. tintinnabu-
lum might have been introduced to Phang-nga beaches
via ship transport, and the competition for habitat niche is
compromised, compared to previously occupying cosmo¬
politan yl. amphitrite.

Remarks. Megabalanus tintinnabulum has relatively
larger shell plates than those of Amphibalanus . All three

examined species (M tintinnabulum, A. amphitrite and
A. reticulatus) in family Balanidae have opercular valves
with prominent growth ridges horizontally, and tergum
with a clear spur. The coloration among these three spe¬
cies is easily distinguishable, in that purplish longitudinal
striations presenting A. amphitrite, vertical and longitu¬
dinal red-orange striations with orange-pale pink back¬
ground presenting A. reticulatus and brownish red sur¬
face with some irregular and unclear longitudinal stripes
presenting M. tintinnabulum.

Identification key

la Shell conical to low conical with 4 plates with distinct parletes or shell with 4 plates with indistinct parietes or fused

parietes, parietes multi-tubiferous.2

lb Shell with 6 plates with distinct parietes.5

2a Shell low conical, parietes discrete, summit of radii oblique, orifice pentagonal and wide, external surface of shell with

deep longitudinal striations. Newmanella spinosus Chan & Cheang, 2016

2b Shell conical, parietes not discrete, summit of radii horizontal, orifice circular or oval and small.3

3a Shell green, external surface of shell with longitudinal striation, shell plates separable, tergum with obvious beak and

tergum with sharp and narrow spur. Tetraclita squamosa (Bruguiere, 1789)

3b Shell greyish black, external surface of shell with mosaic scale-like, plates inseparable, tergum without beak and with
broad spur.4

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Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

4a Angle between basal margin and tergal margin of scutum is almost perpendicular.

. Tetraclita kuroshioensis Chan, Tsang & Chu, 2007

4b Angle between basal margin and tergal margin of scutum is curved....Tetraclita singaporensis Chan, Tsang & Chu, 2007

5a Parietes solid.6

5b Parietes tubiferous.8

6a Body length 10-30 mm, gigantic appearance. Euraphia hembeli Conrad, 1837

6b Body length 3-10 mm, tergum with 3-4 lateral depressor crests.7

la Mandible with four teeth, cirri I with conical spines, cirri II with multi-cuspidate setae and basal guard, articulation of

opercular valves deep (shape of articulation similar to jigsaw-shaped), . Chthamalus malayensis Pilsbry, 1916

7b Mandible with three teeth and 11 smaller setae at the lower margin, articulation of opercular valves shallow (shape of

articulation from outside view similar to bird beak. Euraphia depressa (Poli, 1795)

8a Parietal tubes single row and irregular shaped, shell with irregular and deep longitudinal striations, shell purplish white...

. Megabalanus tintinnabulum (Linnaeus, 1758)

8b Parietal tubes single row and uniform.9

9a External surface with purple longitudinal striations from apex to base against white surface.

. Amphibalanus amphitrite (Darwin, 1854)

9b External surface with shall longitudinal and horizontal striations, shell white-pale pink and orange.

. Amphibalanus reticulatus (Utinomi, 1967)

Discussion

In the present study, we examine geographical distri¬
bution of sessile acorn barnacles along Thai Peninsular
coastal areas including the Gulf of Thailand and the An¬
daman Sea. So far, there has been a lack of information
regarding the diversity of sessilian Thoracican barnacles
in Thailand. Hence, we attempt to generate a checklist to
understand the species diversification and how they dis¬
tribute on intertidal rocky shores and sandy shores along
the coast of Thailand. At least ten different forms of acorn
barnacles were diagnosed so far that are classified into
6 genera and 3 families (Chthamalidae, Tetraclitidae and
Balanidae), which can be distinguished based on their
external shell morphology, including pattern of pariet¬
es, opercular plates, and arthropodal characters as de¬
scribed in previous literatures (Ross and Perreault 1999;
Chan 2001; Chan et al. 2007a, b; Chan et al. 2009; Loza-
no-Cortes and Londono-Cruz 2013; Chen et al. 2014; Ha-
yashi and Chan 2015; Chan and Cheang 2016).

Our study also shows that the numbers of species
found in the Andaman Sea (8 species) are more than
those found in the Gulf of Thailand (6 species). At Na
Tai station located in the Andaman Sea, up to 8 spe¬
cies (6 genera and 3 families) were recorded. Four of
these 8 species were found only at this station including
Newmanella spinosus, Euraphia hembeli, Megabalanus
tintinnabulum and Tetraclita singaporensis. In other
examined stations, only 2-3 species could be found,
and most of them were of the genus Amphibalanus,
Tetraclita, and Chthamalus. The differences in species
abundance between two coastlines might probably due
to the past history of the barnacle colonization. It has
been shown in Voris (2000) that sea level was fiuctuated
during the Pleistocene, caused by glaciation. The spread
of acorn barnacle seen in present day is possibly due to
successful colonization when there were the connections
between the eastern part of Indian Ocean and the Gulf of

Thailand. The nature of local habitats such as the incom¬
ing oceanic current and freshwater discharge might also
be another factor promoting or limiting the boundary of
barnacle distribution. In addition, the spread of the bar¬
nacles found in the Gulf of Thailand was probably fa¬
cilitated by the influence of the South China Sea Warm
Current (SCSWC) as shown in the case of Chthamalus
malayensis (Tsang et al. 2012). However, at this present
work, we cannot clearly conclude that all of these spe¬
cies found in this work successfully distributed before
the glaciation or influenced by nature of specific local
habitats as further extensive works need to be done to
include more stations along both coastlines with proper
oceanographic data.

In addition, we found five new records identified as
Newmanella spinosus, Euraphia depressa and Euraphia
hembeli, Tetraclita singaporensis, and Tetraclita kurosh¬
ioensis on which the presence of these species in Thai¬
land has not been mentioned in any literatures. N. spino¬
sus, E. hembeli and T. singaporensis can only be seen at
Na Tai station, Phang-nga province while E. depressa is
specific to Khao Sam Muk, Chon Buri province. Howev¬
er, we cannot rule out the possibility of their presences in
other places and more intensive field surveys covering all
provinces along Thailand's coasts are required.

Recently, there are 26 species in the genus Chthama¬
lus (Chan et al. 2009). In this study, one of them is clear¬
ly diagnosed as Chthalamus malayensis based on distinct
shell, operculum morphology and arthropodal characters.
However, we also found another Chthamalid which has
shallow articulation of tergum and scutum; suggesting
the possibility of a different species. Surprisingly, this
Chthamalids is similar to Chthamalus depressus (reas¬
signed as Euraphia depressa), described in Southward
(1964). The presence in Thailand was not mentioned
as they were thought to be found around the Mediter¬
ranean. In addition, the Chthamalids we found exhibit
great variation and this has previously been reported that

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Zoosyst. Evol. 93 (1) 2017, 13-34

Chthamalids have high intraspecific variation in exter¬
nal morphology (Helmuth et al. 2006; Hawkins et al.
2008) and thus using shell morphology is not ideal for
taxonomic identification; thus several studies have used
other measures for species diagnosis, including opercu¬
lar plate geometry (Tsang et al. 2012), light microsco¬
py and SEM of arthropodal characters (e.g. the number
of conical spines and the number of setules of the basal
guard setae on cirri and pattern of oral cones) (Miller and
Blower 1989; Southward and Newman 2003; Yan and
Chan 2004; Tsang et al. 2012) and molecular approaches
(Tsang et al. 2012). In any future studies, we will use
all of these measures, particularly the examination of
mitochondrial COI, 12s rDNA, 16s rDNA sequences or
performing DNA barcoding in order to get accurate iden¬
tifications of chthamalid barnacles.

According to a field survey on water quality and met¬
al contamination of both coastal regions of Thailand, the
Andaman Sea is still in a good condition compared to the
Gulf of Thailand. On the other hand, habitat degradation
along the Gulf of Thailand is much more severe and the
number of species of these sessile arthropods has been
declining dramatically over the last 20 years due to high
amount of water pollution. For example, along Chon Bu¬
rl’s coast around 20 years ago, at least five species were
commonly seen along rocky shores of the now develop¬
ing centrum area. Recently, however, only Amphihala-
nus amphitrite have been able to tolerate severe human
activities and even in some sites there are no more bar¬
nacles on rocky shores. This might be because the local
communities have been releasing non-treated waste water
directly into the sea (personal communication and unpub¬
lished report (1996): Department of Biology, Faculty of
Science, Burapha University). Hence, the richness of bar¬
nacle species can also be used to indirectly monitor the
conditions of sea water.

Taken together, we demonstrate a clearer view of
diversity for acorn barnacles from various localities in
Thailand. This study shows at least 10 species of barna¬
cles, in total, exist along Thai coast regions. Future works
with more sampling sites and further in-depth investiga¬
tions using SEM and molecular approaches with the help
of phylogenetic analysis will provide a much better view
especially of the history of barnacles and intraspecific
variation between sessile crustaceans and that may reveal
new barnacle species inhabiting Thailand.

Acknowledgement

This work was supported by Grant for Graduate Student
2015, Faculty of Science, Burapha University, Thailand.
We would like to thank Assistant Professor Dr. Chuta
Boonphakdee, Assistant Professor Pongrat Dumrongro-
jwattana, Mr. Rungwit Chaijirawong, Mr. Santi Suanla
and Ms. Salisa Nithikulthananan for imaging assistance
and Mr. Robert Fuke for reading through a draft of the
manuscript.

References

Achituv Y, Safriel UN (1980) Euraphia depressa (Poll) (Crustacea Cirri-
pedia), A recent Mediterranean colonizer of the Suez canal. Bulletin
of Marine Science 30(3): 724-726.

Barnard KH (1924) Contributions to the crustacean fauna of South Af¬
rica - 7. Cirripedia. Annals of the South Africa Museum 20: 1-103.

Barrett PH, Freeman RB (2016) The Works of Charles Darwin: Vol 12:
A Monograph on the sub-class Cirripedia (1854), Vol II. Routledge.

Borradaile LA (1900) On some crustacean from the South Pacific. Part
5. Arthrostracans and barnacles. Proceedings of the Zoological So¬
ciety of London 1900: 795-799.

Brickner I, Hoeg JT (2010) Antennular specialization in cyprids of
coral-associated barnacles. Journal of Experimental Marine Bi¬
ology and Ecology 392: 115-124. https://doi.org/10.1016/j.jem-
be.2010.04.015

Brickner I, Eoya Y, Achituv Y (2010) Diverse life strategies in two
coral-inhabiting barnacles (Pyrgomatidae) occupying the same host
(Cyphastrea chalcidicum), in the northern Gulf of Eilat. Journal of
Experimental Marine Biology and Ecology 392: 220-227. https://
doi.org/10.1016/j.jembe.2010.04.022

Broch H (1922) Papers from Dr. Th. Mortensen’s Pacific Expedi¬
tion 1914-1916, X. Studies on Pacific cirripedes. Videnskabelige
Meddelelser fra Dansk Naturhistorisk Forening i Kobenhavn 73:
251-358.

Broch H (1931) Papers from Dr. Th. Mortensen’s Pacific Expedition
1914-1916, EVE Indomalayan Cirripedi. Videnskabelige Med¬
delelser fra Dansk Naturhistorisk Forening i Kobenhavn 91: 1-146.

Bruguiere M (1789) Encyclopedie methodique. Historie naturelle des
Vers. 1, 158-173.

Carlton JT, Newman WA, Pitombo FB (2011) Barnacle invasions:
Introduced, cryptogenic, and range expanding Cirripedia of North
and South America. Galil BS, Clark PF, Carlton JT (Eds) In the
Wrong Place - Alien Marine Crustaceans: Distribution, Biology
and Impacts - Series in Invasion Ecology XVI. Springer, Dordrecht,
159-214. https://doi.org/l0.1007/978-94-007-0591 -3-5

Chan BKK (2001) Studies on Tetraclita squamosa and Tetraclita ja-
ponica (Cirripedia: Thoracica) 1: adult morphology. Journal of Crus¬
tacean Biology 21: 616-630. http://doi.org/10.1651/C-2350

Chan BKK, Tsang EM, Chu KH (2007a) Cryptic diversity of the Tetra¬
clita squamosa complex (Crustacea: Cirripedia) in Asia: descrip¬
tion of a new species from Singapore. Zoological Studies 46(1):
46-56.

Chan BKK, Tsang EM, Chu KH (2007b) Morphological and genetic
differentiation of the acorn barnacle Tetraclita squamosa (Crusta¬
cea, Cirripedia) in East Asia and description of a new species of
Tetraclita. Zoological Scripta 36: 79-91. https://doi.org/10.llll/
j.l463-6409.2007.00260.x

Chan BKK, Hsu CH, Southward AJ (2008) Morphological variation
and biogeography of an insular intertidal barnacle Hexechamaesi-
pho pilsbryi (Crustacea: Cirripedia) in the Western Pacific. Bulletin
of Marine Science 83(2): 315-328.

Chan BKK, Prabowo RE, Eee K-S, Eee K-H (2009) Crustacean Fauna
of Taiwan: Barnacles, Volume 1-Cirripedia: Thoracica excluding the
Pyrogomatidae and Acastinae. National Taiwan Ocean University,
Keelung.

Chan BKK, Cheang CC (2016) First discovery of a new species of
Newmanella Ross, 1969 (Balanomorpha: Tetraclitidae) in the western

zse.pensoft.net

Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

Pacific, with a note on the new status of Neonrosella Jones, 2010.
Zootaxa 4098(2): 201-226. https://doi. 0 rg/lO.l 1646/zootaxa.4098.2.1.

Chen HN, Tsang LM, Chong VC, Chan BKK (2014) Worldwide ge¬
netic differentiation in the common fouling barnacle, Amphibalanus
amphitrite. Biofouling 30: 1067-1078. https://doi.org/10.1080/0892
7014.2014.967232

Chen YY, Lin HC, Chan BKK (2012) Description of a new species
of coral-inhabiting barnacle, Darwiniella angularis sp. n. (Cirripe¬
dia, Pyrgomatidae) from Taiwan. ZooKeys 214: 43-74. https://doi.
org/10.3897/zookeys.214.3291

Conrad TA (1837) Descriptions of new marine shells from upper Cali¬
fornia, collected by Thomas Nuttal, Esq. Journal of the Academy of
Natural Sciences of Philadelphia (Series 1) 7: 227-268.

Crisp D, Southward AJ, Southward E (1981) On the distribution of the
intertidal barnacles Chthamalus stellatus, Chthamalus montagui and
Euraphia depressa. Journal of the Marine Biological Association
UK 61: 359-380. https://doi.Org/10.1017/S0025315400047007

Daniel A (1956) The cirripedes of the Madras coast. Bulletin of the
Madras Government Museum 6(2): 1-40.

Darwin C (1854) A monograph on the sub-class Cirripedia with figures
of all species. The Balanidae, Verrucidae, 684 pp.

Davadie C (1963) Etude des Balanes fossiles d’Europe et d’Afrique. Sys-
tematique et stmcture des balanes fossiles d’Europe et d’Arique, 146 pp.

de Oliveira EPH (1941) Contribuicao ao conhecimento dos crustaceos
do Rio de Janeiro. Sub-ordern “Balanomorphe” (Cirripedia: Thora-
cica). Memorias do Instituto Oswaldo Cruz 36(1): 1-31.

Dong Y, Chen Y, Cai R (1980) Preliminary study on the Chinese cir-
ripedian fauna (Crustacea). Acta Oceanologica Sinica 2: 124-131.

Frith DW, Tantanasiriwong R, Bhatia O (1976) Zonation and abun¬
dance of macrofauna on a mangrove shore, Phuket Island. Phuket
Marine Biological Center Research Bulletin 10: 37.

Gmelin JF(1791) Systematic Naturae. 3212.

Gruvel A (1905) Monographie des Cirrhipedes ou thecostraces. 472 pp.

Hayashi R (2013) A checklist of turtle and whale barnacles (Cirripe¬
dia: Thoracica: Coronuloidea). Journal of the Marine Biological
Association of the United Kingdom 93(1): 143-182. https://doi.
org/10.1017/S0025315412000847

Hayashi R, Chan BKK (2015) New records of the tetraclitid barnacle
Tesseropora alba (Cirripedia: Thoracica: Tetraclitoidea) in the Pacif¬
ic waters of Taiwan and Okinawa. Species Diversity 20(2): 183-189.
https://doi.Org/10.12782/sd.20.2.183

Hawkins SJ, Moore PJ, Burrows MT, Poloczanska E, Mieszkowska N,
Herbert RJH, Jenkins SR, Thompson RC, Genner MJ, Southward
AJ (2008) Complex interactions in a rapidly changing world: Re¬
sponses of rocky shore communities to recent climate change. Cli¬
mate Research 37: 123-133. https://doi.org/10.3354/cr00768

Helmuth BST, Mieszkowska N, Moore P, Hawkins SJ (2006) Eiving on
the edges of two changing world: Forecasting the responses of rocky
intertidal ecosystems to climate change. Annual Review of Ecology,
Evolution and Systematics 37: 373-404. https://doi.org/10.1146/an-
nurev.ecolsys.37.091305.110149

Henry DP (1957) Some littoral barnacles from the Tuamotu, Marshall, and
Caroline Islands. Proceedings of the United States national Museum
107(3381): 25-38. https://d 0 i. 0 rg/l0.5479/si.00963801.107-3381.25

Henry DP, McEaughlin PA (1975) The barnacles of the Balanus amphi¬
trite complex (Cirripedia, Thoracica). Zoologische Verhandelingen
141: 1-254.

Henry DP, McEaughlin PA (1986) The recent species of Megabala-
nus (Cirripedia, Balanomorpha) with special emphasis on Balanus
tintinnabulum (Einnaeus) sensu lato. Zoologische Verhandelingen
235:le69.

Hiro F (1936) Report on the cirripedia collected in the Malayan wa¬
ters by the ship ‘Zuiho-maru’. Japanese Journal of Zoology 6(4):
621-636.

Hiro F (1937) Studies on cirripedian fauna of Japan II. Cirripeds found in
the vicinity of the Seto marine Biological Eaboratory. Memoirs of the
College of Science, Kyoto Imperial University, Series B 12: 385-478.

Hiro F (1938) On the Japanese forms of Balanus amphitrite Darwin.
Zoological Magazine (Tokyo) 50: 299-313.

Hiro F (1939) Studies on the cirripedian fauna of Japan. IV. Cirripeds of
Formosa (Taiwan), with some geographical and ecological remarks.
Memoirs of the College of Science, Kyoto Imperial University,
Series B 15: 245-284.

Hoek PPC (1913) Cirripedia of the Siboga-Expedition. Siboga-Expeditie
Reports 31: 129-275.

Holm ER (2012) Barnacles and biofouling. Integrative and Compara¬
tive Biology 52(3): 348-55. https://doi.org/10.1093/icb/ics042

Holthuis EB, Heerebout GR (1972) Vondsten van de zeepok Balanus
tintinnabulum (Einnaeus, 1758) in Nederland. Bijdragen tot de Fau-
nistiek van Nederland. II. Zoologische Bijdragen, Eeiden 13: 24-31.

Hoeg JT, Moller OS (2006) When similar beginnings lead to different
ends: Constraints and diversity in cirripede larval development. In¬
vertebrate Reproduction & Development 49: 125-142. https://doi.or
g/10.1080/07924259.2006.9652204

Jones DS, Hewitt MA, Sampey A (2000) A checklist of the Cirripedia
of the South China Sea. The Raffles Bulletin of Zoology 8: 233-307.

Jones DS (2004) Barnacles (Cirripedia: Thoracica) of the Dampier Ar¬
chipelago, Western Australia. Records of the Western Australian
Museum Supplement 66: 121-154.

Karande AA, Palekar VC (1963) On a shore barnacle Chthamalus ma-
layensis Pilsbry from Bombay, (India). Annals and Magazine of
Natural History, series 13 6: 231-234.

Kim MH, Yamaguchi T (1996) Earval development and phylogenetic
relationship between Chthamalus challengeri and Euraphia pilsbryi
(Subclass Cirripedia, Suborder Balanomorpha, Family Chthamali-
dae). Marine Fouling 12: 1-23.

Kolosvary GV (1943) Cirripedia Thoracica in der Sammlung des Un-
garischen National-Museums. Annales Historico-Naturales Musei
Nationalis. Hungarici 36: 67-120.

Kruger DP (1911) Beitrage zur Cirripedienfauna Ostasien. Beitrage zur
Naturgeschichte Ostasiens herausgegeben von. F. Doflein. Konglige
Bayerische Akademie der Wissenschaften, Munich Mathema-
tische-physikalische Klasse. Abhandlungen Supplement Band 2: 1-72.

Eacombe D, Rangel EF (1978) Cirripedios de Arraial do Cabo, Cabo
Frio Publicapoes do Intituto de Pesquisas da Marina 129: 1-12.

Eimpsaichol P, Khokiattiwong S, Bussarawit N (1991) Water quality
of the Andaman Sea coast of Thailand. Technical paper. Phuket,
Thailand: Phuket Marine Biological Center.

Einnaeus C (1758) Systema Naturae. Homiae. Editio Decima, Reformata
Volume 1. 824 pp.

Eozano-Cortes DF, Eondono-Cruz E (2013) Checklist of barnacles
(Crustacea; Cirripedia: Thoracica) from the Colombian Pacific. Ma¬
rine Biodiversity 43(4): 463-471. https://doi.org/10.1007/sl2526-
013-0175-2

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 13-34

Martin JW, Olesen J, H 0 eg JT (2014) Atlas of Crustacean Larvae. Johns
Hopkins University Press, Baltimore.

Maruzzo D, Aldred N, Clare AS, Hoeg JT (2012) Metamorphosis in
the Cirripede Crustacean Balanus amphitrite. PLoS ONE 7: e37408.
https://doi.org/10.1371/journal.pone.0037408

Miller KM, Blower SM (1989) Comparison of larval and adult stag¬
es of Chthamalus dalli and Chthamalus fissus (Cirripedia: Tho-
racica). Journal of Crustacean Biology 9: 242-256. https://doi.
org/10.2307/1548504

Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing
the global threat of invasive species to marine biodiversity. Fron¬
tiers in Ecology and the Environment 6(9): 485-492. https://doi.
org/10.1890/070064

Newman WA, Ross A (1976) Revision of the balanomorph barnacles,
including a catalog of the species. Memoirs of the San Diego Society
of Natural History 9: 1-108.

Nilsson-Cantell CA (1921) Cirripeden-Studien. Zur Kenntnis der Bi-
ologie, Antomie und Systematic dieser Gruppe. Zoologiska Bidrag
Fran Uppsala 7: 75-390.

Pilsbry HA (1907) Hawaiian cirripedia. Bulletin of the Bureau of Fish¬
eries, Washington 26: 181-190.

Pilsbry HA (1916) The sessile barnacles (Cirripedia) contained in the
collections of the US National Museum: including a monograph of
the American species. Bulletin of the United States National Muse¬
um 93: 1-366. https://doi.Org/10.5479/si.03629236.93.l

Pilsbry HA (1928) Eittoral barnacles of the Hawaiian islands and Japan.
Proceedings of the Academy of Natural Science of Philadelphia 79:
305-317.

Pitombo FB (2004) Phylogenetic analysis of the Balanidae (Cirripedia,
Balanomorpha). Zoological Scripta 33(3): 261-276. https://doi.
org/10.1111/J.0300-3256.2004.00145.X

Poll GS (1791) Testacea utriusque Siciliae eorumque historia et
anatome, 1. Parmae. https://doi.org/10.5962/bhl.title.79042

Pollution Control Department (2001) A report of sea water of Gulf of
Thailand. Ministry of Natural Resources and Environment, Bangkok,
Thailand.

Pope EC (1965) A review of Australian and some Indomalayan Ch-
thamalidae (Crustacea, Cirripedia). Proceedings of the Einnean So¬
ciety of New South Wales 90: 10-77.

Rawangkul S, Angsupanich S, Panitchart S (1995) Preliminary study of
barnacles damaging the mangrove plantation Rhizophora mucrona-
ta at Tha Phae canal, Nakom Si Thammarat. In: The ninth nation¬
al seminar on mangrove ecology, mangrove conservation for Thai
society in the next decade. National Research Council of Thailand
Bangkok. Paper No. III-06.

Ren X (1984) Studies on Chinese Cirripedia (Crustacea). III. Family
Chthamalidae. Studia Marina Sinica 22: 145-163.

Ren X, Eui R (1979) Studies on Chinese Cirripedia (Crustacea) II.
Family Tetraclitidae. Oceanologia et Eimnologia Sinica 10(4):
338-353.

Ross A, Perreault RT (1999) Revision of the Tetraclitellinae and de¬
scription of a new species of Newmanella Ross from the tropical
Westem-Atlantic Ocean (Cirripedia: Tetraclitoidea). Sessile organ¬
isms 15(2): 1-8. https://doi.org/10.4282/sosj.15.2_l

Rossel NC (1972) Some barnacles (Cirripedia, Thoracica) of Puerto Gal-
era found in the vicinity of the U.P. Marine Biological Eaboratory.
Natural and Applied Science Bulletin, Philippines 24: 143-285.

Santhakumaran EN, Sawant SG (1991) Biodeterioration of man¬
grove vegetation by marine organisms along Indian coast - an
annotated bibliography. Wood Biodegradation Division (Marine)
403004: 48.

Sophia Rani S, Pmbhu S, Przyadharshini S (2010) Infestation of bar¬
nacle {Balanus amphitrite) in the mangrove environment. World
Journal of Fish and Marine Sciences 2(4): 307-310.

Southward AJ (1964) On the European species of Chthama¬
lus stellatus (Cirripedia). Crustaceana 6: 241-254. https://doi.
org/10.1163/156854064X00010

Southward AJ, Burton RS, Coles SE, Dando PR, DeFelice R, Hoover J,
Parnell PE, Yamaguchi T, Newman WA (1998) Invasion of Hawai¬
ian shores by an Atlantic barnacle. Marine Ecology Progress Series
165: 119-126. https://doi.org/10.3354/mepsl65119

Southward AJ, Newman WA (2003) A review of some common In-
do-Malayan and western Pacific species of Chthamalus barnacles
(Crustacea: Cirripedia). Journal of the Marine Biological Associa¬
tion of the United Kingdom 83: 797-812. https://doi.org/10.1017/
S0025315403007835h

Stebbing TRR (1910) General catalogue of South African Crustacea.
Annals of the South Africa Museum 6(4): 563-575.

Stubbings HG (1964) Cirripedia from the Congo Estuary and adjacent
coasts in the Musee Royal de I’Afrique Centrale, Tervuren, Belgium.

Stubbings HG (1967) The Cirripedia fauna of tropical West African. Bulle¬
tin of the British Museum (Natural History), Zoology 15(6): 229-319.

Thiyagarajan V, Venugopalan V, Subramoniam T, Nair K (1997) De¬
scription of the naupliar stages of Megabalanus tintinnabulum (Cir¬
ripedia: Balanidae). Journal of Crustacean Biology 17(2): 332-342.
https://doi.org/10.2307/1549282

Tsang EM, Chan BKK, Wu TH, Ng WC, Chatterjee T, Williams GA,
Chu KH (2008) Population differentiation in the barnacle Chthama¬
lus malayensis: postglacial colonization and recent connectivity
across the Pacific and Indian Oceans. Marine Ecology Progress Se¬
ries 364: 107-118. https://doi.org/10.3354/meps07476

Tsang EM, Wu TH, Shih HT, Williams GA, Chu KH, Chan BKK (2012)
Genetic and morphological differentiation of the Indo-West Pacific
intertidal barnacle Chthamalus malayensis. Integrative and Compar¬
ative Biology 52: 388-409. https://doi.org/10.1093/icb/ics044

Utinomi H (1954) Invertebrate fauna of the intertidal zone of the Tokara
Islands. IX. Cirripedia. Publications of the Seto Marine Biological
Eaboratory 4: 17-26.

Utinomi H (1956) Colored illustrations of seashore animals of Japan.
168 pp. [pis. 64,1-VII]

Utinomi H (1959) Thoracic cirripeds from the environ of Banyuls. Vie
Milieu 10: 379-399.

Utinomi H (1960) On the world-wide dispersal of a Hawaiian
barnacle, Balanus amphitrite hawaiiensis Broch. Pacific Science
14(1): 43-50.

Utinomi H (1967) Comments on some new and already known cirripeds
with emended taxa with special reference to the parietal structure.
Publications of the Seto Marine Biology Eaboratory 15: 199-237.

Utinomi H (1968) Pelagic shelf and shallow-water cirripedia from the
Indo-west pacific. Videnskabelige Meddelelser fra Dansk Naturhis-
torisk Forening i Kobenhavn 131: 161-186.

Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia shore¬
lines, river systems and time durations. Journal of Biogeography 27:
1153-1167. https://doi.Org/10.1046/j.1365-2699.2000.00489.x

zse.pensoft.net

Pochai, A. et al.: The diversity of acorn barnacles (Cirripedia, Balanomorpha)...

Weltner W (1987) Verzeichnis der bisher beschriebenen recenten Cirri-
pedienarten. Archiv fiir Naturgeschichte 1: 227-280.

Wood W (1815) General conchology, or a description or shells arranged
according to the Linnean System 1. 246 pp.

Yamaguchi T (1987) Changes in the barnacle fauna since the Miocene
and the infraspecific structure of Tetraclita in Japan (Cirripedia:
Balanomorpha). Bulletin of Marine Science 41: 337-359.

Yan Y, Chan BKK (2004) A new barnacle species from Hong Kong: Ch-
thamalus neglectus sp. nov. (Cirripedia: Thoracica: Chthamalidae).
Journal of the Marine Biological Association of the United Kingdom
84: 133-138. https://doi.org/10.1017/S0025315404008999h

Yu MC, Kolbasov GA, Chan BKK (2016) A new species of sponge
inhabiting barnacle Bryozobia (Archaeobalanidae, Bryozobiinae) in
the West Pacific. ZooKeys 571: 1-20. https://doi.org/10.3897/zoo-
keys.571.6894

Zevina GB, Tarasov NI (1963) Cirripedia thoracica of the mainland
coasts of south-eastern Asia (Yellow, East and South China Seas).
Trudy Instituta Okeanology 70: 76-100.

Supplementary material 1

Arthropodal characters of Tetraclita kuro-
shioensis

Authors: Ashitapol Pochai, Sutin Kingtong, Woranop Sukparangsi,
Salinee Khachonpisitsak

Data type: species data

Explanation note: Tetraclita kiiroshioensis collected from (BUU16.
TC.TKOl) from Na Tai beach, Phang-nga. A.-I. Eight microscopy
on arthropodal characters. A. Cirri I, B.-C. Close up on cirri I show¬
ing serrulate setae, D. Cirri II, E.-F. Close up on cirri II showing
serrulate setae, G. Maxillule, H. Mandible, I. Eabrum.

Copyright notice: This dataset is made available under the Open Data¬
base Eicense (http://opendatacommons. 0 rg/licenses/odbl/l.O/). The
Open Database Eicense (ODbE) is a license agreement intended
to allow users to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided that the original
source and author(s) are credited.

Supplementary material 2

Arthropodal characters of Tetraclita singapo-
rensis

Authors: Ashitapol Pochai, Sutin Kingtong, Woranop Sukparangsi,
Salinee Khachonpisitsak

Data type: species data

Explanation note: Tetraclita singaporensis collected from (BUU16.
TC.TSG02) from Na Tai beach, Phang-nga. A.-I. Eight microscopy
on arthropodal characters. A. Cirri I, B.-C. Close up on cirri I show¬
ing serrulate setae, D. Cirri II, E.-F. Close up on cirri II showing
serrulate setae, G. Maxillule, H. Mandible, I. Eabrum.

Supplementary material 3

Arthropodal characters of Tetraclita squamosa

Authors: Ashitapol Pochai, Sutin Kingtong, Woranop Sukparangsi,
Salinee Khachonpisitsak

Data type: species data

Explanation note: Tetraclita squamosa collected from Hin Ngam beach,
Nakhon Si Thammarat (BUU16.TC.TS01). A.-I. Eight microscopy
on arthropodal characters. A. Cirri I, B.-C. Close up on cirri I show¬
ing serrulate setae, D. Cirri II, E.-F. Close up on cirri II showing
serrulate setae, G. Maxillule, H. Mandible, I. Eabrum.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 35-44 | DOI 10.3897/zse.93.11041

4>yEnsPFr.

museum fur naturkunde

Redescription of Nothobranchius lucius and description of a new species
from Mafia Island, eastern Tanzania (Cyprinodontiformes, Aplocheilidae)

Wilson J. E. M. Costa^

1 Laboratory of Systematics and Evolution ofTeleost Fishes, Institute of Biology, Federal University of Rio de Janeiro, Caixa Postal 68049, CEP
21941-971, Rio de Janeiro, Brazil

http://zoobank. org/5E9353 71-5 7D2-4D44-A 003-A61F40B54A85

Corresponding author: Wilson J. E. M. Co5to (wcosta@acd.ufrj.br)

Abstract

Received 3 November 2016
Accepted 10 January 2017
Published 16 January 2017

Academic editor;

Peter Bartsch

Key Words

Biodiversity hotspot
East African coastal forests
Nothobranchius melanospilus species
group

Rufiji River
systematics
taxonomy

Examination of specimens listed in the original description of Nothobranchius lucius re¬
vealed that they belong to two species. Nothobranchius lucius is redescribed based on the
type series and other specimens collected in the type locality area, the Kibasira Swamp
area, Rufiji River basin, Tanzania, at elevations between 250 and 300 m. Nothobranchius
insularis sp. n. is described on the basis of specimens collected in the north part of Mafia
Island, Tanzania, at about 10-15 m elevation. Nothobranchius lucius and A. insularis are
considered closely related species based on the shared presence of long jaws; caudal fin,
in males, with a broad dark grey to black band on its posterior margin; black dots over
the whole fiank, in females; metapterygoid curved, with its middle and dorsal portions
separated from the sympletic by a broad interspace; and posterior process of the quadrate
shorter than the ventral length of the quadrate without process. Characters useful to dis¬
tinguish them include premaxillary dentition, caudal fin shape, colour pattern of fiank and
unpaired fins in females, fin length, and number of neuromasts of the posterior section of
the anterior supraorbital series. Both species are members of a group that also includes
N. elongatus, N. hengstleri, N interruptus, N jubbi, N krammeri, and N. melanospilus,
which are all diagnosed by the presence of two neuromasts in the anterior section of the
anterior supraorbital series.

Introduction

The East Africa region comprising the coastal forests
of south-eastern Kenya and eastern Tanzania is an im¬
portant centre of biological diversity often known as
the East Africa biodiversity hotspot (EABH), with high
occurrence of endemic species (Myers et al. 2000, Aze-
ria et al. 2007). This region exhibits the greatest species
diversity of Nothobranchius Peters, 1868, a killifish ge¬
nus that occurs in a wide geographical portion of central
and eastern Africa (e.g., Parenti 1981). Among the about
60 valid species in the genus, 27 have been recorded in
EABH (e.g., Costa 2009, Dorn et al. 2014). Species of
Nothobranchius live in temporary pools formed during
the rainy season, where resistant eggs undergo diapause
during the dry season (e.g., Polacik et al. 2011, Pin-

ceel et al. 2015). In EABH, there are two rainy seasons,
the Tong rains’ (Masika), from March to May, and the
‘short rains’ (Muli), from October to December, which
alternate with dry periods when pools and some streams
completely disappear, as described first by Fitzgerald
(1898). Species of Nothobranchius and other African
and South American aplocheiloid killifishes possessing
this uncommon life cycle have been equivocally called
annual fishes, reflecting the past belief that these Ash¬
es have a single generation per year (e.g., Myers 1942).
Aplocheiloid killifishes with this life cycle have been al¬
ternatively known as seasonal killifishes in more recent
studies (e.g., Costa 2002).

Species of Nothobranchius have been recently pro¬
posed as model organisms for ageing processes since they
are naturally short-lived and easily bred in laboratories

Copyright Wilson J. E. M. Costa. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

Costa, WJ.M.: Redescription of Nothobranchius lucius and description of a new species...

(e.g., Genade et al. 2005, Harel et al. 2015). However,
they are mainly known as aquarium fishes due to the
striking eolouration exhibited by males of most speeies
in the genus. Consequently, in the last four deeades many
eolleeting trips in EABH have been reported in the aquar¬
ium fish literature (e.g., Seegers 1997, Wildekamp 2004;
Neumann 2008), which resulted in several new taxonom¬
ic records and descriptions of new species.

In a brief revision of the N. melanospilus species
group, Wildekamp et al. (2009) described N. lucius
Wildekamp, Shidlovskiy & Watters, 2009 on the basis of
material collected in the Kilombero River drainage, Tan¬
zania, which had been formerly identified as N. aflf. mela¬
nospilus in the aquarium fish literature (e.g., Wildekamp
2004). In the original description of N. lucius, specimens
from the Mafia Island, in Tanzania, previously identified
as N. melanospilus (Pfeflfer 1896) by Wildekamp (2004),
were listed as additional non-type material belonging to
N. lucius. The N. melanospilus species group was tenta¬
tively diagnosed by the presence of dark dots on the fiank
in females (i.e., black in N. melanospilus, dark brown in
N. lucius and pale grey in N. makondorum Wildekamp,
Shidlovskiy & Watters, 2009, according to Wildekamp et
al. 2009). Subsequently, monophyly of this species group
was supported in a multigene phylogeny (Dom et al.
2014). All specimens listed by Wildekamp et al. (2009)
is deposited in the Musee Royal de TAfrique Centrale
(MRAC), Tervuren, Belgium.

While studying aplocheilid collections deposited in
MRAC, discrepancies were found between data obtained
by the current author from that listed by Wildekamp et
al. (2009) from the same specimens. Consequently, a re¬
description of N. lucius is warranted and presented here.
Comparisons also indicated that the populations from the
Mafia Island, an off-shore island in the coast-line of Tan¬
zania, belong to a distinct, new species, which is herein
described.

Methods

All material examined is deposited in Musee Royal de
TAfrique Central, Tervuren (MRAC). Morphometric and
meristic data were taken following Costa (1988), except
for the snout length, measured between the anterior mar¬
gin of the orbit and the anterior extremity of the middle
portion of the upper jaw; measurements are presented as
percent of standard length (SL), except for those related
to head morphology, which are expressed as percent of
head length. Specimens with deformed body were not
measured to avoid unnecessary error. Fin-ray counts
include all elements. Osteological preparations (C&S)
were made according to Taylor and Van Dyke (1985).
Terminology for frontal squamation follows Hoedeman
(1958) and for cephalic neuromast series Costa (2001).
Species were delimited using unique combinations of
character states (diagnosability criterion; e.g., Davis and
Nixon 1992).

Results

Nothobranchius lucius Wildekamp, Shidlovskiy &
Watters, 2009

Fig. 1, Table 1

Nothobranchius lucius Wildekamp, Shidlovskiy & Watters, 2009: 247
(holotype: MRAC A7-02-P-9, 49.6 mm SL; type locality: large pool
on west side of road between Ifakara and the Kilombero River ferry,
2 km south of Ifakara, 1 km north of the Kilombero River, Tanzania,
8°10.30’S36°41.54’E).

Material examined. MRAC A7-02-P-9, holotype;
MRAC A7-02-P-10-25, 16 paratypes (1 C&S); Tanza¬
nia: pool on west side of the road between Ifakara and
the Kilombero River ferry, 2 km south of Ifakara, 1 km
north of the Kilombero River, 8°10.30’S 36°41.54’E,
about 250 m asl; B. Watters et al, 10 Jun. 2000. - MRAC
98-008-P-0007-0012, 6 paratypes; Tanzania: 2 km south
of Ifakara, on east side of the road to Kilombero Riv¬
er ferry, northernmost pool between village and ferry;
8°10.04’S 36° 41.61’E, about 250 m asl; B. Watters et
al, 1 Jun. 1995. - MRAC A7-02-P-26-27, 2; Tanzania:

I km south of Minepa village, large circular pool on
west side of Ifakara-Eupiro road, 17 km south of Ifakara;
8°16.34’S 36°40.83’E, about 270 m asl; B. Watters etal,

II Jun. 2000. - MRAC A7-02-P-28-32, 5; Tanzania: 2
km southwest of Eupiro on road to Malinyi, 27 km south
of Kilombero River ferry, ditch on southeast side of road;
8°23.45’S 36°39.45’E, about 300 m asl; B. Watters et
al, 11-12 Jun. 2000. - MRAC A7-02-P-37, 1; Tanzania:
small pool at culvert on southeast side of Ifakara-Ruipa
road, 37 km west of Ifakara, 0.5 km northeast of the Junc¬
tion to Narubungo village, on northern fianks of Kibasira
Swamp; 8°08.88’S 36°24.9EE, about 280 m asl; B. Wat¬
ters et al, 9 Jun. 2002.

Diagnosis. Nothobranchius lucius differs from all
other species of the N. melanospilus group, except N.
insularis, by having snout pointed in lateral view, jaws
moderately long (vs. snout blunt to weakly pointed, jaws
short); caudal fin, in males, with broad dark grey to black
band on the posterior margin (vs. narrow); presence, in fe¬
males, of dark dots over the whole flank (dark dots when
present restricted to the posterior portion of the flank). It
is distinguished from N. insularis by having inner pre¬
maxillary teeth larger than teeth of the outer premaxillary
tooth row (vs. smaller); caudal fin rounded in males (vs.
subtruncate); in females, flank dark dots are rounded and
arranged in horizontal rows (vs. dots vertically elongated,
often arranged in oblique rows); unpaired fins, in females,
with dark grey dots extending over most fin (dots restrict¬
ed to the basal portion of unpaired fins); caudal, pectoral
and pelvic fins longer (caudal fin length in males 31.3-
34.9 % SE and 30.3-32.9 % SE in females of N. lucius,
vs. 26.9-29.6 % SE in males and 22.8-27.4 % SE in fe¬
males of N. insularis', pectoral-fin length 22.2-24.5 % SE
in males and 20.2-24.6 % SE in females, vs. 17.1-21.8
% SE and 14.2-19.3 % SE, respectively; pelvic-fin length
11.6-13.1 % SE in males and 11.5-13.0 % SE in females.

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Zoosyst. Evol. 93 (1) 2017, 35-44

Figure 1. Nothobranchius lucius: A. MRAC A7-02-P-9, holotype, male, 49.6 mm SL; Tanzania; 2 km S of Ifakara; B. MRAC A7-
02-P-26-27, male, 59.4 mm SL; Tanzania: 1 km S of Minepa; C. MRAC A7-02-P-26-27, female, 55.8 mm SL; Tanzania: 1 km S
of Minepa.

vs. 8.6-11.0 % SL and 9.6-11.0 % SL, respectively); and
two neuromasts in the posterior section of the anterior su¬
praorbital series (vs. three).

Description. Morphometric data appear in Table 1.
Dorsal profile slightly concave to nearly straight on head,
convex from nape to posterior end of dorsal-fin base,
about straight on caudal peduncle; ventral profile convex
from lower jaw to anal-fin base, about straight on caudal

peduncle. Body deep, compressed. Greatest body depth
at vertical between bases of pectoral and pelvic fins. Jaws
short, snout blunt in lateral view. Jaw teeth canine, nu¬
merous, irregularly arranged, outer teeth greater than in¬
ternal teeth. Gill-rakers of first branchial arch 4 + 14-15.
Six branchiostegal rays.

Dorsal and anal fins moderate in males, extremity
rounded, with short filamentous rays along distal margin.

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Costa, WJ.M.: Redescription of Nothobranchius lucius and description of a new species...

6°D'0"S

7“0'0"S

8“0'0"S

9®0'0"S

37‘’0"0"E 38®0'0"E 39‘^0'0"E 40^0'0"E

Figure 2. Geographical distribution of Nothobranchius lucius (stars), Nothobranchius cf lucius (square), and Nothobranchius
insularis sp. n. (circles); dotted areas are marshes.

Table 1. Morphometric data of Nothobranchius lucius.

Holotype

pa retypes

male

males (7)

females (9)

Standard length (mm)

49.6

40.4-53.7

35.7-52.4

Percent of standard length

Body depth

27.4

27.0-31.8

24.6-29.6

Caudal peduncle depth

14.9

13.8-16.0

12.4-13.9

Pre-dorsal length

61.3

59.9-68.7

62.6-66.4

Pre-pelvic length

53.3

50.6-54.4

50.7-56.4

Length of dorsal-fin base

25.1

23.2-25.9

18.4-22.9

Length of anal-fin base

23.2

22.2-25.5

15.9-18.5

Caudal-fin length

31.2

31.7-34.9

30.3-32.9

Pectoral-fin length

22.3

22.2-24.5

20.2-24.6

Pelvic-fin length

12.0

11.6-13.1

11.5-13.0

Head length

33.0

31.8-34.6

31.9-34.9

Percent of head length

Head depth

78.4

72.7-84.8

65.7-75.7

Head width

66.7

64.6-70.4

62.5-68.3

Snout length

35.0

32.5-37.1

30.7-33.9

Lower jaw length

30.9

30.2-33.6

28.2-30.4

Eye diameter

23.1

22.7-26.2

23.0-27.0

dorsal fin longer than anal fin; in females, dorsal fin round¬
ed, anal fin sub-triangular and slightly longer than dorsal
fin. Caudal fin subtruncate. Pectoral fin rounded, poste¬
rior extremity between pelvic-fin base and anus. Pelvic
fin small, tip reaching urogenital papilla; pelvic-fin bases
medially in contact. Dorsal-fin origin on vertical between
base of first and second anal-fin rays. Dorsal-fin rays 14-

16; anal-fin rays 16-18; caudal-fin rays 29-31; pectoral-fin
rays 19-20; pelvic-fin rays 6. Minute contact organs on
first and second pectoral-fin rays and distal portion of dor¬
sal fin in males; rows of papillate contact organs along two
distal thirds of most rays of anal fin in males.

Scales small, cycloid; body and head entirely scaled,
except ventral surface of head. Minute filamentous contact
organs along posterior margin of scales on middle portion
of fiank and latero-ventral portion of head in males. Body
squamation extending over anterior 30 % of caudal-fin
base; no scales on dorsal and anal-fin bases. Frontal squa¬
mation irregularly arranged in two longitudinal rows.
Longitudinal series of scales 29-30; transverse series of
scales 9-11; scale rows around caudal peduncle 16.

Anterior supraorbital series of neuromasts arranged
in single section placed in shallow depression, with five
neuromasts; in specimens above 45 mm SL, anterior se¬
ries partially divided in two sections, with two larger neu¬
romasts in each section and smaller one between them.
Posterior supraorbital series with four neuromasts placed
in shallow depression. Infraorbital series with 16-17 neu¬
romasts, pre-opercular series 12-13, mandibular 10-13.
One neuromast per scale of lateral line.

Colouration in alcohol (Fig. 1). Males. Flank, dorsum
and head light brown, darker on posterior portion of scales
of dorsal portion of fiank, dorsum and opercle; venter
pinkish grey; pale grey spots on suborbital region; branchi-
ostegal membrane dark grey. Dorsal and anal fins hyaline
with transverse series of grey spots, almost inconspicuous

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Zoosyst. Evol. 93 (1) 2017, 35-44

in anal fin. Caudal fin pale yellow with broad dark grey to
black stripe along whole fin margin, broader on posterior
margin; posterior sub-marginal area lighter. Pectoral fin
hyaline, pelvic fin greyish hyaline with black tip.

Females. Flank and dorsum pale brown, side of head
and venter pale yellow; rounded dark brown to black
dots highly concentrated on whole trunk and head except
venter, irregularly arranged in horizontal rows on flank.
Whole unpaired fins hyaline with dark grey dots. Paired
fins hyaline; few dark grey dots on basal portion of pec¬
toral fin.

Distribution. Nothobranchius lucius occurs in locali¬
ties along the Kilombero Valley, which is limited to west
by the Udzungwa Mountains and to east by the Mbari-
ka Mountains, forming the Kibasira Swamp that is part
of the Rufiji River basin (Fig. 2). This region is about
300 km from the coastline and collecting localities are
situated at between 250 and 300 m asl. Two specimens
collected in the Luhule River floodplains, in coastal Tan¬
zania (MRAC A7-02-P-35-36, one male and one female,
7°19.95’S 39°17.38’E, at about 20 m asl) are here tenta¬
tively identified as N. lucius. This species has been also
recorded from the Mbezi and Ruhoi river basins, eastern
Tanzanian (Wildekamp et al. 2009), but no specimen
was deposited in museum collections, making identity of
these records still uncertain.

Nothobranchius insularis sp. n.

http://zoobank.org/CC856CE9-244D-4642-9727-C41B819B28E7
Fig. 3, Table 2

Holotype. MRAC A7-02-P-33, 1 male, 52.9 SL; Tanza¬
nia: Mafia Island, approximately 3 km south of Kiron-
gwe, 7°49.58’S 39°48.87’E, about 15 m asl; B. Watters
et al., 31 May 2002.

Paratypes. MRAC A7-02-P-34, 1 female, 46.4 mm
SE; collected with holotype. MRAC A702-P-38-44, 4
males, 43.7-55.2 mm SE (1 C&S), 3 females, 44.0^9.8
mm SE; Tanzania: Mafia Island, approximately 0.5 km
east of Kirongwe, 7°48.12’S 39°49.97’E, about 10 m asl;
same collectors and date as holotype.

Diagnosis. Nothobranchius insularis is distinguished
from all species of the N. melanospilus group, except N.
lucius, in possessing snout pointed in lateral view, jaws
moderately long (vs. snout blunt to weakly pointed, jaws
short); caudal fin, in males, with broad dark grey to black
band on the posterior margin (vs. narrow); presence, in
females, of dark dots over the whole flank (dark dots
when present restricted to the posterior portion of the
flank). The new species differs from N. lucius by having
inner premaxillary teeth smaller than teeth of the outer
premaxillary tooth row (vs. larger); caudal fin subtruncate
in males (vs. rounded); in females, flank dark dots are ver¬
tically elongated and often arranged in oblique rows (vs.
dots rounded, arranged in horizontal rows); unpaired fins,
in females, with dark grey dots when present restricted to
their basal portion (extending over most fin); caudal, pec¬

toral and pelvic fins shorter (caudal fin length 26.9-29.6
% SE in males and 22.8-27.4 % SE in females of N. insu¬
laris, vs. 31.3-34.9 % SE in males and 30.3-32.9 % SE in
females of N. lucius', pectoral-fin length 17.1-21.8 % SE
in males and 14.2-19.3 % SE in females, vs. 22.2-24.5
% SE and 20.2-24.6 % SE, respectively; pelvic-fin length
8.6-11.0 % SE in males and 9.6-11.0 % SE in females,
vs. 11.6-13.1 % SE and 11.5-13.0 % SE, respectively);
and three neuromasts in the posterior section of the ante¬
rior supraorbital series (vs. two).

Description. Morphometric data appear in Table 2.
Dorsal and ventral profiles slightly convex from snout to
posterior end of dorsal and anal-fin bases, about straight
on caudal peduncle. Body relatively slender, compressed.
Greatest body depth at vertical just in front of pelvic-fin
base. Jaws slightly elongated, snout pointed in lateral
view. Jaw teeth canine, numerous, irregularly arranged,
outer teeth greater than internal teeth. Gill-rakers of first
branchial arch 4-5 + 14-15. Six branchiostegal rays.

Dorsal and anal fins broad in males, extremity round¬
ed, with short filamentous rays along distal margin, dor¬
sal fin slightly longer than anal fin; in females, dorsal fin
rounded, anal fin sub-triangular and slightly longer than
dorsal fin. Caudal fin subtruncate. Pectoral fin rounded,
posterior extremity between pelvic-fin base and anus.
Pelvic fin small, tip reaching between anus and urogen¬
ital papilla; pelvic-fin bases medially in close proximi¬
ty. Dorsal-fin origin on vertical between base of first and
third anal-fin rays. Dorsal-fin rays 15-16; anal-fin rays
16-18; caudal-fin rays 29-30; pectoral-fin rays 19; pel¬
vic-fin rays 6. Minute contact organs on first and second
pectoral-fin rays in males; rows of papillate contact or¬
gans along distal portion of middle dorsal-fin rays and
two thirds of most rays of anal fin in males.

Scales small, cycloid; body and head entirely scaled,
except ventral surface of head. Minute filamentous contact
organs along posterior margin of scales on middle portion
of flank and latero-ventral portion of head in males. Body
squamation extending over anterior 40 % of caudal-fin
base; no scales on dorsal and anal-fin bases. Frontal squa¬
mation irregularly arranged in two longitudinal rows.
Eongitudinal series of scales 31-32; transverse series of
scales 9-10; scale rows around caudal peduncle 16.

Anterior supraorbital series of neuromasts arranged in
two separate sections, each placed in shallow depression,
the anterior section with two neuromasts, the posterior
one with three; sometimes minute neuromast between
depressions. Posterior supraorbital series with four neu¬
romasts placed in shallow depression. Infraorbital series
with 18-21 neuromasts, pre-opercular series 14-18, man¬
dibular 17-18. One neuromast per scale of lateral line.

Colouration in alcohol (Fig. 3). Males. Flank, dor¬
sum and head light brown, darker on posterior portion
of scales of dorsal portion of flank, dorsum and opercle;
venter pinkish grey; branchiostegal membrane dark grey.
Dorsal and anal fins hyaline with transverse series of grey
spots, almost inconspicuous in anal fin. Caudal fin pale
yellow with dark grey to black stripe along whole fin

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Figure 3. Nothobranchius insularis sp. n.: A. MRAC A7-02-P-33, holotype, male, 52.9 mm SL; Tanzania: 3 km S of Kirongwe,
Mafia Island; B. MRAC A7-02-P-38-44, paratype, male, 48.3 mm SL; Tanzania; 0.5 km S of Kirongwe, Mafia Island; C. MRAC
A7-02-P-38-44, paratype, female, 49.8 mm SL; Tanzania: 0.5 km S of Kirongwe, Mafia Island.

margin, broader on posterior margin. Pectoral fin hyaline,
pelvic fin greyish hyaline with black tip.

Females. Flank and dorsum pale brown, side of head
and venter pale yellow; vertically elongated dark grey to
black dots irregularly arranged in oblique rows on whole

flank; sometimes few pale grey dots on opercular region.
Unpaired fins hyaline; elongated grey dots on basal por¬
tion of dorsal fin; anal and caudal fin often without dark
marks, sometimes with almost inconspicuous pale grey
dots on basal portion. Paired fins hyaline.

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Table 2. Morphometric data of Nothobranchius insularis.

Holotype

paratypes

male

males (3)

females (4)

Standard length (mm)

52.9

37.4-46.1

44.0-49.8

Percent of standard length

Body depth

30.9

29.7-30.4

26.4-29.9

Caudal peduncle depth

15.0

13.6-14.8

13.3-14.1

Pre-dorsal length

63.5

59.9-65.2

64.7-66.7

Pre-pelvic length

51.4

48.5-51.1

50.7-52.0

Length of dorsal-fin base

24.7

20.5-25.4

19.1-21.5

Length of anal-fin base

23.0

20.1-24.0

15.1-16.9

Caudal-fin length

27.1

26.9-29.6

22.8-27.4

Pectoral-fin length

18.5

17.1-21.8

14.2-19.3

Pelvic-fin length

10.0

8.6-11.0

9.6-11.0

Head length

32.1

31.0-32.3

29.5-32.8

Percent of head length

Head depth

85.3

79.3-82.7

77.1-81.2

Head width

67.0

65.0-65.8

64.6-70.1

Snout length

34.0

26.9-32.1

32.7-37.7

Lower jaw length

33.6

29.7-32.8

26.7-30.8

Eye diameter

26.7

26.7-27.9

26.4-28.8

Etymology. From the Latin insularis, meaning per¬
taining to an island and referring to the occurrence of the
new species on Mafia Island.

Distribution. Nothobranchius insularis is known
from two close localities in the northern part of the Mafia
Island, Tanzania, at about 10-15 m asl (Fig. 2).

Discussion

Wildekamp et al. (2009) designated the type series of
N. lucius containing the holotype and 22 paratypes that
were collected in the Kilombero River drainage. An addi¬
tional 18 non-type specimens were also listed. However,
the table of morphometric and meristic data included in
that paper indicates a total of 53 specimens of N. lucius
examined, not 41 as indicated above. Such discrepancy
supports the idea that the number of specimens used in
the description was larger than that reported in the type
material list, even when adding specimens listed under
the non-types section that also includes material herein
described as N. insularis. It is remarkable to notice that
the type series of N. lucius includes some specimens that
are poorly preserved (e.g. part of MRACA7-02-P-10-25).
These latter specimens have deformed body and dam¬
aged fins. Interestingly, other non-type specimens that
are listed from the same drainage are well preserved (e.g.
MRAC A7-02-P-26-27, 28-32).

Herein I speculate that measurements derived from
poorly preserved specimens contributes to the variation
presented by Wildekamp et al. (2009), which exceeds
the variation reported herein based solely on the well
preserved specimens reported by these authors. In
addition, I have found discrepancies in what they report
for some meristic characters, which are not subject to
misinterpretation due to poor preservation. For example.

Wildekamp et al. (2009) report the following for A. lucius:
dorsal-fin rays 14-17, anal-fin rays 15-19, longitudinal
series scales 31-35, and transverse series scales 12-14.
Herein, however, I document that dorsal-fin rays range
from 15-17, never 14; anal-fin rays range from 16-18,
never 15 nor 19; longitudinal series scales range from
31-33, never 34 nor 35; and transverse series scales were
9-10, never 12-14. Lower fin-ray counts reported by
Wildekamp et al. (2009) may be due to the first ray being
often minute and embedded by thick epithelial tissue, but
other differences noted above can not be explained.

Wildekamp et al. (2009: 238) distinguished N. lucius
from other morphologically similar congeners by it hav¬
ing a more slender body and stronger dentition. When
diagnosing N. lucius, Wildekamp et al. (2009: 247)
distinguished this species from N. melanospilus and N.
makondorum by the longer head, longer snout and more
slender body in males. Morphometric values presented in
that study, however, were notably overlapped among the
three species, indicating that these characters are not use¬
ful to elFectively distinguish species of the N. melanospi¬
lus group. I confirm this conclusion in the present study.
The present comparison of jaw dentition in species of the
N. melanospilus group also indicates that the dentition of
N. lucius and N. insularis is not stronger than in other
species, but in fact, N. lucius and N. insularis differs from
other species of the group by both having more elongat¬
ed jaw bones, which often yields a pike-like appearance
in lateral view. In N. lucius and N. insularis the length
between the anterior border of the dentary and the pos¬
terior tip of the angulo-articular is longer than the length
between the anterior tip of the quadrate and the posterior
margin of the preopercle (Fig. 4A; vs. shorter in the re¬
maining species of the N. melanospilus group. Fig. 4B).

According to Wildekamp et al. (2009: 238), N. lucius
may be distinguished from other species of the N. mela¬
nospilus group by two colouration characters: “a denser
pattern of dark brown (not black) spots on the body, head
and all fins of the females” (vs. black spots on the flank
and base of the unpaired fins in N. melanospilus and grey
spots on the flank in N. makondorum), and “a wide black
margin and orange-red submargin to the caudal fin” in
males (vs. caudal fin red with a narrow black margin).
However, the first diagnostic character does not corre¬
spond to the figure of a live female of N. lucius from the
type locality that is included in that same paper. The fe¬
male in the figure shows that black dots, not brown, cover
the whole flank, the side of the head, and the unpaired
fins (Wildekamp et al. 2009: 248, fig. 9). In preserved
females of N. lucius here examined, dots are dark brown
to black, rounded, and distributed on the whole flank, side
of the head, a large portion of the unpaired fins, and the
basal portion of the pectoral fin; the dots of the flank are
mainly arranged in horizontal rows (Fig. 1C). The col¬
our pattern documented here for N. lucius greatly differs
from the colour pattern exhibited by preserved females of
N. insularis. In this species, dark grey to black dots are
vertically elongated and mainly arranged in oblique rows

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Figure 4. Jaws, jaw suspensorium and opercular apparatus, left side, lateral view, of; A. Nothobranchius lucius, paratype, male,
MRACA7-02-P-10-25,43.0 mm SL; B. N. melanospilus, male, UFRJ 6591,43.5 mm SL. Larger stippling indicates cartilage. Scale
bar = 1 mm.

on the flank, being rare or absent on the side of the head,
and are restricted to the basal portion of the unpaired flns,
while being absent on the pectoral fln (Fig. 2C). The oc¬
currence of this female colour pattern in live exemplars of
N. insularis is confirmed in a photograph of a live female,
published in an aquarium journal paper that is a report of
a collecting trip in the Mafia Island (Nagy 2009: 154).

Wildekamp et al. (2009) first diagnosed the N. melano¬
spilus group, comprising N. lucius, N. makondorum and
N. melanospilus, on the basis of the presence of dark dots
on the flank of females. However, examination of the ma¬
terial listed by Wildekamp et al. (2009) as belonging to N.
makondorum revealed that only female specimens from
the type locality area (i.e., Ruvuma River basin, southern
Tanzania) have grey dots on the flank, whereas specimens
from all other areas to south do not show dark pigmen¬

tation. Although this group is corroborated by molecular
data (Dorn et al. 2014), no unique morphological char¬
acter was found to be useful to unambiguously diagnose
the N. melanospilus group as delimited by Wildekamp et
al. (2009). On the other hand, a more inclusive clade also
comprising A. elongatusNsf iXdQkamp, 1982, A. hengstleri
Valdesalici, 2007, A. insularis, A. interruptus Wildeka¬
mp & Berkenkamp, 1979, A jubbi Wildekamp & Berk-
enkamp, 1979, and A krammeri Valdesalici, 2008, in
adittion to A. lucius, A. makondorum and A melanospi¬
lus, is here diagnosed by the presence of two neuromasts
in the anterior section of the anterior supraorbital series
(Fig. 5). In other nothobranchines, the anterior section
contains a single neuromast. The A melanospilus group
as herein delimited is also supported by molecular data
(Wildekamp et al. 2009, Dom et al. 2014). Therefore, I

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Zoosyst. Evol. 93 (1) 2017, 35-44

Figure 5. Diagrammatic representation of the latero-sensory system on the dorsal surface of the head in: A. Nothohranchius lucius,
MRAC A7-02-P-28-32, male, 43.6 mm SL; B. Nothohranchius insularis sp. n., MRAC A702-P-38-44, paratype, male, 48.3 mm
SL. arn - anterior rostral neuromast; asass - anterior section of the anterior supraorbital series; prn - posterior rostral neuromast;
psass - posterior section of the anterior supraorbital series; pss - posterior supraorbital series.

Figure 6. Left isolated premaxilla, dorsal view, ascending pro¬
cess inclined backwards, of A. Nothohranchius lucius, paratype,
male, MRAC A7-02-P-10-25, 43.0 mm SL. B. Nothohranchius
insularis sp. n., paratype, male, MRAC A702-P-38-44, 43.7
mm SL. Scale bar = 1 mm.

propose to include all the eight species listed above in the
N. melanospilus group.

Monophyly of the group comprising N. lucius and N.
insularis is supported by derived characters states used to
distinguish them from other congeners, including the pres¬
ence of dark dots on the whole flank in females and the
relatively long jaws, as discussed above. The present study
also indicates that two character states of the Jaw suspenso-

rium are uniquely found in N. lucius and N. insularis: the
metapterygoid is curved and its middle and dorsal portions
are separated from the sympletic by a broad interspace (vs.
nearly straight and in close proximity or in contact with
sympletic) and the posterior process of the quadrate is
short, its length shorter than the ventral length of the quad¬
rate without process (vs. approximately equal or greater)
(Fig. 4). Among species of the N. melanospilus group, N.
lucius is unique in having an inner row of teeth directed
inside the mouth on the median portion of premaxilla that
are longer than the teeth of the external row (Figs 4 and 6).

Acknowledgements

This study was developed during a six-month stay at Musee
Royal de FAfrique Centrale, Tervuren, Belgium (MRAC),
funded by CNPq (Conselho Nacional de Desenvolvi-
mento Cientlflco e Tecnologico - Ministerio de Ciencia e
Tecnologia, Brazilian Federal Government, grant process
200627/2015-5). I am especially grateful to Jos Snoecks
for providing me the necessary conditions to study African
killiflshes at MRAC. Thanks are also due to Miguel Par-
rent, Baudouin Mafuta and Emmanuel Abwe for technical
assistance. The manuscript befitted from the valuable crit¬
icisms provided by Emmanuel Vreven and Thomas Phil-
brick, and to Peter Bartsch for editorial support.

References

Azeria ET, Sanmartin I, As S, Carlson A, Burgess N (2007) Biogeo¬
graphic patterns of the East African coastal forest vertebrate fauna.
Biodiversity and Conservation 16: 883-912. https://doi.org/10.1007/
si0531-006-9022-0

zse.pensoft.net

Costa, WJ.M.: Redescription of Nothobranchius lucius and description of a new species...

Costa WJEM (1988) Sistematica e distribui 9 ao do complexo de espe-
cies Cynolebias minimus (Cyprinodontiformes, Rivulidae), com a
descri 9 ao de duas especies novas. Revista Brasileira de Zoologia 5;
557-570. https://doi.org/10.1590/SO 101-81751988000400004
Costa WJEM (2001) The neotropical annual fish genus Cynolebias
(Cyprinodontiformes: Rivulidae): phylogenetic relationships, tax¬
onomic revision and biogeography. Ichthyological Exploration of
Freshwaters 12: 333-383.

Costa WJEM (2002) The neotropical seasonal fish genus Nematolebias
(Cyprinodontiformes: Rivulidae: Cynolebiatinae): taxonomic revi¬
sion with description of a new species. Ichthyological Exploration
of Freshwaters 13: 41-52.

Costa WJEM (2009) Species delimitation among populations of the
eastern Tanzanian seasonal killifish Nothobranchius korthausae
(Cyprinodontiformes: Nothobranchiidae). Ichthyological Explora¬
tion of Freshwaters 20: 111-126.

Davis JI, Nixon KC (1992) Populations, genetic variation, and the de¬
limitation of phylogenetic species. Systematic Biology 41: 421-435.
https://doi.Org/10.1093/sysbio/41.4.421
Dom A, Musilova Z, Platzer M, Reichwald K, Cellerino A (2014) The
strange case of East African annual fishes: aridification correlates
with diversification for a savannah aquatic group? BMC Evolution¬
ary Biology 14: 210. https://doi.org/10.1186/sl2862-014-0210-3
Fitzgerald WWA (1898) Travels in the coastlands of British East Africa and
the islands of Zanzibar and Pemba. Chapman & Hall, Eondon, 834 pp.
Genade T, Benedetti M, Terzibasi E, Roncaglia P, Valenzano DR, Catta-
neo A, Cellerino A (2005) Annual fishes of the genus Nothobranchius
as a model system for aging research. Aging cell 4: 223-233. https://
doi.org/10.1111/j. 1474-9726.2005.00165.X
Harel I, Benayoun BA, Machado B, Singh PP, Hu C-K, Pech ME,
Valenzano DR, Zhang E, Sharp SC, Artandi SE, Brunet A (2015)
A platform for rapid exploration of aging and diseases in a naturally
short-lived vertebrate. https://doi.Org/10.1016/j.cell.2015.01.038
Hoedeman JJ (1958) The frontal scalation pattern in some groups of tooth-
carps (Pisces, Cyprinodontiformes). Bulletin of Aquatic Biology 1:23-28.

Myers GS (1942) Studies on South American freshwater fishes I. Stan¬
ford Ichthyological Bulletin 2: 89-114.

Myers N, Mittermeir RA, Mittermeir CG, da Fonseca GAB, Kent J
(2000) Biodiversity hotspots for conservation priorities. Nature 403:
853-858. https://doi.Org/10.1038/35002501

Nagy B (2009) Die Insel Mafia. DKG-Journal 41: 146-157.

Neumann W (2008) Prachtgrundkarpfiinge. Supplement 9. Deutsche
Killifisch Gemeinschaft, Marktheidenfeld, 128 pp.

Parent! ER (1981) A phylogenetic and biogeographic analysis of cyp-
rinodontiform fishes (Teleostei, Atherinomorpha). Bulletin of the
American Museum of Natural History 168: 335-557. http://hdl.han-
dle.net/2246/438

Pinceel T, Vanschoenwinkel B, Deckers P, Gregoir A, Ver Eecke T,
Brendonck E (2015) Early and late developmental arrest as com¬
plementary embryonic bet-hedging strategies in African killifish.
Biological Journal of the Einnean Society 114: 941-948. https://doi.
org/10.1111/biJ.12474

Polacik M, Donner MT, Reichard M (2011) Age structure of annual
Nothobranchius fishes in Mozambique: is there a hatching synchro¬
ny? Journal of Fish Biology 78: 796-809. https://doi.org/10.llll/
J.1095-8649.2010.02893.X

Seegers E (1997) Killifishes of the world. Old World killis II. Verlag
ACS, Mbrfelden-Walldorf, 109 pp.

Taylor WR, Van Dyke GC (1985) Revised procedures for staining
and clearing small fishes and other vertebrates for bone and carti¬
lage study. Cybium 9: 107-109. http://sfi.mnhn.fr/cybium/numer-
os/1985/92/01 -Taylor%5b92%5d 107-119.pdf

Wildekamp RH (2004) A world of killies: atlas of the oviparous cyp-
rinodontiform fishes of the world, vol. 4. The American Killifish
Association, Elyria, Ohio, 398 pp.

Wildekamp RH, Shidlovskiy KM, Watters BR (2009) Systematics of the
Nothobranchius melanospilus species group (Cyprinodontiformes:
Nothobranchiidae) with description of two new species from Tan¬
zania and Mozambique. Ichthyological Exploration of Freshwaters
20: 237-254.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 45-94 | DOI 10.3897/zse.93.10039

4>yEnsPFr.

museum fur naturkunde

An illustrated catalogue of Rudolf Sturany’s type specimens in
the Naturhistorisches Museum Wien, Austria (NHMW):

Red Sea gastropods

Paolo G. Albano\ Piet AJ. Bakker^, Ronald Janssen^, Anita Eschned

1 Department of Palaeontology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

2 Natiiralis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands

3 Malacology Section, Senckenberg Research Institute and Natural History Museum, Senckenberganlage 25, 60325 Frankfurt am Main, Germany,

4 Naturhistorisches Museum Wien, 3. Zoologische Abteilung, Burgring 7, 1010 Wien

http://zoobank.org/0BAlB843-2BD4-49FC-8FDA-F68041A5D167
Corresponding author; Paolo G. Albano (pgalbano@gmail.com)

Received 3 September 2016
Accepted 29 November 2016
Published 18 January 2017

Academic editor:

Matthias Glaubrecht

Key Words

Type specimens
Pola expeditions
deep-sea
Gastropoda
Indo-Pacific province
Red Sea
Rudolf Sturany

Abstract

The Natural History Museum in Vienna hosts the samples of the late 19* century Aus¬
tro-Hungarian “Pola” expeditions to the Eastern Mediterranean and the Red Sea. Rudolf
Sturany studied these samples and described several new species. The type material of
35 species and forms of gastropods collected in the Red Sea is listed and illustrated. For
each species, the available type material is listed, the original description and a translation
into English is provided, and the current taxonomic status of the species is commented
upon whenever possible. All species are illustrated in colour and with SEM imaging, with
the exception of Stylifer thielei, whose only specimen was broken by Johannes Thiele in
Berlin to study the soft parts. Finally, a table of the Pola deep and coastal stations where
molluscs were collected is provided, with modern names.

Introduction

Rudolf Sturany was a malacologist who worked at the Nat¬
ural History Museum (Naturhistorisehes Museum Wien,
NHMW) in Vienna between 1889 and 1922. He studied
the samples collected by the Austro-Hungarian deep-sea
expeditions to the Eastern Mediterranean Sea and the Red
Sea aboard the vessel “Pola”, the first to explore the deep
habitats of the Red Sea (Janssen and Taviani 2015). For a
detailed account of the Austro-Hungarian deep-sea expe¬
ditions see Schefbeck (1996) and, for the material collect¬
ed by the “Pola” expeditions, see Stagl et al. (1996).

Sturany described several molluscan species (Stur¬
any 1896, 1899, 1900a,b, 1903). This paper focuses on
the 35 gastropod taxa described in two different works

(Sturany 1900a,b and 1903). In 1900, Sturany described
a first batch of deep water species (Solariella illustris,
Fusus bifrons, Nassa thaumasia, Nassa steindachneri,
Nassa xesta, Nassa munda, Nassa lathraia, Nassa stiph-
ra, Nassa sporadica, Columbella erythraeensis, Colum-
bella nomanensis, Pleurotoma nannodes, Pleurotoma
potti, Pleurotoma inchoata and Pleurotoma siebenrocki).
This paper was published in two issues of the journal An-
zeiger der Kaiserlichen Akademie der Wissenschaften,
Mathematisch-Naturwissenschaftliche Classe, and it did
not have figures. The main work on Red Sea gastropods
was published later in the Denkschriften der kaiserlichen
Akademie der Wissenschaften, in 1903. It listed all the
species found and illustrated all the new species, whether
described in 1900 or 1903. Tables with locality data were

Copyright Paolo G. Albano et al. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

provided. It is important to highlight that the 1903 work
included a repeat of the descriptions of the species de¬
scribed in 1900. A line just before the description refers
to the original description in the Anzeiger. Moreover, in
some later works, this paper is cited as being published in
1904, probably because the volume of the Denkschriften
had this date on the frontispiece. However, the first page
of this work specifies that it was vorgelegt in der Sitzu-
ng am 2 April 1903 (presented in the meeting of 2 April,
1903). In the library of the Natural History Museum of
Vienna, preprints {Besenders abgedruckt...) with double
pagination published in 1903 (date on their frontispiece)
are present, and this should be considered the correct year
of publication for the new names therein introduced.

Knowledge about name-bearing types is fundamental to
sound taxonomic research. Indeed, the International Code of
Zoological Nomenclature (ICZN 1999: 72F.4) recommends
the publication of lists of types housed in institutions. Our
work follows this recommendation; moreover, we tried to
provide to the taxonomic community detailed illustrations of
type specimens and their diagnostic characters.

A glimpse on Rudolf Sturany’s life

Rudolf Sturany (13 April 1867 - 28 February 1935) was
a Viennese zoologist and one of the most important Aus¬
trian malacologists. He studied at the Universities of Vi¬
enna and Leipzig and obtained his PhD in 1891 in Vienna
(Adensamer 1935a, b, c; Stagl 2012). He began to work
as a volunteer at the Natural History Museum of Vienna
in September 1889. One year later he started his official
career at the NHMW as assistant, became adjunct curator
in 1901 and 6 years later curator, being responsible for
the collections of molluscs, bryozoans, brachiopods and
tunicates. Excursions for scientific research took him to
Bosnia, Herzegovina, Dalmatia, Montenegro, Albania and
Crete, where he found and described several species new
to science, especially land and freshwater snails. His good
contacts with zoologists and malacologists of his time en¬
abled Sturany to work on important scientific material (the
"Taurus" expedition to the Sea of Marmara, Obrutschew’s
expedition to the region of Pamir, the "Pola" expeditions).
He obtained important collections (Obrutschew, Tschapek,
Gerstenbrandt, parts of Mollendorffs, Monterosato’s and
Velitschowsky’s collections), which led to an enormous
growth and enrichment of the Museum mollusc collection.
During World War I, an eye disease occurred and steadi¬
ly deteriorated, forcing Sturany to retire in 1922, after 33
years dedicated to his malacological work at the NHMW.

Malacological collections attheNaturhis-
torisches Museum Wien

Besides the important type-material of Sturany, there are
other valuable types of historical importance at the mol¬
lusc collection of the NHMW. Ignaz von Born established

its oldest part with his work on the imperial collection,
which was published in the 1778 “Index rerum naturali-
um Musei C^sarei Vindobonensis - Pars I. Testacea”
and in the superb 1780 volume “Testacea Musei Caesarei
Vindobonensis, quae jusso Mariae Theresiae Augustae”
(Eschner 2005). Eater, parts of the Monterosato Collec¬
tion were acquired in 1889 and the Draparnaud Collection
was purchased probably in 1815 (Vinarski and Eschner
2016). Georg von Frauenfeld, curator of the mollusc col¬
lection at the beginning of the 19* century, collected and
described many new species (Eschner 2008).

Materials and methods

This work fulfils the efforts carried out by museum cura¬
torial staff and external researchers to segregate, label and
properly store Sturany’s type material. Type series of spe¬
cies described by Sturany were retrieved from the main
collection. Only for one species, Stylifer thielei, no type
material is available, because the only collected specimen
was broken by J. Thiele of the Museum of Berlin to study
the soft parts (Sturany 1903). We identified the syntypes
best matching the original description but refrained from
any lectotype designation following recommendation
74G of the International Code of Zoological Nomencla¬
ture.

For each species, we provide references to the original
description and figure, and indicate the original localities,
a list of the type and additional (i.e., collected during the
“Pola” expedition but not explicitly mentioned in Sturany’s
original descriptions) material, the original description and
its translation into English. All inventory numbers provided
refer to the Mollusca collection of NHMW. Earlier attempts
to update the taxonomy of Sturany’s species have been un¬
dertaken by Dekker and Orlin (2000) and Janssen in Janssen
and Taviani (2015). Specialist taxonomists helped us with
notes on the validity of the species and other comments (D.
Geiger for Fissurellidae, D. Herbert for Chilodontidae and
Trochidae, A. Waren for Eulimidae, A. Kohn for Conidae
S.S., A. Bonfitto for Turridae and allied families). The sys¬
tematic arrangement follows Bouchet and Rocroi (2005)
for most families and Bouchet et al. (2011) for Conoidea.

Photos were mostly shot with a Nikon SMZ25 mi¬
croscope; large shells were photographed with a Canon
350D camera, a 50 mm lens and extension tubes. SEM
images were taken with a JEOE JSM-6610EV, using low
vacuum without coating. Specimen measurements have
been added if substantially dissimilar from those reported
in the original description or missing.

The material studied by Sturany comes from off-shore
“stations” (Table 1) and coastal “localities” (Table 2); we
stuck to this terminology. In the two tables, we report the
collecting sites with their original orthography in German
and a modern name among square brackets. The coordi¬
nates are those provided by Sturany. Type localities were
established based on the information provided by Stura¬
ny. In case the type series came from several stations or

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Zoosyst. Evol. 93 (1) 2017, 45-94

Table 1. Olf-shore stations of the “Pola” expedition (from Sturany 1903).

Station

number

Locality

Coordinates

Depth

[m]

“unweit Suez” [near Suez, Egypt]

29° 37'N, 32° 29'E

-48

“sudlich von Yenbo” [south of Yanbu’ al Bahr, Saudi Arabia]

23° 2rN, 37° 37'E

-791

“nachst den St. Johns-lnsein” [cose to St. John’s Island, Egypt]

23° 20'N, 36° 20'E

-780

“vor Jidda” [off Jeddah, Saudi Arabia]

21° 36'N, 38° 33'E

-902

“bei Yenbo” [Yanbu’ al Bahr, Saudi Arabia]

23° 4rN, 38° 9'E

-610

“vor Yenbo” [off Yanbu’ al Bahr, Saudi Arabia]

24° 5'N, 37° 45'E

-700

“bei Sherm Sheikh” [near Abu Ghusun, Egypt]

24° 15'N, 35° 37'E

-562

[Red Sea]

24° 48'N, 35° 25'E

-535

“sudlich der Insel Senafir” [south of Sanafir Island]

27° 43'N, 34° 47'E

-900

“nachst der Noman-lnsel” [Noman Island, Saudi Arabia]

26° 53'N, 35° 17'E

-740

“unweit von Ras Abu Massahrib, Noman Insel” [close to Ras Abu Massahrib, Noman
Island, Saudi Arabia]

26° 34'N, 35° 33'E

-825

“bei Ras Mallap im Golfe von Suez” [Ra’s Mal’ab in the Gulf of Suez, Egypt]

29° 7.6'N, 32° 56'E

-50

“bei Tor im Golfe von Suez” [El Tor, Egypte]

28° 9.3'N, 33° 35.5'E

-38

“bei Nawibi im Golfe von Akabah” [Nuweiba, Gulf of Aqaba, Egypt]

29° 7.5'N, 34° 49.5'E

-920

“bei Nawibi im Golfe von Akabah” [Nuweiba, Gulf of Aqaba, Egypt]

28° 58.6'N, 34° 43.7'E

-314

“nordlicher Theil des Golfes von Akabah” [northern part of the Gulf of Aqaba]

29° 13.5'N, 34° 47.8'E

-350

107

“sudlich von Jidda” [south of Jeddah, Saudi Arabia]

21° 19'N, 38° 5rE

-748

109

“westiich von Jidda” [Jeddah, Saudi Arabia]

21° 19'N, 37° 39'E

-890

114

“zwischen Suakim und Lith” [between Suakin, Sudan, and Al Lith, Saudi Arabia]

19° 38'N, 37° 55'E

-535

117

“sudlich von Raveya” [south of Raveya, Sudan]

20° 16.9'N, 37° 33.5'E

-638

121

“westiich von Kunfidah” [west of Al Qunfudhah, Saudi Arabia]

18° 51.9'N, 39° 5.4'E

-690

124

“bei Lith” [Al Lith, Saudi Arabia]

19° 57.3'N, 39° 29.2'E

-430

127

“sudbstlich von Akik Seghir” [South-east of Akik Seghir Eritrea]

17° 42.2'N, 39° 42.3'E

-341

128

“bei Akik Seghir” [Akik Seghir, Eritrea]

18° 7.7'N, 39° 11.2'E

-457

130

“westiich von Kunfidah” [west of Al Qunfudhah, Saudi Arabia]

19° 17'N, 39° 37'E

-439

135

“sudostlich von Akik Seghir” [south-east of Akik Seghir, Eritrea]

17° 26.rN, 39° 19'E

-332

138

“bstlich von Akik Seghir” [east of Akik Seghir, Eritrea]

18° 3'N, 40° 14.7'E

-1308

143

“nachst der Insel Harmil” [near Harmil Island, Dahlak Archipelago, Eritrea]

17° 7'N, 39° 55'E

-212

145

“ostlich von J. Dahalak” [east of Dahlak Island, Eritrea]

16° 2.6'N, 41° 13.5'E

-800

156

“nordlich von Jidda” [north of Jeddah, Saudi Arabia]

22° 5rN, 38° 2'E

-712

165

“nachst der Insel Senafir” [near Sanafir Island]

27° 37.4'N, 35° 3.6'E

-780

170

“bei der Insel Noman” [Noman Island, Saudi Arabia]

27° 0.2'N, 35° 17.6'E

-690

175

“bei Koseir” [El Quseir, Egypt]

26° 4'N, 34° 30'E

-690

176

“bei Koseir” [El Quseir, Egypt]

25° 57'N, 34° 36.rE

-612

177

“bei Koseir” [El Quseir, Egypt]

26° 14'N, 34° 22.4'E

-676

178

“bei Koseir” [El Quseir, Egypt]

26° 19'N, 34° 24.5'E

-720

179

“bei Koseir” [El Quseir, Egypt]

26° 34.5'N, 34° 14.7'E

-490

184

“nachst den Brothers-lnseIn” [near Brother Islands, northern Red Sea]

26° 34'N, 35° 25.5'E

-876

localities, we stated as type locality the smaller geograph¬
ical area that encompasses all collecting sites.

A taxon list in alphabetical order with the page number
of this paper is provided in Table 3.

Systematic list of taxa

Family Fissurellidae Fleming, 1822
Emarginula harmilensis Sturany, 1903

Figure 1

Sturany, 1903: 235, plate V, figures 12a-b.

Type locality. Station 143, “nachst der Insel Harmil”
[near Harmil Island, Dahlak Archipelago, Eritrea]
17°7'N, 39°55'E, 212 m.

Type material. Holotype: NHMW 84290, length 6.8 mm.

Original description. Von der Station 143 (212 m); 1
Exemplar.

Die Schale ist 7 V 2 mm lang, 4 mm hoch, 5 V 4 mm breit.
Der stark nach ruckwdrts und etwas nach unten gekehrte
Apex fdllt fast mit dem Hinterende der Schale zusammen:
die absolute Distanz des Wirbelendes zum Schalenende
betrdgt 2 mm, die relative (bei Projection derselben zur
Basis) nur V 2 mm. Die schmutzigweifie bis gelbe Grund-
farbe des Gehduses erhdlt durch radiar angeordnete
Fleckchen, Linien und Punkte von brauner bis grunlicher
Farbe ein gesprenkeltes Aussehen. Milchweijl gefdrbt
sind die zahlreichen Hauptradiarrippen, zwischen denen
zartere Rippen liegen, die mitunter dunkler erscheinen
(zwischen je 2 Hauptrippen liegt eine Nebenrippe). Die

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Table 2. Coastal localities of the “Pola” expedition (from Sturany (1903)).

Locality number

Locality

Coordinates/Region

“Ismalia am Timsah-See” [Timsah Lake, Ismailia, Egypt]

Suez Canal

“Bittersee” [Great Bitter Lake, Egypt]

Suez Canal

“Suez” [Suez, Egypt]

Gulf of Suez

“Zafarana” [Zaafarana, Egypt]

Gulf of Suez

“Ras Mallap” [Ra’s Mal’ab, Egypt]

Gulf of Suez

“Ras Abu Zenima (Zenihme)” [Abu Zenima, Egypt]

Gulf of Suez

“Ras Gharib” [Ras Ghareb, Egypt]

Gulf of Suez

“Tor” [El Tor, Egypt]

Gulf of Suez

“Akabah” [Aqaba, Jordan]

Gulf of Aqaba

“Nawibi” [Nuweiba, Egypt]

Gulf of Aqaba

“Bir al Mashiya” [Bir al Mashiya, Saudi Arabia]

Gulf of Aqaba

“Dahab (Mersa Dahab)” [Dahab, Egypt]

Gulf of Aqaba

“Senafir-lnsel” [Sanafir Island, Strait of Tiran]

Northern Red Sea, 28° - 26°N

“Sherm Sheik” [Sharm El-Sheikh, Egypt]

Northern Red Sea, 28° - 26°N

“Ras Muhammed” [Ras Mohammed, Egypt]

Northern Red Sea, 28° - 26°N

“Shadwan-lnsel” [Jazirat Shakir, Egypt]

Northern Red Sea, 28° - 26°N

“Noman-lnsel (Ras Abu Massahrib)” [Ras Abu Massahrib, Noman Island, Saudi Arabia]

Northern Red Sea, 28° - 26°N

“Ras Abu Somer” [Ra’s Abu Sawmah, Egypt]

Northern Red Sea, 28° - 26°N

“Brothers-lnsel” [Brother Islands, Egypt]

Northern Red Sea, 28° - 26°N

“Sherm Habban (Abban)” [Sharm Habban, Saudi Arabia]

Northern Red Sea, 28° - 26°N

Koseir [El Quseir, Egypt]

Northern Red Sea, 28° - 26°N

“Mersa Dhiba” [Mersa Dhiba, Egypt]

26°-24°N

“Dadalus Riff” [Daedalus Reef, Red Sea]

26°-24°N

“Hassani-lnsel” [Al Hasani, Saudi Arabia]

26°-24°N

“Sherm Sheikh (Mersa Sheikh)” [near Abu Ghusun, Egypt]

26°-24°N

“Yenbo (Jembo)” [Yanbu’ al Bahr, Saudi Arabia]

26°-24°N

“Port Berenice” [Berenice Troglodytica, Egypt]

24°-22°N

“St. Johns-lnsel” [St. John’s Island, Egypt]

24°- 22°N

“Sherm Rabegh” [Rabigh, Saudi Arabia]

24°- 22°N

“Mersa Halaib” [Halayeb, Egypt]

24°- 22°N

“Jidda (Djeddah)” [Jeddah, Saudi Arabia]

22°- 20°N

“Raveiya (Mahommed Ghul)” [Gul Mohammad, Saudi Arabia]

22°- 20°N

“Lith” [Al Lith, Saudi Arabia]

22°- 20°N

“Sawakin (Suakim)” [Suakin, Sudan]

20° - 18°N

“Kunfidah (Kunfuda)” [Al Qunfudhah, Saudi Arabia]

20° - 18°N

“Akik Seghir” [Eritrea]

20° - 18°N

“Ras Turfa” [near Jazan, Saudi Arabia]

18° - 16°N

“Sarso-lnsel” [Sarso Island, Saudi Arabia]

18° - 16°N

“Harmil-lnsel” [Harmil Island, Dahlak Archipelago, Eritrea]

18° - 16°N

“Kadhu-lnsel” [Kad-Hu, Dahlak Archipelago, Eritrea]

18° - 16°N

“Massawa (Massaua)” [Massawa, Eritrea]

16°- 11°N

“Dahalak-lnsel, resp. Nakhra Khor Island” [Nakhra Khor, Dahlak Archipelago, Eritrea]

16°- 11°N

“Kamaran-lnsel” [Kamaran Island, Yemen]

16°- 11°N

“Zebayir-lnsel (Zebejir)” [Jabal Zubayr, Yemen]

16°- 11°N

“Ghuleifaka (= Landzunge Ras Mujamela)” [Ras Mujamila, Yemen]

16°- 11°N

“Hanfela-lnsel” [island in the Bay of Anfile, Eritrea]

16°- 11°N

“Jebel Zukur-lnsel (Djebel Zukur)” [Jazirat Jabal Zuqar, Yemen]

16°- 11°N

“Abayil-lnsel” [Sel Abayil Deset, Eritrea]

16°- 11°N

“Asab” [Assab, Eritrea]

From 14°N until the end of the
Bab al-Mandab Strait

“Perim-lnsel” [Perim Island, Yemen]

From 14°N until the end of the
Bab al-Mandab Strait

erwdhnten Rippen werden von vielen zarten Querlini-
en gekreuzt, an den Kreuzungsstellen der Hauptrippen
sind perlenfdrmige Verdickungen ausgebildet. Der Ein-
schnitt der Schale ist etwas Idnger als 3 mm: die Rander
derselben sind gerade und innen mit einem verdickten
Belage versehen, der sich in Form einer immer starker

werdenden weifien Schwiele bis in die Wirbelgegendfort-
setzt. Die Rinne zwischen der Wirbelhdhe und dem blin-
den Ende des Einschnittes ist stark vertieft, weifi gefdrbt
und quer gestreift.

Die neue Art ist mit E. bellula A. Ad. von den Philip-
pinen verwandt.

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Table 3. List of treated taxa in alphabetical order, with original
name, current family placement, and figure in this paper.

Taxon

Family

Page, Figure

batheon, Conus planiliratus var.

Conidae

Page 82, Figure 27

beblammena, IPIeurotoma

Raphitomidae

Page 85, Figure 28

bifrons, Fusus

Fasciolariidae

Page 60, Figure 11

camaranensis, Capulus

Hipponicidae

Page 53, Figure 4

dichroma, Clathurella

Raphitomidae

Page 86, Figure 29

epicharis, Mangelia
(Glyphostoma)

Raphitomidae

Page 88, Figure 30

erythraeensis, Columbeiia
(Mitreiia)

Coiumbeiiidae

Page 57, Figure 9

erythraeensis, Eucheius

Chiiodontidae

Page 49, Figure 2

gonatophora, Mitra (IThaia)

Mitridae

Page 73, Figure 19

haiaibensis, Eiusa

Pyramideiiidae

Page 90, Figure 31

harmiiensis, Emarginuia

Fissureiiidae

Page 47, Figure 1

iiiustris, Soiarieiia

Trochidae

Page 51, Figure 3

inchoata, Pieurotoma (IDriliia)

Driiiiidae

Page 77, Figure 22

iathraia, Nassa

Nassariidae

Page 62, Figure 12

lithensis, Atys (Roxania)

Fiaminoeidae

Page 91, Figure 33

minor, Mitra tenuis f.

Mitridae

Page 73, Figure 20

mueiieriae, Euiima

Euiimidae

Page 53, Figure 5

munda, Nassa

Nassariidae

Page 64, Figure 13

nana, Nassa thaumasia var.

Nassariidae

Page 69, Figure 17

nannodes, Pieurotoma (Surcuia)

Horaiciavidae

Page 79, Figure 24

nomanensis, Coiumbeiia
(Mitreiia)

Coiumbeiiidae

Page 59, Figure 10

orthophyes, Euiima

Euiimidae

Page 55, Figure 6

paucicostata, Eusus bifrons f.

Fascioiariidae

Page 62, Figure 11

pertabuiata, Mangeiia

Ciathureiiidae

Page 79, Figure 25

potti, Pieurotoma (Driiiia)

Driiiiidae

Page 75, Figure 21

senafirensis, Triforis (? Virioia)

Triphoridae

Page 57, Figure 8

siebenrocki, Pieurotoma (Ciavus)

Driiiiidae

Page 78, Figure 23

sporadica, Nassa

Nassariidae

Page 65, Figure 14

steindachneri, Nassa

Nassariidae

Page 66, Figure 15

stiphra, Nassa

Nassariidae

Page 68, Figure 16

thaumasia, Nassa

Nassariidae

Page 68, Figure 17

thieiei, Stylifer

Euiimidae

Page 56, Figure 7

torensis. Conus acuieiformis f.

Conidae

Page 81, Figure 26

trivittata, Syrnola

Pyramideiiidae

Page 91, Figure 32

xesta, Nassa

Nassariidae

Page 69, Figure 18

Translation. From station 143 (212 m); one specimen.

The shell is 7.5 mm long, 4 mm high, 5.25 mm wide.
Apex positioned strongly backward and downward al¬
most coinciding with the end of the shell: the absolute
distance from the apex to the shell margin is 2 mm, the
distance between the apex projection on the base and the
posterior margin is only 0.5 mm. The whitish to yellow
background shell colour has a spotted appearance be¬
cause of the radially arranged blotches, lines and dots
of brown to greenish colour. The numerous main radial
ribs are milky white, whereas the finer ribs in between
are darker (between two main ribs there is one finer rib).
The ribs are crossed by many delicate transverse lines,
the intersections form pearl-shaped tubercles. The slit is
slightly longer than 3 mm: its edges are straight show¬
ing internally a thickened coating, continuing as white
callus in the spire. The groove between the apex and the

slit [anal fasciole] is very deep, white and transversely
ribbed.

The new species is related to E. bellula A. Adams from
the Philippines.

Comments, [text by D. Geiger] The species is clearly a
member of Emarginula given the overall shell outline, the
height of the shell as well as the slit with parallel margins.
It is not a juvenile Fissurellinae or Diodorinae, because at
the size of Sturany’s specimen a hole would have formed.
Note that some juvenile Diodora have been described as
distinct species, such as Puncturella piccirida Palazzi &
Villari, 2001 from the Mediterranean. However it lacks
the distinctive internal septum of Puncturella.

Sturany’s E. harmilensis is characterized by a rather
uncommon color pattern of tan spiral bands. Those are
also found in E. costulata Deshayes, 1863, described
from Reunion Island. Herbert (1987: figs 39-40) illustrat¬
ed the by him designated lectotype, and a more typical,
fully-grown specimen (figs 41^2), and discussed previ¬
ous misidentifications of the species as E. tenuicostata
Adams & Sowerby, 1863. The shared characters include
overall shape, placement of the spire, length of the slit,
color pattern, and number and strength of the ribs. Many
species found along the coast of East Africa are also en¬
countered in the Red Sea. Accordingly, E. harmilensis
Sturany, 1903 is a junior synonym of E. costulata Desh¬
ayes, 1963.

Family Chilodontidae Wenz, 1938
Euchelus erythraeensis Sturany, 1903

Figure 2

Sturany, 1903: 266, plate V, figure 6.

Type locality. Locality 10 “Nawibi” [Nuweiba, Gulf of
Aqaba, Egypt].

Additional original localities. Locality 25 (Northern
Red Sea) (Table 2).

Type material. Lectotype: NHMW 37964 (station not
specified, but likely locality 10, height 6.6 mm), designat¬
ed by D.G. Herbert (1996), illustrated by Sturany (1903)
in plate V, figure 6. Further two paralectotypes NHMW
37963 (locality 25).

Original description. Von den Localitdten 10 und 25.

Das abgebildete Exemplar stammt von Nawibi und
weist die folgenden Dimensionen auf: Hohe der Schale
6,5 mm, Breite derselben 6 mm Hohe (Lange) der Mund-
ung 3,6, Breite derselben 2,5 mm. Von den 6 Umgdngen
sind blofi die beiden ersten frei von einer Sculptur auf
dem 3. Umgange sind bereits 3 Spiralrippen, auf dem 5.
deren 4 bis 5 zu sehen. Diese Spiralrippen, nicht gleich
in der Starke, sondern meist etwas variabel, tragen zahl-
reiche Knoten von weifier oder gelbbrauner Farbe. Die
Grundfarbe des Gehduses ist weifi, Flecken von gelb¬
brauner Oder olivengruner Farbe finden sich ohne Re-

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 1. Emarginula harmilensis Sturany, 1903, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea, Red Sea). A-F, H. Holo-
type, NHMW 84290: top (A-B), aperture (C), left side (D-E), protoconch (F), microsculpture (H). G. Original figure by Sturany
(1903). Scale bars; A-E: 1 mm, F; 0.1 mm, H; 0.5 mm.

gelmdfiigkeit und hdufig in Zickzacklinien quer iXber die
letzten Umgdnge vertheilt. Die Basis der Schale trdgt
zwischen der Peripherie und dem perspectivischen Na-
bel 7 concentrische Knotenreihen von gemischter Farbe.
Mit E. foveolatus A. Ad. ist diese Form nahe verwandt.

Translation. From localities 10 and 25.

The figured specimen is from Nawibi and has the fol¬
lowing dimensions: height of the shell 6.5 mm, width 6

mm, height (length) of the mouth 3.6, width 2.5 mm. Of
the six whorls, the first two lack a sculpture. On the third
whorl, three spiral ribs are visible; on the fifth whorl, four
to five ribs. These spiral ribs are not of equal size and
carry numerous white or yellow-brown tubercles. The
background colour of the shell is white; patches of yel¬
low-brown or olive green colour can be found without
regularity and often distributed in zigzag lines across the
last whorls. The base of the shell shows seven concentric

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Zoosyst. Evol. 93 (1) 2017, 45-94

Figure 2. Euchelus erythraeensis Sturany, 1903, Locality 10 (Nawibi, Gulf of Aqaba, Red Sea). A-F, I. Lectotype, NHMW 37964;
front (A-B), right side (C), top (D), back (E), bottom (F), protoconch (I). G. Original lectotype label. H. Original figure by Sturany
(1903). Scale bars; A-F; 2 mm, I; 0.2 mm.

series of tubercles of mixed colour between the periphery
and the umbilicus.

Form closely related to E.foveolatus A. Adams.

Comments. This name is considered a junior synonym of
Clanculus tonnerrei (G. Nevill & H. Nevill, 1874) (Her¬
bert 1996).

Family Trochidae Rafinesque, 1815
Solariella illustris Sturany, 1900

Figure 3

Sturany, 1900b: 211-212; redescribed and illustrated in Sturany (1903),
page 234, plate I, figures 7a-c.

Original localities. Station 48 (700 m) and Station 143
(212 m) (Central and Southern Red Sea; Table 1).

Type material. Two syntypes: NHMW 84287 (station
48), the specimen figured by Sturany (1903), plate I,
figure 7a-c has been segregated, its diameter is 8.3 mm.
Further seven syntypes NHMW 84288 (station 48).

Original description. Gehduse ziemlich festschalig,
breit kegelig, weit und perspectivisch genabelt, oben
weifiUch mit unregelmdfiig vertheilten, gelben Flecken
und irisierend. Unten milchweifi mit glasig durchschei-
nenden Querstreifen (die allerdings nur bei frischen

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 3. Solariella illustris Sturany, 1900, Station 48 (Yanbu’ al Bahr, Saudi Arabia, Red Sea). A-D, F-G. Figured syntype,
NHMW 84287; front (A), right side (B), back (C), top (D), bottom (F), apex (G). E. Original figure by Sturany (1903). Scale bars:
A-D, F: 2 mm, G: 0.2 mm.

Stucken sichtbar sind und damn einen stark irisierenden
Glanz besitzen), mit brauner Einfassung des Nabels.
Von den mdfiig gewolbten 6-7 Windungen ist der Apex
(1-1 1/2 Umgdnge) glatt, gelb oder mitunter rosig an-
gehaucht; auf der folgenden Windung beginnt ein Mit-
telkiel, der sich bis zur Mundung verfolgen lasst, dort
jedoch schon uber die Mitte geriickt ist und welcher mit¬
unter auf der vorletzten Windung von einem ganz nahe
darunter entspringenden Kiel begleitet und schliefilich an
Starke ubertrojfen wird. Auf den Schlusswindungen steht
ndchst derNaht eine Spiralreihe von Hockerchen, welche
sich vor der Mundung wieder abschwdchen, ferner ist die
letzte Windung noch durch einige Spiralrippen oben und
zahlreiche concentrische Spiralfurchen auf der Unter-
seite ausgezeichnet. Uberall, und zwar am deutlichsten
auf den ndchst der Naht gelegenen Umgangspartien sind
auch Anwachsstreifen in Form von Querriefen sichtbar.
Der Nabel betrdgt 1/3 der Gehdusebreite und wird von
einigen Reihen dicht stehender, durch zahlreiche Quer-
einschnitte regelmdfiig gegitterter oder geperlter Rippen

umstellt, die sich tief hinein verfolgen lassen. Die oben
vorgezogen Mundung ist innen perlmutterglanzend: der
Deckel hdutig, mit einigen concentrischen Ringen.

Grofier Durchmesser der Schale 7,4 - 9,1, kleiner
Durchmesser 6,1 - 8,0 mm, Hohe 4,7 - 6,4, respective
3,6 - 5,0; Langendurchmesser der Mundung 3,5 - 4,1,
Breite derselben 2,9 - 3,6 mm.

Die neueArt liegt von Station 48 (700 m) in leeren Ge-
hdusen, von Station 143 (212 m) sammt dem Thiere vor.

Translation. Fairly thick shell, broadly conical, with a
wide and deep umbilicus, on top whitish with irregular
yellow spots and iridescence. The bottom is milky white
with glassy translucent horizontal stripes (these are only
visible in fresh specimens and have a strong iridescent
lustre), the umbilicus rim is brown. Of the moderately
convex six to seven whorls, the apex (1-1.5 whorls) is
smooth, yellow or pink coloured sometimes; on the next
whorl, a keel in the middle of the whorl starts and can be
followed down to the aperture, but here it is positioned

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above the centre and it is sometimes accompanied on
the penultimate whorl by a keel, which arises very close
below it and is finally stronger. On the final whorls, a
spiral row of tubercles develops next to the suture, and
is less strong close to the mouth, furthermore the last
whorl is characterized by several spiral lines on top and
numerous concentric spiral grooves on bottom. Every¬
where, but especially close to the suture, transversal
growth lines are visible. The umbilicus is one third of
the shell width and is surrounded by a few dense se¬
ries of transversal incisions crossed by tubercled ribs,
which continue deep inside it. Mouth elongated above,
inside nacreous: the operculum is membranaceus, with
concentric grooves.

Larger shell diameter 7.4 to 9.1, smaller diameter 6.1
to 8.0 mm, height 4.7 to 6.4, respectively 3.6 -5.0; the
mouth is 3.5 to 4.1 high, and 2.9 to 3.6 mm wide.

The new species was collected as empty shells at sta¬
tion 48 (700 m), while empty shells were collected at sta¬
tion 143 (212 m).

Comments. Solariella illustris is closely related to
Ethminolia nektonica (Okutani, 1961) (Herbert 1992).
Dekker and Orlin (2000: 18) and Janssen in Janssen and
Taviani (2015: 525) assigned this species to Ilanga.

Family Hipponicidae Troschel, 1861
Capulus camaranensis Sturany, 1903

Figure 4

Sturany, 1903: 256-257, plate VII, figures lla-c.

Original locality: Locality 43, “Kamaran-Insel” [Kama-
ran Island, Yemen], 16°- 11°N.

Type material. Ten syntypes: NHMW 37797 (locality
43), the specimen figured by Sturany (1903), plate I, fig¬
ure 1 la-c has been segregated, its width is 8.4 mm.

Original description. Die erwachsene Schale be-
steht im ganzen aus 3 Umgdngen; die ersten 2 glas-
hellen Windungen bilden einen aufwdrts gerichteten
Apex, der jedoch nicht immer deutlich erkennbar ist,
die letzte Windung den Haupttheil des Gehduses. Die
grofie querovale Mundung ist unten vorgezogen und
hat einen breiten, verdickten Spindelrand. Die weifie
Grundfarbe der Schale wird von mehreren verschieden
breiten Langs- oder Spiralbandern von gelbbraunem
bis orangefarbigem Ton verdrangt. An der Unterseite
der Schlusswindung und gegen den Mundrand zu treten
bei diesen Binden hdufig Verschmelzungen zu Flecken-
partien auf.

Junge Schalen sind einfarbig weifi und haben die Ge¬
stalt von C. hungaricus; die Mundung ist kreisrund, der
aufwdrts gekehrte Apex steht noch ndher zum Spindel-
rande, erst mit dem Anwachsen der Schale werden sie
voneinander durch einen weiteren Raum getrennt.

Die Art wurde von der Localitdt 43 (Kamaran-Insel)
gebracht, und zwar sitzen die meisten.

Exemplare auf Stacheln von Goniocidaris canaliculata
A. Ag. Einige junge Schalen haben sich auf alter en Exem-
plaren derselben Art angesetzt. Das Ansetzen geschieht
unter Ausbildung eines festen, dicken, kalkigen Basal-
stuckes, das genau in die Mundung der Schale passt und
2 neben einander liegende, annahernd ovale Flecken als
Muskelabdrucke erkennen Idsst.

Translation. The adult shell consists of three whorls; the
first two glassy whorls form an antrorse apex that is not
always clearly recognizable, the last whorl is the main
part of the shell. The large transversely oval mouth is
elongated at the bottom and has a broad, thickened col-
umellar lip. The white background colour of the shell is
replaced by several different wide longitudinal or spiral
yellow-brown to orange bands. On the basal part of the
last whorl and towards the lip these bands frequently
merge into dotted areas.

Young shells are plain white and have the shape of C.
hungaricus, the aperture is circular, the antrorse apex is
very close to the columellar lip; only with shell growth,
they get separated by more space.

The species was brought from the locality 43 (Kama-
ran Island), sitting usually on spines of Goniocidaris can¬
aliculata A. Ag. Some young shells are attached to older
specimens of the same species. They adhere by forming a
solid, thick, chalky base fitting precisely into the aperture
and revealing two adjacent, almost oval dots from muscle
imprints.

Comments. The identification of the echinoderm Gonio¬
cidaris canaliculata A. Agassiz, 1863 cannot be verified
based on the available material (Figure 4 F). Capulus
camaranensis was considered a synonym of Malluvium
lissum (E. A. Smith, 1894) in the family Hipponicidae by
Dekker and Orlin (2000: 21).

Family Eulimidae Philippi, 1853
Eulima muelleriae Sturany, 1903

Figure 5

Sturany, 1903: 258, plate VI, figure 10.

Type locality. Locality 31, “Jidda (Djeddah)” [Jeddah,
Saudi Arabia] 22°- 20°N.

Type material. Holotype: NHMW 37809, height 3.1 mm.

Original description. Von der Localitdt 31.

Die neue Art griindet sich auf ein einziges in Miilleria
mauritiana Q. & G. gefundenes Exemplar (Dr. v. Maren-
zeller hat die Schale bei der Bestimmung jener Holothu-
rie entdeckt). Sie ist nahe verwandt mit E. modicella A.
Ad. von Japan und den Philippinen, von ihr jedoch in
einigen Punkten verschieden. Das Gehduse ist stark nach
rechts geneigt (mithin links concav, rechts oben convex
gebaut) und besteht aus etwa 11 allmdhlich anwachsend-
en Umgdngen; die Hdhe der Schale betrdgt 3,4, die Brei-
te 1,2, die Hdhe der Mundung circa 1 mm.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 4. Capulus camaranensis Sturany, 1903, Locality 43 (Kamaran Island, Yemen, Red Sea). A-E. Figured syntype, NHMW
37797: left side (A-B), protoconch (C), aperture (D), top (E). F. Post-metamorphic stage attached to Goniocidaris canaliculata (A.
Agassiz, 1863). G. Original figure by Sturany (1903). H. Original label. Scale bars; A-B, D-F: 1 mm, C: 0.2 mm.

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Figure 5. Eulima muelleriae Sturany, 1903, Locality 31 (Jeddah, Saudi Arabia, Red Sea). A-E, G. Holotype, NHMW 37809; front
(A-B), right side (C-D), back (E), protoconch (G). F. Original figure by Sturany (1903). H. Original holotype label. Scale bars:
A-E: 0.5 mm, G; 0.1 mm.

Translation. From locality 31.

The new species is based on a single specimen found
on Mulleria mauritiana Quoy & Gaimard [Echinoder-
mata, Holothuriidae] (the shell was discovered by Dr.
von Marenzeller when identifying this holothurian). It
is closely related to E. modicella A. Adams from Japan
and the Philippines, but differs in some respects. The
shell is strongly bent to the right (therefore concave
on left side, convex on top right side [it looks like a
mistake because the opposite is true]) and consists of
about 11 gradually increasing whorls; the height of the
shell is 3.4, the width of 1.2, the height of the aperture
about 1 mm.

Comments. Waren (1984) placed this species in Mela-
nella and provided photos of living specimens and of sec¬
tions of the snail in situ on the host.

Eulima orthophyes Stnrany, 1903

Figure 6

Sturany, 1903; 258, plate VI, figure 8.

Type locality. Locality 32, “Raveiya (Mahommed Ghul)”
[Gul Mohammad, Saudi Arabia] 22°- 20°N.

Type material. Holotype: NHMW 37810, height 7 mm.

Original description. Von der Localitdt 32; ein einziges
Exemplar.

Die glatte, stark glanzende, weifi gefdrbte Schale ist
nahezu gerade gewachsen, der Apex ist nur minimal
nach rechts geneigt. Es sind 11 Umgdnge vorhanden,
die durch eine fadenformige Naht voneinander getrennt
werden; das Ausmafi der Schale betrdgt 7,4 : 2,6 mm, die
Milndung ist ungefdhr 2 V 2 mm hock

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 6. Eulima orthophyes Sturany, 1903, Locality 32 (Gul Mohammad, Saudi Arabia, Red Sea). A-E, G. Holotype, NHMW
37810: front (A-B), right side (C-D), back (E), protoconch (G). F. Original figure by Sturany (1903). H. Original holotype label.
Scale bars: A-E: 1 mm, G: 0.1 mm.

Der Gestalt nach hat die neue Art eine gewisse
Ahnlichkeit mit Sty lifer acicula Gld., im Gehduseaufbau
auchmitE. solidula^r/. u. Rve. von den Sandwich-Inseln
(Berliner Museum!).

Translation. From locality 32; a single specimen.

The smooth, very shiny, white-coloured shell is almost
straight; the apex is minimally inclined to the right. There
are 11 whorls, which are separated by a filiform suture;
the size of the shell is 7.4 mm high and 2.6 mm wide, the
mouth is about 2.5 mm high.

The form of the new species resembles Stylifer acicula
Gould, the shell shape is similar to E. solidula Adams and
Reeve from the Sandwich Islands (Berlin Museum).

Stylifer thielei Stnrany, 1903

Figure 7

Sturany, 1903: 258, with text figure.

Type locality. Locality 31, “Jidda (Djeddah)” [Jeddah,
Saudi Arabia] 22°- 20°N.

Type material. Destroyed.

Original description. Von der Localitdt 31; ein einziges
Exemplar.

Die merkwurdig gestaltete und insbesondere auch
durch den geschweiften Mundrand ausgezeichnete Schale
ist aus 5 Umgdngen aufgebaut und besitzt einen zitzen-

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Figure 7. Original figure of Stylifer thielei Sturany, 1903.

formigen Apex. Sie entbehrt jedweder Sculptur, ist matt
im Gldnze und weifi der Farbe nach. Hohe der Schale
5 V 2 , Breite 3 V 2 mm. Herr Prof. Dr. Johannes Thiele in
Berlin war so freundlich, die Weichtheile dieser Schnecke
zu untersuchen und vor der nothwendig gewordenen Zer-
triimmerung der Schale die beigegebenen Zeichnungen
anzufertigen. Zufolge des Fehlens einer Radula gehort
das Thier zur Gattung Stylifer Brod.

Translation. From the locality 31; a single specimen.

The remarkably shaped shell is characterized by the
curly lip, it consists of five whorls and has a teat-shaped
apex. It lacks any sculpture, is dull in lustre and white
in colour. Height of shell 5.5, width 3.5 mm. Prof. Dr.
Johannes Thiele in Berlin was so kind to examine the
soft parts of the snail and to prepare the drawings before
crushing the shell. According to the lack of a radula the
animal belongs to the genus Stylifer Broderip.

Comments. Sturany found a single specimen and sent it to
Johannes Thiele in Berlin for the study of the soft parts (Stu¬
rany 1903). The shell was reported to have been crushed
to extract the animal, indeed no shells were found in the
Vienna and the Berlin museums (C. Zom, pers. comm.).
Waren (1981) placed it in the genus Stylapex and provided
further figures of the shell and of living individuals. In any
case, Stilifer is the correct spelling of the genus, Stylifer
being an incorrect subsequent spelling by Broderip (1832).

Family Triphoridae Gray, 1847

Triforis (fViriola) senafirensis Sturany, 1903

Figure 8

Sturany, 1903: 262-263, plate V, figures 7a-b.

Type locality. Locality 13, “Senafir-Insel” [Sanafir Is¬
land, Strait of Than], Northern Red Sea, 28°- 26°N.

Type material. Holotype: NHMW 37912, height 4.2 mm.

Original description. Von der Localitdt 13; ein einziges
Exemplar. Das 5 mm hohe und FA mm breite Gehduse ist
zierlich gebaut und Idsst die Naht, welche einem zwischen
Spiralrippen laufenden Raum gleichkommt, schwer er-
kennen. Es bilden ungefdhr 5 feinsculptierte Umgdnge das

mutzenformig gestaltete, blasig aufgetriebene Embryonal-
gewinde, und darauf folgen die 9-10 Hauptumgdnge der
Schale. Auf jenem Embryonalgewinde werden zahlreiche
Querlinien von 2 spiral angeordneten Rippchen gekreuzt,
auf den ubrigen Schalenwindungen laufen zuerst 2, dann 3
Spiralrippen von milchweifier Farbe und flachgedriickter
Oberfldche, zwischen denen mikroskopisch feine Quer-
strichelchen erkennbar sind. Die Gesammtfarbe des Ge-
hduses ist dunkelrothbraun. Die Mundung ist entsprech-
end dem Gattungscharakter gestaltet und trdgt oben am
Aufienrande einen kleinenAusschnitt. Die Form ist dhnlich
der als T. hilaris Hinds, bekannten Art von Zebu (Berliner
Museum!) und dem Pacifischen Ocean (Tryon-Pilsbry).

Translation. From location 13; a single specimen. The 5
mm high and 1.5 mm wide shell is finely built and makes
the suture, which is similar to the space between spiral
cords, hard to see. About five finely sculpted whorls form
the cap-shaped inflated protoconch, then followed by the
nine to ten teleoconch whorls. On the protoconch numer¬
ous axial ribs cross two spiral keels; on the teleoconch
whorls, initially two, then three spiral milky-white flat
cords run, microscopically fine horizontal lines can be
seen between them. The main colour of the shell is dark
reddish brown. The aperture is typical of the genus and
carries on top of the outer lip of a small notch. The shape
is similar to T. hilaris Hinds known from Cebu (Berlin
Museum!) and the Pacific Ocean (Tryon-Pilsbry).

Comments. The holotype had originally a complete pro¬
toconch because Sturany described it as being formed by
five whorls. Now the apex is clearly broken and only two
whorls are left. Nonetheless, it can be seen that the apex
is multispiral.

Family Columbellidae Swainson, 1840
Columbella (Mitrella) erythraeensis Sturany, 1900

Figure 9

Sturany, 1900b: 208-209; redescribed and illustrated in Sturany (1903),
page 226, plate I, figure 5.

Type locality. Station 54, 24°48'N, 35°25'E, Central Red
Sea, 535 m.

Type material. Holotype: NHMW 84221, height 13.1 mm.

Original description. Schale spindelfdrmig, glanzend,
weifi, mit Spuren von gelber Netzzeichnung; von den 8
Umgdngen sind die ersten 2 milchweifi, glatt, zitzenfor-
mig, diefolgenden 11/2 mitziemlich entfernt voneinander
stehenden, deutlichen und derben Querrippchen ausges-
tattet, die ubrigen bis auf die fadenfbrmige Naht und eine
allerfeinste mikroskopische Spiralsculptur, sowie die mit
Spiralreifen umstellte Basis des letzten Umganges glatt.
MitAusnahme der Embryonalschale sind die Windungen
nahezu flach und ungefdhr stufig abgesetzt. Mundung mit
6 Zdhnchen am Aufienrande, mit einer Verdickung hinter
demselben und mit schwachen

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 8. Triforis senafirensis Sturany, 1903, Locality 13 (Sanafir Island, Strait of Tiran, Northern Red Sea). A-H. Holotype,
NHMW 37912: front (A-B), left side (C-D), back (E), protoconch (F, H), peristome (G). I. Original figure by Sturany (1903).
J. Original holotype label. Scale bars: A-E: 1 mm, F, H: 0.2 mm, G: 0.5 mm.

Hockerchen auf der Spindel.

Hohe des Gehduses 12,5 mm, Breite 4,0 mm, Hohe der
Mundung 5,5 mm. Bin einziges Exemplar von Station 54
(535 m).

Translation. Shell fusiform, shiny, white, with traces of
a yellow net pattern; of the eight whorls, the first two are
milky white, smooth, teat-shaped, the following one and
half has separated, pronounced and coarse axial ribs, the
others almost smooth with the exception of the thread¬
like suture, the fine microscopic spiral sculpture, and

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Figure 9. Columbella erythraeensis Sturany, 1900, Station 54 (Central Red Sea). A. Original figure by Sturany (1903). B-E. Holotype,
NHMW 84221; front (B), right side (C), back (D), protoconch (E). F. Original holotype label. Scale bars: B-D: 2 mm, E; 0.2 mm.

spiral rings at base of the last whorl. With exception of
the embryonic shell, the whorls are nearly flat and scalar.
Aperture with six teeth on the outer lip, with a fold and
weak tubercles on the columella.

Shell height 12.5 mm, width 4.0 mm, height of the
mouth 5.5 mm. One specimen from station 54 (535 m).

Comments. The species has a fine spiral sculpture which
is poorly visible in our figure.

Columbella (Mitrella) nomanensis Sturany, 1900

Figure 10

Sturany, 1900b; 209; redescribed and illustrated in Sturany (1903), page
226, plate I, figure 6.

Type locality. Station 170, “bei der Insel Noman” [No¬
man Island, Saudi Arabia] 27°0.2'N, 35°17.6'E, 690 m.

Type material. Holotype: NHMW 84222, height 7.2 mm.

Original description. Schale spindel-bis eiformig, matt
glanzend, mit Spuren von orangegelben Flecken auf

gelblich weifiem Grunde; von den 8 1/2 Umgdngen sind
die ersten 31/2 milchweifi und glatt, die ubrigen kaum
gewolbt und mit ziemlich dicht stehenden Spiralstreifen
ausgestattet, die an der Basis zu groberen Spiralrip-
pchen anwachsen.

Naht fadenformig. Am dufieren Mundungsrande sitzen
6 Zdhnchen, an der Spindel schwache undeutliche Hock-
erchen, Mundungscanal breit und abgestutzt, zuriickge-
bogen.

Hohe des Gehduses 8,0 mm, Breite 3,2 mm; Hohe der
Mundung 3,7 mm. Bin Exemplar von Station 170 (690 m).

Translation. Shell fusiform to ovoid, glossy, with trac¬
es of orange-yellow flammules on a yellowish-white
ground; of the eight and half whorls, the first three and
half are milky white and smooth, the others slightly
curved and with dense spiral striae that grow into coarse
spiral ridges at the base.

Suture Aliform. At the outer lip six teeth, on the colu¬
mella weak indistinct tubercles, siphonal canal wide and
truncate, curved.

Shell height 8.0 mm, width 3.2 mm; mouth height 3.7
mm. One specimen from station 170 (690 m).

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 10. Columbella nomanensis Sturany, 1900, Station 170 (Noman Island, Saudi Arabia, Red Sea). A-E, H-L Holotype,
NHMW 84222; front (A-B), right side (C-D), back (E), protoconch (H-I). F. Original figure by Sturany (1903). G. Original holo¬
type label. Scale bars; A-E; 1 mm, H; 0.2 mm, I; 0.1 mm.

Family Fasciolariidae Gray, 1853

Fusus bifrons Sturany, 1900

Figure llA-D, I-J

Sturany, 1900a: 197-198; redescribed and illustrated in Sturany (1903),
pages 220-221, plate I, figures 1 and 3.

Original localities. Stations 9, 20, 47, 48, 76, 81, 107,
109, 121, 145, 156, 165, 170, 175, 176, 178, 179, 184
(490 - 900 m) (Red Sea; Table 1). In the original descrip¬
tion Sturany did not refer to any particular station. There¬
fore, it is assumed that the whole material listed in 1903
constitutes the type material as listed below.

Type material. Figured syntypes: NHMW 84162 (local¬
ity 145), illustrated by Sturany (1903) in plate I, figure
la, height 137.6 mm. NHMW 84147 (station 20): 1 spec¬
imen, illustrated by Sturany (1903) in plate I, figure 3a.

Further syntypes: NHMW 84148 (station 20): 1 spec¬
imen; NHMW 84150 (station 20): 1 specimen; NHMW
84152 (station 48): 1 specimen; NHMW 84153 (station
76): 1 specimen; NHMW 84157 (station 107): 1 speci¬
men; NHMW 84158 (station 109): 1 specimen; NHMW
84159 (station 121): 1 specimen; NHMW 84163 (station
156): 5 specimens.

Additional material. NHMW 84160 (station 145): 3
specimens; NHMW 84161 (station 145): 1 specimen;
NHMW 84169 (station 175): 1 specimen, foxmpaucicos-
tata written on label, but looks like the nominal species.

Original description. Schale lang spindelfdrmig, ziem-
lich schlank, mehr oder minder festschalig, mit langem,
kaum gedrehtem Canal; von den 11 starker oder schwd-
cher gewolbten Umgdngen sind die ersten 1 1/2 als glat-
tes, bldschenfdrmiges

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Figure 11. Fusus bifrons Sturany, 1900, Station 145 (east of Dahlak Island, Eritrea). A. Original figure of form typica by Sturany
(1903). B-D, I-J. Figured syntype, NHMW 84147 (f. typica); front (B), right side (C), back (D), protoconch (I-J). E. Original figure
of form paucicostata by Sturany (1903). F-H, K-L. Figured syntype, NHMW 84146 (f. paucicostata): front (F), right side (G), back
(H), protoconch (K-L). Scale bars: B-D, F-H; 20 mm; I-J, K-L; 0.2 mm.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Embryonalgewinde abgesetzt, auf welches einige
zarte Querrippen folgen, die nun aber bald zu derberen
Querwulsten anwachsen und als solche entweder bis auf
die letzte Windung reichen (F. typical oder nur drei bis
vier Umgdnge besetzen (F. paucicostata/ Ferner ist eine
deutliche, engstehende Spiralsculptur ausgeprdgt: es
wechseln stdrkere und schwdchere Spiralreifen ziemlich
regelmdfiig ab, welche entsprechend gewellt sind, wo sie
iiber die Faltenrippen laufen. Spindel mit Belag, schwach
Oder gar nicht gerunzelt. Gaumen mit engen Falten be-
setzt. Mundung oval, nach oben etwas zugespitzt. Farbe
gelblichweifi, bei frischen Exemplaren etliche Spiralrei¬
fen braun gefdrbt.

Bis 160 mm lang und 38mm breit; Mundung sammt
Canal bis 92 mm lang und 19 mm breit.

Diese neue Art Idsst sich weder mit F. multicarinatus
Lm., noch mit F. turricula Kien. (= forceps Perry) glatt
vereinigen, dock ist sie immerhin von der letztgenannten
Art abzuleiten, von der sie durch eine weniger einschnei-
dende Naht, feinere Spiralreifen und engere Berippung
des Gaumens unterschieden ist. Sie bewohnt die conti-
nentale Zone des Rothen Meeres und wurde hier zwi-
schen 490 und 900 m Tiefe des Ofteren gedredscht. Die
F. paucicostata ist eine charakteristische Abweichung,
die sich gewohnlich schon bei jungen Schalen durch das
relativ grofiblasige Embry onalgewinde verrdth, sowie
durch das fruhzeitige Aufhdren der Querwulste, wodurch
die folgenden Windungen flacher sich gestalten und ge-
rade verlaufende Spiralreifen bekommen, das ganze Ge-
hduse auch specifisch leichter wird.

Translation. Fusiform and elongated shell, rather slen¬
der, more or less robust, with long, slightly twisted canal;
of the 11 more or less convex whorls, the first 1 1/2 are
separated into a smooth, infiated

protoconch after which some delicate axial ribs follow,
which soon grow into coarser varices and either contin¬
ue down to the last whorl (f typica) or are present only
on three to four whorls (f paucicostata). Additionally, a
clear, fine spiral sculpture takes form: stronger and weaker
spiral rings alternate on a fairly regular basis and are un¬
dulated when they cross the ribs. Columella with a callus,
weakly or not at all wrinkled. Aperture with fine teeth,
oval, slightly pointed in the upper part. Colour yellowish
white, with some brown spiral lines in fresh specimens.

Up to 160 mm long and 38 mm wide; aperture with
canal up to 92 mm long and 19 mm wide.

This new species cannot be merged either with F. mul¬
ticarinatus Lamarck or with F. turricula Kiener {=forceps
Perry), but it can be distinguished from the latter species
because of a shallower suture, finer spiral threads and nar¬
rower ribbing of the lip. It inhabits the continental zone
of the Red Sea and was dredged at depths of 490-900 m.
The form paucicostata is a characteristic deviation, usually
shown in young shells by the relatively large bubbled pro¬
toconch and the early disappearance of the axial ribs, so
that the following whorls appear fiatter, the spiral threads
straighter and the whole shell is significantly lighter.

Comments. Sturany described two forms or varieties
of this species, which differ only slightly in the more or
less extended development of axial ribs in respect to their
strength and number. Both forms intergrade and are con¬
sidered phenotypical variations of the same taxon (see
also Snyder 2002).

Fusus bifrons f. paucicostata Sturany, 1900

Figure 11E-H,K-L

Sturany, 1900a: 197-198; redescribed and illustrated in Sturany (1903),
pages 220-221, plate 1, figures 2 and 4.

Type material. Figured syntypes: NHMW 84146 (station
9): 1 specimen, illustrated by Sturany (1903) in plate I,
figure 4a; NHMW 84171 (station 175): 1 specimen, re¬
ported on label that this specimen is illustrated by Sturany
(1903) in plate I, figure 2a, height 113 mm.

Further syntypes: NHMW 84149 (station 20): 2 spec¬
imens; NHMW 84151 (station 20): 1 specimen; NHMW
84154 (station 76): 1 specimen; NHMW 84155 (station
76): 5 specimens; NHMW 84156 (station 81): 1 speci¬
men; NHMW 84164 (station 165): 1 specimen; NHMW
84165 (station 165): 1 specimen; NHMW 84172 (station
176): 1 specimen; NHMW 84173 (station 176): 1 speci¬
men; NHMW 84175 (station 179): 3 specimens; NHMW
84176 (station 179): 3 specimens; NHMW 84177 (sta¬
tion 179): 2 specimens; NHMW 84178 (station 179): 1
specimen; NHMW 84179 (station 184): 1 specimen. Two
more specimens are present without labels and inventory
numbers, they probably come from stations 47 and 178.

Additional material. NHMW 84166 (station 170): 3
specimens; NHMW 84167 (station 175): 1 specimen;
NHMW 84168 (station 175): 1 specimen; NHMW 84169
(station 175): 1 specimen, form paucicostata written on
label, but looks like the nominal species; NHMW 84170
(station 175): 7 specimens.

Original description, translation and comment. See

Fusus bifrons.

Family Nassariidae Iredale, 1916

Nassa lathraia Sturany, 1900

Figure 12

Sturany, 1900a; 200-201; redescribed and illustrated in Sturany (1903),
pages 224-225, plate II, figures 2a-b.

Type locality. Station 130, “westlich von Kunfidah”
[west of Al Qunfudhah, Saudi Arabia], 19°17'N, 39°37'E,
439 m.

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Figure 12. Nassa lathraia Sturany, 1900, Station 130 (A1 Qunfudhah, Saudi Arabia, Red Sea). A-B, D-G, I. Figured syntype,
NHMW 84203: front (A-B), right side (D-E), back (F), protoconch (G, I). C. Original figure by Sturany (1903). H. Original label
of figured syntype. Scale bars: A-B, D-F: 1 mm, G, I: 0.2 mm.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Additional original localities. Stations 48, 51, 54, 107,
114, 121, 127, 130 (439 - 748 m) (Central and Southern
Red Sea; Table 1).

Type material. Figured syntypes: NHMW 84203 (station
130; height: 6.6 mm, figured in Sturany 1903, plate II,
figures 2a-b), NHMW 84205 (station 135): 1 specimen
(figured in Sturany 1903, plate II, figures la-b). Further
syntypes: NHMW 71640/0/745 (station 130): 2 specimens;
NHMW 84196 (station 48): 2 specimens; NHMW 84197
(station 51): 3 specimens; NHMW 84198 (station 54): 5
specimens; NHMW 84199 (station 107): 2 specimens;
NHMW 84200 (station 114): 5 specimens; NHMW 84201
(station 121): 1 specimen; NHMW 84202 (station 127):
1 specimen; NHMW 84204 (station 130): 12 specimens.

Original description. Von den Stationen 48, 51, 54, 107,
114, 121, 127, 130 (439 - 748 m). Diese Form ist von
N. munda durch die bedeutend spdrlicher vorhandenen,
jedoch schdrfer ausgeprdgten Querrippen unterschieden,
zwischen denen die Spiralstreifung deutlich sichtbar
wird. Mit Ausnahme der glatten Anfangswindungen tra-
gen die Umgdnge oben ndchst der Naht eine besonders
abgesetzte Kornchenreihe.

Hohe des Gehduses circa 71/2, Breite circa 3 1/2 mm;
Mundung circa 3 1/2 mm hoch und 2 mm breit.

Wie N. munda m. in der continentalen Zone gefunden,
in Tiefen zwischen 439 und 748 m.

Translation. From stations 48, 51, 54, 107, 114, 121,
127, 130 (439 - 748 m). Distinguished from N. munda
by the much sparser, but more sharply pronounced axial
ribs between which the spiral stripes are clearly visible.
Except for the smooth initial whorls, the others bear a
tubercled cord on their upper part next to the suture.

Shell height about 7.5, width about 3.5 mm; mouth
about 3.5 mm high and 2 mm wide.

Like N. munda, it is found in the continental zone, at
depths of 439-748 m.

Comments. For discussion of relationships and nomen¬
clature see under Nassa munda.

Nassa munda Stnrany, 1900

Figure 13

Sturany, 1900a: 200; redescribed and illustrated in Sturany (1903), page
223-224, plate II, figures 4a-b.

Type locality. Station 135, “stidosthch von Akik Seghir”
[south-east of Akik Seghir, Eritrea], 17°26.rN, 39°19'E,
332m.

Additional original localities. Station 135 (332 m) and
145 (800 m) (Southern Red Sea; Table 1).

Type material. Figured syntype: NHMW 84190 (station
135; height: 9.9 mm; figured in Sturany 1903, plate II,

figures 4a-b). Further syntypes: NHMW 71640/0/746
(station 135): 4 specimens; NHMW 84191 (station 135):
14 specimens; NHMW 84192 (station 145): 1 specimen.

Additional material. NHMW 84193 (station 170): 1
specimen.

Original description. Gehduse klein und festschalig,
kegelig-oval; von den acht Umgdngen sind die ersten
gerundet und glatt, die ubrigen stufig abgesetzt und mit
zahlreichen Querwulsten (etwa 26 auf der Schlusswin-
dung) ausgestattet, die von Spiralstreifen gekreuzt und
gekerbt werden. Auch ist durch eine schdrfer eingegra-
bene Spirallinie der oberste Theil jeder Windung als eine
Reihe von Hockerchen abgesetzt. Auf dem Aufienrande
der Mundung in der Regel sechs bis acht Zdhnchen, von
denen einige besonders hervortreten konnen. Andeutung
von Banderung nur selten zu beobachten.

Hohe der Schale 71/2 bis 9 3/4, Breite 4 1/4 bis 5 mm;
Hohe der Mundung 3 1/2 bis 4 1/2, Breite derselben 2 bis
2 3/4 mm.

Von Station 135 (332 m) und 145 (800 m) vorliegend.

Translation. Shell small and thick, conical-oval; of the
eight whorls, the first are rounded and smooth, the other
scalariform with numerous axial ribs (about 26 on the last
whorl) which are crossed and notched by spiral threads.
The uppermost part of each whorl bears a strongly sculp¬
tured spiral cord with a series of tubercles. On the outer
edge of the mouth, there are usually six to eight teeth,
some of which may be particularly prominent. Traces of
colour bands can rarely be observed.

Height of the shell 7.5 to 9.75, width 4.25 to 5 mm;
height of the mouth 3.5 to 4.5, width 2 to 2.75 mm.

From station 135 (332 m) and 145 (800 m).

Comments. Cernohorsky (1984: 156) listed munda
as nomen dubium and possible synonym of Nassarius
{Zeuxis) idyllius (Melvill & Standen, 1901).

Nassa lathraia as well as N. sporadica, N. stiphra and
N. munda are published at the same date and are regarded
synonymous. Examination of the type material as well as
of rich material from various expeditions to the deep Red
Sea (RJ) shows that the various names only denote sculp¬
tural variants which can be observed to occur together in
part at the same stations and which cannot be told apart
as different taxa. Whereas Janssen in Janssen and Tavi-
ani (2015) used lathraia as valid name, Dekker and Orlin
(2000: 28) should be regarded as first revisers who se¬
lected Nassarius mundus (Sturany, 1900) as valid name
for the taxon explicitly denoting the other names as syn¬
onyms. Cernohorsky (1984: 103) regarded lathraia as a
possible synonym of Nassarius {Niotha) sinusigerus (A.
Adams, 1852). Whether this is correct needs further study
and comparison of many other conchologically similar
species. If it proves correct, sinusigerus would become
the valid name for this assemblage of forms denoted by
Sturany with four names.

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Figure 13. Nassa munda Sturany, 1900, Station 135 (Akik Seghir, Eritrea, Red Sea). A-C, E. Figured syntype, NHMW 84190;
front (A), right side (B), back (C), protoconch (E). D. Original figure by Sturany (1903). F. Original label of figured syntype. Scale
bars: A-C: 2 mm, E; 0.2 mm.

Nassa sporadica Sturany, 1900

Figure 14

Sturany, 1900a: 201; redescribed and illustrated in Sturany (1903), page
224, plate II, figures 5a-b.

Type material. Holotype: NHMW 84194, height 11.7 mm.

Type locality. Station 54, 24°48'N, 35°25'E, Central Red
Sea, 535 m.

Original description. Das Gewinde dieser mit N. munda
m. verwandten Form besteht aus 8 1/2 Umgdngen und ist

oben stufig abgesetzt. Die Querwulste stehen bedeutend
enger als bei jener Art, so dass auf der letzten Windung
etwa 35 abzuzdhlen sind. Von einer Banderung nur ganz
geringe Spuren sichtbar. Aufienrand der Mundung mehr-
fach und unregelmdfiig gezdhnt.

Hohe der Schale 11 V 2 , Breite 6 1/4 mm; Mundung 6
mm hoch und 3 1/2 mm breit. — Bin einziges Exemplar
von Station 54 (535 m).

Translation. The spire of this species is related to the
one of N. munda and consists of 8.5 whorls and is sca-

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 14. Nassa sporadica Sturany, 1900, Station 54 (Central Red Sea). A-C, E. Holotype, NHMW 84194: front (A), right side
(B), back (C), protoconch (E). D. Original figure by Sturany (1903). F. Original holotype label. Scale bars: A-C: 2 mm, E: 0.2 mm.

lariform on top. The axial ribs are significantly closer
compared to the mentioned species, so on the last whorl
35 can be counted. Only very small traces of colour
bands are visible. Lip with numerous and irregular
teeth.

Shell height 11.5, width 6.25 mm; mouth 6 mm high
and 3.5 mm wide. One specimen from station 54 (535 m).

Comments. Nassa sporadica was regarded as nomen du-
bium and possible synonym of Nassarius (Zeuxis) crebri-
costatus (Schepman, 1911) by Cemohorsky (1984: 160).
For further comments on validity of sporadica see under
Nassa munda.

Nassa steindachneri Sturany, 1900

Figure 15

Sturany, 1900a: 199; redescribed and illustrated in Sturany (1903), pages
222-223, plate II, figures 9a-c.

Type locality. Station 170, “bei der Insel Noman” [No¬
man Island, Saudi Arabia], 27°0.2'N, 35°17.6'E, 690 m.

Additional original localities. Stations 124, 135, 170
and 179 (314 - 690 m) (Red Sea; Table 1).

Type material. Figured syntype: NHMW 84187 (sta¬
tion 179): 1 specimen (figured in Sturany 1903, plate II,

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Figure 15. Nassa steindachneri Sturany, 1900, Station 170 (Noman Island, Saudi Arabia, Red Sea). A-C, H. Syntype, NHMW
84186: front (A), right side (B), back (C), protoconch (H). D-F. Syntype, NHMW 84185, Station 135 (Akik Seghir, Eritrea, Red
Sea); front (D), right side (E), back (F). G. Original figure by Sturany (1903). I. Original label of syntypes NHMW 84186. Scale
bars: A-F; 3 mm, H: 0.2 mm.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

figures 9a-c). Further syntypes: NHMW 84186 (station
170) 3 specimens ; NHMW 84185 (station 135): 3 spec¬
imens and 1 fragment; NHMW 84188 (station 179): 5
specimens.

Additional material. NHMW 84184 (station 94): 3 spec¬
imens; NHMW 111537 (station 51): 1 specimen.

Original description. Gehduse in Gestalt und Win-
dungszahl mit der vorigen Art ubereinstimmend, von ihr
aber durch die bis zur Mundung herabreichende Cancel-
lierung gut unterschieden. Nur das Embryonalgewinde
ist glatt, die ubrigen Umgdnge sind durch grobere,
etwas gekriimmte Querwulste und zarte Spirallinien
regelmdfiig gegittert; der oberste Theil der letzten vier
Windungen ist uberdies von dem ubrigen Theile der-
selben durch eine mit der Naht parallel laufende, defer
einschneidende Spiral fur che als wulstige Kornchenreihe
getrennt. Von den Binden der verwandten Art sind nur
noch Spuren sichtbar.

Hohe der Schale 29, Breite 13 mm; Mundung 13 mm
hoch und 7 mm breit. — Von den Stationen 124, 135, 170
und 179 vorliegend; in Tiefen bis 690 m gefunden.

Translation. Shell in shape and number of whorls ana¬
logue the previous species, but well differentiated by the
cancellated sculpture descending to the mouth. Only the
protoconch is smooth, the remaining whorls are regularly
gridded by coarser, slightly curved varices and delicate
spiral lines; the uppermost part of the last four whorls is
also separated from the other parts by an incised spiral
channel running parallel to the suture as a thick series
of tubercles. Of the colour bands observed in the related
species, only traces are here visible.

Shell height 29, width 13 mm; mouth 13 mm high and
7 mm wide. Found in stations 124, 135, 170 and 179; at
depths up to 690 m.

Comments. When a lectotype shall be selected, a spec¬
imen should be taken which is better preserved than the
specimen figured by Sturany, which has a partly eroded
protoconch and early teleoconch whorls. For discussion
of relationships see under thaumasia.

Nassa stiphra Sturany, 1900

Figure 16

Sturany, 1900a: 200-201; redescribed and illustrated in Sturany (1903),
page 224, plate II, figures 3a-b.

Type locality. Station 143, “nachst der Insel Harmil”
[near Harmil Island, Dahlak Archipelago, Eritrea]

17°7'N, 39°55'E, 212 m.

Type material. Holotype: NHMW 84195, height: 6.9 mm.

Original description. Schale gedrungen, kegelformig,
aus sieben gerundeten, durch eine tiefe Naht getrennten

Umgdngen aufgebaut, von denen das Embry onalgewinde
schwach gekielt und glatt ist, die ubrigen wie bei N. mun-
da mit deutlichen Querwulsten ausgestattet sind (mit 22
Wulsten auf der Schlusswindung). Auch zarte Spiral¬
linien treten auf, jedoch nur unter der Naht und im Um-
kreise des Nabels deutlich. Der Aufienrand der Mundung
trdgt sechs bis sieben Zdhne, von denen ein mittlerer und
der unterste krdftiger sind. Auf der letzten Windung zwei
gelbe Binden auf weifiem Grunde.

Hohe der Schale 7,2, Breite 4,2 mm; Mundung 3,5 mm
hoch und circa 2 mm breit. — Ein Exemplar von Station
143 (212 m).

Translation. Shell compact, cone-shaped, composed of
seven rounded whorls separated by a deep suture; the pro¬
toconch is weakly keeled and smooth, the teleoconch is
equipped with significant axial ribs (22 on the final whorl)
as in N. munda. Also delicate spiral threads occur, but
are distinct only under the suture and around the umbili¬
cus. The outer lip carries internally six to seven teeth, of
which the median and the lowest are the strongest. On the
last whorl, there are two yellow bands on white ground.

Shell height 7.2, width 4.2 mm; mouth 3.5 mm high
and about 2 mm wide. One specimen from station 143
(212 m).

Comments. This name was listed by Cernohorsky (1984:
107) as a questionable synonym of Nassarius (Niotha)
agapetus (Watson, 1882). For further comments see un¬
der munda.

Nassa thaumasia Sturany, 1900

Figure 17A-E

Sturany, 1900a: 198-199; redescribed and illustrated in Sturany (1903),
page 222, plate II, figure 8.

Type locality. Ras Abu Somer (not specified in the origi¬
nal text, but very likely locality 18, littoral; Table 2).

Additional original localities. 94 (314 m) (Northern Red
Sea, Table 1).

Type material. Eectotype: NHMW 37579 (locality 18;
height 27 mm), fixed by erroneous inference of “holo¬
type” (ICZN art. 74.6) by Cernohorsky 1984: 132, pi. 25
fig. 10. Paralectotype: NHMW 111535: 1 specimen (Ras
Abu Somer, likely locality 18).

Additional material. NHMW 84180 (station 87): 7
specimens.

Original description. Gehduse festschalig, aus 10 1/2
langsam zunehmenden, schwach stufig abgesetzten
Windungen kegelig aufgebaut; das Embry onalgewinde
glatt, die daraujfolgenden Umgdnge mit breiten Quer¬
wulsten und vier bis funf Spiralreihen ausgestattet, die
Schlusswindungen (2 1/2 oder mehr) abgegldttet bis auf

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eine zur Naht parallel ziehende Spiralfurche und eine
Reihe von Spirallinien in der Nabelgegend im Umkrei-
se des Ausschnittes der Mundungsbasis; auf gelblich-
weifiem Grundtone sind gelbbraune Querstriemen in
unregelmdfiiger und spdrlicher Vertheilung und auf dem
letzten Umgdnge zwei breite, gelbbraune Langsbinden
mehr oder minder ausgeprdgt; kurz vor dem dufieren
Mundungsrand ein dicker Wulst, im Gaumen, sowie auf
dem Wulste der Spindel und der Mundungswand eine
grofiere Anzahl von Falten; der untere Theil des dufieren
Mundungsrandes etwas ausgezackt.

Hdhe der Schale 27,2, Breite 13,0mm; Hdhe der
Mundung 14,0, Breite 7,5mm. Fundort: Ras Abu Somer
(litoral).

Translation. Shell thick, conical, made of 10.5 slowly
growing, weakly scalariform whorls; smooth protoconch,
the following whorls have broad axial ribs and four to
five spiral threads, the final whorls (two and half or more)
smooth except for a groove parallel to the suture and a
series of spiral lines in the umbilical region close to the
aperture; on the yellowish-white background there are
irregularly and sparsely distributed yellow-brown flecks
and on the last whorl there are two wide, yellow-brown
spiral bands more or less pronounced; shortly before the
outer lip there is a thick varix; there is a large number of
folds on the callus of the columella and the inner lip; the
lower part of the lip is slightly jagged.

Shell height 27.2, width 13.0 mm; height of the mouth
14.0, width 7.5 mm. Locality: Ras Abu Somer (littoral).

Comments. Nassa steindachneri, thaumasia, thauma-
sia var. nana and xesta are regarded as synonymous. N.
thaumasia var. nana and steindachneri occur togeth¬
er at station 94 and both lots show the same variability
of sculpture from regularly reticulated to nearly smooth
last whorls. Janssen in Janssen and Taviani (2015: 526)
used steindachneri as valid name because this is the most
common variant, but Dekker and Orlin (2000: 28) syn-
onymised already these taxa and as first revisers selected
Nassarius thaumasius (Sturany, 1900) as valid name. Nas¬
sa thaumasia was considered by Cemohorsky (1984: 130)
as synonym of Nassarius {Zeuxis) castus (Gould, 1850).
However, this is most probably wrong, because accord¬
ing to own observations (RJ) thaumasia has a much finer
sculpture consisting of dense reticulation, especially on
the early whorls, more numerous and finer spiral ribs on
the fasciole, only weakly canaliculated sutures and a much
lesser developed sutural nodules. Cemohorsky figured the
alleged “holotype” of thaumasia on his pi. 25 fig. 10.

According to Cemohorsky (1984: 135), Nassa stein¬
dachneri is a synonym of Nassarius {Zeuxis) siquijoren-
sis (A. Adams, 1852). If this proves to be correct, siquijo-
rensis would become the valid name for the assemblage
of nominal taxa described by Sturany, but this needs fur¬
ther study.

Nassa thaumasia f. nana Sturany, 1900

Figure 17H-J

Sturany, 1900a: 199; redescribed and illustrated in Sturany (1903), page
222, plate II, figure 7.

Original localities. 94 (314 m) and 96 (350 m) (Northern
Red Sea, Table 1).

Type material. Syntypes: NHMW 84181 (station 94):
1 specimen; NHMW 84182 (station 94): 11 specimens;
NHMW 84183 (station 96): 1 specimen.

Original description. In der continentalen Zone (Station
94 [314 m] und Station 96 [350 mj) kommt eine kleinere
Form vor (var. nana m.), deren Ldnge 20 und deren Brei¬
te 10 mm betragt bei einer Mundungsausdehnung von 10
V 2 : 6mm.

Translation. In the continental zone (station 94 [314 m]
and station 96 [350 m]), there is a smaller form (var. nana)
with 20 mm length and 10 mm width, at the aperture 10.5
high and 6 mm wide.

Comments. The variety nana was introduced for the
deep water specimens; the specimen illustrated in Figure
17 H-J is 19.8 mm high. For further comments see under
thaumasia.

Nassa xesta Sturany, 1900

Figure 18

Sturany, 1900a: 199-200; redescribed and illustrated in Sturany (1903),
page 223, plate II, figures 6a-b.

Type locality. Station 143, “nachst der Insel Harmil”
[near Harmil Island, Dahlak Archipelago, Eritrea]

17°7'N, 39°55'E, 212 m.

Type material. Holotype: NHMW 84189, height 19.4 mm.

Original description. Gehduse kegelig aufgebaut,
dickschalig, fettgldnzend; von den 9 1/2 Windungen
sind nur die vierte und fiinfte mit Querwiilsten ausge-
stattet, die ubrigen glatt mit Ausnahme etwa noch des
Basaltheiles der Schlusswindung, wo wieder concen-
trisch angeordnet und am Aufienrande der Mundung als
Kerbung endigend, funfbis sechs Spiralreifen zu zdhlen
sind. Eine Banderung ist nur in Spuren vorhanden,
ferner sind nachst der Naht gelbbraune Flecken sicht-
bar, welche von milchweifien Partien des Grundtones
besonders abstechen. Vor der Mundung ein Wulst, im
Gaumen zahlreiche Falten und ebenso auf den Callus-
partien eine Fdltelung.

Hdhe des Gehduses 20, Breite 10mm; Mundung 9,5
mm hoch und 5,5 mm breit. — Von Station 143 (212 m)
ein einziges Exemplar vorliegend.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 16 . Nassa stiphra Sturany, 1900, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea). A-B, D-G, I. Holotype, NHMW
84195: front (A-B), right side (D-E), back (F), protoconch (G, I). C. Original figure by Sturany (1903). H. Original holotype label.
Scale bars; A-B, D-F: 1 mm, G, I; 0.2 mm.

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Figure 17. Nassa thaumasia Sturany, 1900. A-C, E. Lectotype, NHMW 37579, Ras Abu Somer, Egypt, Red Sea (likely “locality
18”): front (A), right side (B), back (C), protoconch (E). D. Original figure by Sturany (1903). F. Original lectotype label. G. Original
label of the foxmnana. H-J. Voxmnana, syntype NHMW 84181, Station 94 (Nuweiba, Gulf of Aqaba, Egypt): front (H), right side (I),
back (J). Scale bars: A-C, H-J: 5 mm, E: 0.2 mm.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 18. Nassa xesta Sturany, 1900, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea, Red Sea). A-C, E. Holotype,
NHMW 84189: front (A), right side (B), back (C), protoconch (E). D. Original figure by Sturany (1903). F. Original holotype label.
Scale bars: A-C: 3 mm, E: 0.2 mm.

Diese und die vorhergehenden Nassa-^lrfew gehoren
in eine Reihe und lassen sich etwa von N. gaudiosa
Hinds ableiten.

Translation. Shell conical, thick, shiny; of the 9.5 whorls,
only the fourth and the fifth have axial ribs, the others are
smooth except at the base of the final whorl, where five to
six concentric spiral grooves can be counted ending at the
lip as notches. Only traces of colour bands are present,
next to the suture yellow-brown flecks are visible, which
contrast with the milky white ground colour. Before the
aperture there is a thickened spiral rib, the lip and the cal¬
lus have numerous folds.

Height of the shell 20, width 10 mm; aperture 9.5 mm
high and 5.5 mm wide. From station 143 (212 m) a single
specimen was found.

This and the preceding Nassa species belong to a se¬
ries and are related to N. gaudiosa Hinds.

Comments. Cemohorsky (1984: 146) XisiQd xesta as pos¬
sible synonym of Nassarius {Zeuxis) comptus (A. Adams,
1852). However, closer examination of the types demon¬
strates that xesta is only an extreme form of thaumasia to
which it agrees completely with regard to colour pattern
and sculpture of the early teleoconch whorls. For further
comments see under thaumasia.

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Family Mitridae Swainson, 1831
Mitra (IThala) gonatophora Sturany, 1903

Figure 19

Sturany, 1903: 225, plate IV, figure 2.

Original localities. Station 48 (700 m) and 51 (262 m)
(Central Red Sea; Table 1).

Type material. Figured syntype: NHMW 84210 (station
48), illustrated by Sturany (1903) in plate IV, figure 2,
height 7.2 mm. Further syntypes: NHMW 84211 (station
48): 1 specimen; NHMW 84212 (station 51): 2 specimens.

Original description. Von den Stationen 48 (700 m) und
51 (562 m).

Der zundchst folgenden Beschreibung ist ein zur
Abbildung gebrachtes Exemplar von der Station 48 zu
Grunde gelegt, welches bei kaum 8 Umgdngen 8,2 mm
hoch und 2,5 mm breit ist, wahrend die Mundungshohe
4,2 und die Mundungsbreite 1,5 mm betrdgt. Die Schale
ist spindelfdrmig und an der Basis etwas zuruckgebogen.
Die Sculptur beginnt auf der 4. Windung, kurz nach Ab-
lauf der dritten, und zwar mit 3 Spiralreihen von Knoten.
Mit dem Beginne der vorletzten Windung setzt auch eine
Spaltung der beiden unteren Knotenreihen in je 2 zartere
Spiralreifen ein, so dass also auf der vorletzten Windung
1 breitere obere Knotenreihe und 4 zartere, darunter ge-
legene Spiralreifen abzuzdhlen sind. Auf der Schlussw in¬
dung verlaufen unter den genannten Knotenreihen noch
9 in gleichmdfiigen Entfernungen voneinander getrennte
Knotenreihen, welche am dufieren Mundrande endigen,
und uberdies noch einige um den untersten Theil der
Schale gelagerte Spiralreifen. In den Zwischenrdumen
der Knotenreihen liegen regelmdfiige Querstriche, so
dass eine Cancellierung hervorgebracht ist. Das Gehdu-
se ist nicht ganz einfarbig braun, in der Mundung und
ebenso in der ziemlich tiefliegenden Naht ist eine weifie
Fdrbung erkennbar. Auf der Spindel, welche weifi ausge-
schlagen ist, stehen 3 stdrkere Querfalten und unter die-
sen eine schwdchere; iiber ihnen erscheinen einige der
Spiralreifen des letzten Umganges in Form von in das
Spindelfeld hereinragenden Falten fortgesetzt.

Das zweite minder gut erhaltene Exemplar von Station
48 (700 m) Idsst gleichwohl einige Ergdnzungen

der obigen Diagnose zu. Es misst 7 V 2 : 2 Vi mm und
Idsst einen schwachen Glanz des Embryonalgewindes er-
kennen, sowie eine geringe Anzahl von Columellarfalten
(nur 3 Hauptfalten und keine dariibergelagerten
Fortsetzungen der Spiralreifen bis ins Spindelfeld).
Mitra mirifica Rve. ist wohl eine der ndchststehenden
Verwandten.

Translation. From stations 48 (700 m) and 51 (562 m).

The following description is based on a figured spec¬
imen from station 48 [Figure 19 A-G], which has almost
eight whorls, 8.2 mm high and 2.5 mm wide, while the
height of the mouth is 4.2 and the width 1.5 mm. The shell
is fusiform and at the base slightly curved. The sculpture

starts on the fourth whorl, shortly after the end of the third,
with three spiral rows of tubercles. At the beginning of
the penultimate whorl a splitting of the two lower rows of
tubercles in two delicate spiral cords begins, so that on the
penultimate whorl one expanded upper row of tubercles
and four more delicate, lower spiral rows can be counted.
On the final whorl under the mentioned rows of tubercles,
nine further rows of tubercles run at uniform distances and
end at the outer lip, additionally some more spiral rows
run on the lowest part of the shell. In the interstices of the
spiral rows, there are regular axial riblets so that a can¬
cellated sculpture is generated. The shell is not uniformly
brown, in the mouth and on the quite deep suture a white
colouration can be seen. On the columella, which has a
white callus, there are three strong transverse folds, and
below them a weak one; some of the spiral rows of the last
whorl continue above them under the columellar callus.

The second less well-preserved specimen from Station
48 (700 m) [Figure 191-K] allows nevertheless some addi¬
tions to the diagnosis above. It measures 7.5 mm [height]
2.5 mm [width] and reveals a weak lustre of the proto¬
conch, and a small number of columellar folds (only three
main folds, not continuing under the columella callus).

Mitra mirifica Reeve is probably one of the closest rel¬
atives.

Mitra tenuis f. minor Sturany, 1903

Figure 20

Sturany, 1903: 244-245, plate VII, figure 7.

Original localities. Localities 10 and 21 (Northern Red
Sea; Table 2).

Type material. Figured syntype: NHMW 37613 (locality
21), illustrated by Sturany (1903) in plate IV, figure 2,
height 12 mm. Further syntypes: NHMW 37612 (locality
10): 1 specimen; NHMW 37185 (locality 21): 1 specimen
(preserved in ethanol).

Original description. Von den Localitdten 10 und 21.

Das zur Abbildung gebrachte gelbbraune Gehduse von
Koseir ist 11,5 mm hoch und 3,5 mm breit, besitzt eine
Mundung von 6 mm Hdhe und besteht aus 10 Umgdngen.
Die Anfangswindungen sind glatt, zitzenfbrmig, hellgelb
gefdrbt, die folgenden Umgdnge mit einer fadenfbrmigen,
hellfarbigen Verdickung an der oberen Naht und einigen
Spirallinien ausgestattet. Auf dem letzten Umgange Iduft
eine mediane helle Binde, die ebenso wie die erwdhnte
lichte Nahtpartie sich schdrfer von der sie umgebenden
Fdrbung abheben kann (beispielsweise bei einem etwas
kleineren Exemplare von Nawibi). Die Spindel ist mit ei¬
ner stdrkeren und einigen schwdcheren Falten versehen.

Fiir das Rothe Meer ist M. tenuis noch nicht bekanntge-
wesen. Das Berliner Museum besitzt sie von Mauritius und
ebendaher stammt die nahverwandte M. flexilabris Sow.

Translation. From localities 10 and 21.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 19. Mitra gonatophora Sturany, 1903, Station 48 (Yanbu’ al Bahr, Saudi Arabia, Red Sea). A-G. Figured syntype, NHMW
84210: front (A-B), right side (C-D), back (E), protoconch (F-G). H-K. Syntype, NHMW 84211: protoconch (H), front (I), right
side (J), back (K). L. Original figure by Sturany (1903). Scale bars: A-E, I-K: 1 mm, F-H: 0.2 mm.

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Figure 20. Mitra tenuis f. minor Sturany, 1903, Locality 21 (El Quseir, Egypt, Red Sea). A. Original figure by Sturany (1903). B-F. Figured
syntype, NHMW 37613; front (B), right side (C), back (D), microsculpture (E), protoconch (F). G. Original label. Scale bars: B-D: 2 mm,
E-F; 0.25 mm.

The figured shell from El Quseir [locality 21 ] is 11.5
mm high and 3.5 mm wide, has an aperture 6 mm high
and consists of 10 whorls. The protoconch is smooth,
teat-shaped, light yellow, the following whorls show a
filiform, brightly coloured thickening on the suture and
some spiral lines. On the last whorl, there is a median
light coloured band, which may show up from the sur¬
rounding colour like the mentioned bright suture (like
in a slightly smaller specimen from Nawibi [locality
10]). The columella has one stronger and some weaker
folds.

M. tenuis was not yet known from the Red Sea. The Ber¬
lin Museum has specimens from Mauritius and from the
same locality the closely related M. flexilabris Sowerby.

Comments. The description of Mitra tenuis G.B. Sow¬
erby III, 1874 is based on an immature specimen. Cer-
nohorsky (1976) considered both it and Sturany’s minor
form junior synonyms of Mitra typha Reeve, 1845.

Family Drilliidae Olsson, 1964
Pleurotoma (Drillia) potti Sturany, 1900

Figure 21

Sturany, 1900b; 209-210; redescribed and illustrated in Sturany (1903),
page 229, plate III, figures 6a-b.

Type locality. Station 143, “nachst der Insel Harmil”
[near Harmil Island, Dahlak Archipelago, Eritrea] 17°7'N,
39°55'E, 212 m.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 21. Pleurotomapotti Sturany, 1900, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea, Red Sea). A-C, E. Holotype,
NHMW 84250; front (A), right side (B), back (C), protoconch (E). D. Original figure by Sturany (1903). F. Original holotype label.
Scale bars; A-C; 2 mm, E; 0.2 mm.

Type material. Holotype: NHMW 84250, height 12.4 mm.

Original description. Gehduse spindelfdrmig, aus nahe-
zu 8 Umgdngen gebildet, gelbbraun mit geringen Spuren
von etwa 6 —7 braunen Spiralbdndern, welche nur an
dem Wulste vor der Mimdung sichtbar sind; die Anfangs-
windungen glatt, glanzend und gerundet, die ubrigen mit
9—10 starken, schief gestellten und gewinkelten Querfal-
ten ausgestattet, so dass die ganzen Windungen gewin-
kelt erscheinen. Auf dem letzten Umgange schieben sich
zwischen diese hier nur mehr in der 8-Zahl vorhandenen
Querfalten einige undeutliche Nebenfalten ein und steht
unmittelbar vor der Mundung eine gewaltige, von der
Naht bis zur Basis verlaufende, rippenartige Verdickung.
Spiralsculptur nur an der Basis der Schlusswindung an-
gedeutet (schief uber den stielfbrmigen Canal verlaufen¬
de Linien). Mundung langgestreckt, mit leicht zuruckge-
bogenem Canal, scharfem, innen weifi gelippten Rande
und rundem Ausschnitte.

Hohe des Cehduses 12,0, Breite 4,3 mm; Mundung 6,0
hoch und 2,2 mm breit.

Ein Exemplar von Station 143 (212 m).

Als verwandte Formen seien P. pudica Hinds und P.
studeriana Marts, genannt.

Translation. Shell fusiform, with nearly eight whorls,
light brown with fine traces of about 6-7 brown spi¬
ral bands, which are visible only on the lip varix; the
protoconch is smooth, shiny and rounded, the other
9-10 whorls have strong, oblique and angulate axial
ribs, so that the whole whorls appear angulated. On the
last whorl, further indistinct axial threads are present
among the last eight axial ribs and, before the aperture,
there is a large axial thickening running from the suture
to the base. Spiral sculpture can be recognized only at
the base of the last whorl (oblique threads run on the
siphonal canal). Aperture elongated, with slightly re¬
curved canal, and a sharp, white inside, aperture border.

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Figure 22. Pleurotoma inchoata Sturany, 1900, Station 145 (Dahlak Archipelago, Eritrea, Red Sea). A. Original figure by Sturany
(1903). B-D, F. Holotype, NHMW 84251; front (B), right side (C), back (D), protoconch (F). E. Original holotype label. Scale
bars; B-D; 5 mm, F; 0.5 mm.

Height of the shell 12.0 mm, width 4.3 mm; mouth 6.0
mm high and 2.2 mm wide.

One specimen from station 143 (212 m).

P. pudica Hinds and P. studeriana Martens are known
as related forms.

Comments. It is considered to belong to genus Drillia Gray,
1838 by Tucker (2004), but it does not seem to fit well into
this genus. It may belong to Leiocithara Hedley, 1922.

Pleurotoma {IDrillia) inchoata Sturany, 1900

Figure 22

Sturany, 1900b; 210; redescribed and illustrated in Sturany (1903), page
229-230, plate III, figures 8a-b.

Type locality. Station 145, “ostlich von J. Dahalak” [east
of Dahlak Island, Eritrea], 16°2.6'N, 41°13.5'E, 800 m.

Type material. Holotype: NHMW 84251, height 21.2 mm.

Original description. Schale abgestutzt spindelfdr-
mig, hellgelb, aus 9 1/2 Umgdngen bestehend, deren
jeder mit Ausnahme des Embryonalgewindes in seiner
oberen Hdlfte concav, in seiner unteren convex gebaut
ist, und welche mit zahlreichen Spiralreifen und circa
15—16 wellenfdrmig verlaufenden Querrippen ausge-
stattet sind; uberdies stehen zwischen den Querrippen
noch mikroskopisch feine Anwachsstreifen. Unmittelbar
vor der (leider mangelhaft erhaltenen) Mundung eine
knotig angeschwollene und nach rechts vorgezogene
Querrippe.

Hohe der Schale 21,3, Breite 9,0 mm; Hohe der
Mundung 9,1 mm.

Bin einziges Exemplar von Station 145 (800 m).

Verwandt mit P. (Drillia^ pallida Sow.; in der Form an
Columbella angularis Sow. gemahnend.

Translation. Shell truncated and fusiform, pale yellow,
made by 9.5 whorls, concave in their upper half and con-

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

vex in the lower half, with the exeeption of the proto¬
conch; with numerous spiral threads and approximately
15-16 undulated axial ribs among which microscopi¬
cally fine growth lines stand. Immediately prior to the
(unfortunately poorly preserved) aperture, there is a thick
nodulose axial rib bent to the right.

Height of the shell 21.3 mm, width 9.0 mm; height of
the mouth 9.1 mm.

A single specimen from station 145 (800 m).

Related to P. {Drillia) pallida Sowerby; shape remind¬
ing Columbella angularis Sowerby.

Comments. This species can be assigned to the genus
Drillia Gmy, 1838

Pleurotoma {Clavus) siebenrocki Sturany, 1900

Figure 23

Sturany, 1900b: 210-211; redescribed and illustrated in Sturany (1903),
page 230, plate III, figures 9a-c.

Type locality. Station 76, “stidlich der Insel Senafir”
[south of Sanafir Island], 27°43'N, 34°47'E, 900 m.

Type material. Holotype: NHMW 84252, height 36.6 mm.

Original description. Schale gethurmt, geritzt, hellgelb-
braun, aus 12 Umgdngen aufgebaut, die mit Ausnahme
des Embryonalgewindes mit 7—8 knotenartigen Rippen
besetzt sind. In der tief eingeschnurten oberen Partie
der Umgdnge verlaufen feine Spirallinien, im ubrigen
grofiere, mitunter unregelmdfiig geknickte oder undu-
lierte Leistchen; die zahlreichen, feinen Anwachsstreifen
sind meist nur in den concaven Partien sichtbar. Mun-
dung mit tiefem, zungenformigen Ausschnitt oben und
sehr kurzem, zuruckgebogenen Canal unten.

Hohe des Gehduses 36,7, Breite 14,0 mm; Mundung
16,0 mm hoch und 5,5 mm breit.

Bin Exemplar von Station 76 (900 m).

Von der nachstverwandten Art P. (Clavus^ dun-
keri Wl^. durch die gestrecktere Form und die minder
„strombus-artige “ Mundung unterschieden.

Translation. Shell turriculate, striated, light golden
brown, composed of 12 whorls, which have 7-8 nodular
ribs except on the protoconch. In the deeply constricted
upper part of the whorls, there are fine spiral lines, where¬
as in the lower part coarser, sometimes irregularly Hexed
or undulated threads; the numerous, fine growth lines are
usually visible in the concave part only. Mouth with deep,
tongue-shaped posterior siphonal canal and a very short,
recurved anterior canal at the base.

Height of the shell 36.7 mm, width 14.0 mm; mouth
16.0 mm high and 5.5 mm wide.

One specimen from station 76 (900 m).

Distinguished from the closely related species P. {Cla¬
vus) dunkeri Weinkauff by the more elongated shape and
the less “strombus-like” aperture.

Family Horaiclavidae Bouchet, Kantor, Sysoev and
Puillandre, 2011

Pleurotoma (Surcula) nannodes Sturany, 1900

Figure 24

Sturany, 1900b: 209; redescribed and illustrated in Sturany (1903), page
230, plate III, figures 2a-c.

Original localities. Stations 48 (700 m) and 143 (212 m)
(Central and Southern Red Sea; Table 1).

Type material. Illustrated syntype: NHMW 84254 (sta¬
tion 143), illustrated by Sturany (1903) in plate III, fig¬
ures 2 a-c, height 8 mm. Further one syntype NHMW
84253 (station 48).

Original description. Schale reinweifi, abgestutzt spin-
delfbrmig, aus 9 Umgdngen bestehend. Die Embryo-
nalwindungen glatt, die ubrigen gegittert und knotig
sculptiert; ein median angelegter, dominierend breiter,
geperlter Spiralreifen, eine ndchst der Naht verlaufende
schwdchere Knotenreihe und 1 bis 2 feinste Spirallinien
ober und unter der Mitte (auf dem letzten Umgange sind
es naturgemdfi deren mehr) werden ndmlich von den
zahlreichen quer und bogig uber die Umgdnge gestellten
Ldngsrippen gekreuzt. Mundungsrand scharf, mitzungen-
fdrmigem Ausschnitte ndchst der Naht und halbkreisfdr-
miger Bucht an der Basis.

Hohe der Schale 7,1 und 8,4 mm, Breite 2,7 und 3,1
mm; Mundungshohe 2,6 und 3,0, Mundungsbreite 1,2 und
1,4 mm.

Von den Stationen 48 (700 m) und 143 (212 m) je ein
Exemplar.

Die neue Art ist gewissermafien eine Miniaturausgabe
von P. radula Hinds.

Translation. Shell pure white, tmncate fusiform, composed
by nine whorls. Protoconch smooth, the other whorls with
a reticulated and tubercled sculpture; a median, prominent,
wide, tubercled spiral thread; closer to the suture, there are
weaker tubercled threads and one or two fine spiral lines
above and below the median prominent spiral thread (on
the last whorl there are naturally more); the spiral sculpture
is crossed by numerous curved axial ribs. Lip sharp, with
tongue-shaped posterior siphonal canal next to the suture
and a semi-circular anterior canal at the base.

Height of shells is 7.1 mm and 8.4 mm, width 2.7 mm
and 3.1 mm; mouth height 2.6 mm and 3.0 mm, mouth
width 1.2 mm and 1.4 mm. From each of stations 48 (700
m) and 143 (212 m) one specimen.

The new species is a kind of miniature version of P.
radula Hinds.

Comments. This species was assigned to the genus
Paradrillia Makiyama, 1940 by Orlin and Dekker (2000:
32) and Janssen in Janssen and Taviani (2015: 526); it
looks like Paradrillia melvilli Powell, 1969, which could
be a junior synonym.

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Figure 23. Pleurotoma siehenrocki Sturany, 1900, Station 76 (Sanafir Island, Strait of Tiran, Red Sea). A. Original figure by Sturany
(1903). B-E. Holotype, NHMW 84252; front (B), right side (C), back (D), protoconch (E). F. Original holotype label. Scale bars;
B-D 5 mm, E; 1 mm.

Family Clathurellidae H. Adams & A. Adams, 1858

Mangilia pertabulata Sturany, 1903

Figure 25

Sturany, 1903: 231, plate III, figures la-c.

Type locality. Station 145, “ostlich von J. Dahalak” [east
of Dahlak Island, Eritrea], 16°2.6'N, 41°13.5'E, 800 m.

Type material. Holotype: NHMW 84255, height 5.4 mm.

Original description. Von der Station 145 (800 m); ein
einziges Exemplar.

Das spindelfdrmig gestaltete Gehduse besteht aus
8 Windungen, es ist der Farbe nach weifi, nur geringe
Spuren von gelbbrauner Fdrbung insbesondere am
dufieren Mundrande und am Embryonalgewinde sind zu
bemerken. Das Embry onalgewinde besteht aus einem
zitzenformigen, glatten Apex (ungefdhr 1 Umgang) und

2 doppelt gekielten Umgdngen (1 schnurformiger Kiel
steht in der Mitte, ein zweiter schwer auszunehmender
Iduft an der Naht). Die nun folgenden Umgdnge
haben eine mdfiige Anzahl Spiralreifen, von denen
regelmdfiig der mittlere der stdrkste und der am
meisten vorgezogene ist (daher der fast rechtwinkelige
Umriss jeder Windung!) und uberdies Langs- und
Querwulste, die in nicht allzu geringen Entfernungen
von einander stehen und zwischen sich mikroskopisch
feine, schief gestellte Querstrichelchen erkennen
lassen. Bezuglich jener Spiralreifen sei noch bemerkt,
dass 3 — 4 feine iiber dem stdrkeren mittleren und 1
mittelstarker unter ihm liegen und dass auf der letzten
Windung vom Hauptstreifen abwdrts zur Basis der
Schale 12 schwdchere Spiralreifen vertheilt sind.
Die Kreuzungsstellen der Reifen und Wulste sind
naturgemdfi spitzhockerig vorgezogen. Die Mundung
hat einen vorgezogenen, gewellten Mundrand, eine
tiefe, halbmondfdrmige Bucht rechts oben und einen an

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 24. Pleurotoma nannodes Sturany, 1900, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea, Red Sea). A-E, G. Figured
syntype, NHMW 84254: front (A-B), right side (C-D), back (E), protoconch (G). F. Original figure by Sturany (1903). H. Original
label. Scale bars: A-E: 1 mm, G: 0.2 mm.

der Basis etwas zuruckgebogenen kurzen Canal; an der
Mundungswand ist ein Hockerchen zu sehen.

Die Hohe der Schale betrdgt 5,5, die Breite 2,5 mm die
Mimdung ist circa 2 mm hoch und sehr schmal.

Fiir die systematische Stellung der neuen Art sei Hire
Verwandtschaft mit der dhnlich gestalteten, jedoch viel
grofieren Mangilia spurca Hinds (Moll. Voy. Sulph. p. 17,
t. 5, figure 14) und insbesondere mit Mangilia albata E. A.
Smith aus dem Persischen Golfe (Ann. Mag. Nat. Hist. [5]
X, 1882, p. 210) mafigebend.

Translation. From station 145 (800 m); a single specimen.

The fusiform shell consists of eight whorls, it has
a white colour, small traces of yellow-brown colour

can be noticed especially on the outer lip and on the
protoconch. The protoconch consists of a teat-shaped,
smooth, apex (about one whorl) and two double-keeled
whorls (one rope-like cord in the middle, a second hard¬
ly visible at the suture). The following whorls have a
moderate number of spiral threads, of which regular¬
ly the median is the strongest and the most prominent
(hence the almost rectangular profile of each whorl!)
and also show axial and spiral cords which are not too
far away one from each other and among which it is pos¬
sible to recognize microscopically fine threads. On these
threads, it is remarkable that three or four fine threads
run above the strongest median cord and one below it,
and on the last whorl from the strongest median cord

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Figure 25. Mangiliapertabulata Sturany, 1903, Station 145 (Dahlak Archipelago, Eritrea, Red Sea). A-D, F-G. Holotype, NHMW
84255; front (A-B), right side (C), back (D), protoconch (F), microsculpture (G). E. Original figure by Sturany (1903). Scale bars:
A-D; 1 mm, F-G: 0.2 mm.

to the base of the shell there are 12 weaker spiral rings.
The intersections of the ribs and threads show sharp tu¬
bercles. The aperture has an elongated, undulated lip, a
deep, semi-circular posterior sinus on the top right and
at the base a slightly recurved short canal; a small tuber¬
cle can be seen on the inner lip.

The height of the shell is 5.5 mm, the width 2.5 mm,
the aperture is about 3 mm high and very narrow.

Decisive for the systematic position of the new spe¬
cies is its relationship with the similar, much larger Man¬
gilia spurca Hinds (Moll. Voy. Sulph. p. 17, t. 5, figure
14) and in particular with Mangilia albata E.A. Smith
from the Persian Gulf (Ann. Mag. Nat. Hist. [5] X, 1882,

p. 210).

Comments. The species was assigned to Clathurella
Carpenter, 1857 s.l. by Janssen in Janssen and Taviani
2015: 526.

Family Conidae Fleming, 1822

Conus aculeiformis f. torensis Sturany, 1903

Figure 26

Sturany, 1903; 227, plate IV, figures 8a-b.

Original locality: Station 88 (58 m) (El Tor, Egypt, Red
Sea; Table 1).

Type material. Figured syntype: NHMW 84223 (station
88), illustrated by Sturany (1903) in plate III, figures 2a-c,

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

height 30.7 mm. Further five syntypes NHMW 84224
(station 88).

Original description. Von der Station 88 (58 m); einige
wenige Exemplare.

Das langgestreckte, schlanke Gehduse besteht aus ei-
nem Doppelkegel. Das Gewinde ist erhaben und ziemlich
stufig abgesetzt; von dem glatten und glanzenden Embryo-
nalgewinde, das sich von dem ubrigen Theile des Gewin-
des ziemlich deutlich abhebt, fehlt in der Regel das oberste
Spitzchen (ein Umgang oder mehr). Ungefdhr auf der 3.
Windung beginnt die Sculptur, welche aus einem unter der
Mitte gegen die Naht zu gelegenen, breiten Spiralwulste
und aus 2—2 uber diesem in einem etwas ausgehdhlten
Rdume liegenden schwachen Spiralreifen besteht. Auf der
Schlusswindung, die nach unten in einen langen, schmalen
Kegel endigt, nimmt dann jener starke Spiralwulst den
obersten Theil des Kegels ein und ist er ungefdhr 1 mm von
der Naht entfernt. Der letzte Umgang weist concentrische
Spiralfurchen auf und zwar stehen diese Vertiefungen an
der Basis des Umganges dicht aneinander, dabei defer ein-
schneidend, so doss die dazwischenliegenden Partien als
Spiralrippen erscheinen, wahrend in der Mittelpartie der
Schlusswindung die Spiraleinschnitte weiter voneinander
sich entfernen und seichter sind. Die Basalfurchen sind
mit zahlreichen feinen Querstrichelchen ausgestattet, und
ebenso ziehen uber die einzelnen Umgdnge des Gewindes
zarte Querstriche. Die Farbe des Gehduses ist hellgelb, auf
dem Spiralwulste stehen in ziemlich regelmdfiigen Entfer-
nungen abwechselnd mit Weififdrbung dunkelgelbe oder
gelbbraune Flecken, die sich oft nach oben zu ausdehnen,
und auch in der Mitte der letzten Windung stehen ein paar
Reihen grofierer Flecken nebst den Spuren von kleineren,
radialartig angeordneten. Der Aufienrand der sehr engen,
innen weifi gefdrbten Mundung ist scharf und bildet einen
stark vorgezogenen Bogen, der oben, entsprechend dem
obersten vertieften Theile der Schlusswindung, einen con-
caven Einschnitt trdgt.

Ich halte die eben beschriebene Kegelschnecke fur
eine Localform des C. aculeiformis Rve. (Proc. Zool. Soc.
1843), als dessen Heimat bisher nur die indo-australischen
Gewdsser gegolten haben, und sehe auch in C. sieboldi
Rve. (Jeon. f. 269), C. australis auct. (Tryon, Man. of
Conch. VI, p. 73) und C. (Leptoconus^ saecularis Melvill
(Manch. Mem. XLII, 1898, No. 4, p. 10 des Sep., t. 1, figure
23; aus dem Persischen Golfe) nahverwandte Arten.

Translation. From station 88 (58 m); a few specimens.

The elongated, slender shell consists of a double cone.
The spire is high and fairly scalariform; from the smooth
and shiny protoconch that differs quite clearly from the
other parts of the spire, the upper part of the apex is
missing (one whorl or more). Around the third whorl the
sculpture begins, consisting of a sub-median, broad spiral
cord above the suture and two or three spiral threads in
the concave area above. On the last whorl, ending below
in a long, narrow cone, that strong spiral cord occupies
the topmost part of the cone at about 1 mm distance from

the suture. The body whorl has concentric spiral grooves;
these grooves are tightly arranged and deeply incised at
the base of whorl, so that they seem spiral ribs, while in
the middle section of the last whorl the spiral incisions
are faint and shallow. The basal grooves are equipped
with numerous fine spiral threads, which are also present
on the spire. The colour of the shell is light yellow, on
the spiral ridge dark yellow or yellow-brown flecks alter¬
nate with white colour at fairly regular distances, often
expanding upwards; also in the middle of the last whorl
there are a few rows of larger spots. The lip of the very
narrow, inside white, mouth is sharp and forms a strong
elongated curve which, seen from above, carries a con¬
cave incision at the top.

I think that the described cone snail is a local form of
C. aculeiformis Reeve (Proc. Zool. Soc. 1843), which has
been considered distributed only in the Indo-Australian
waters so far; I consider also closely related species: C.
sieboldi Reeve (Jeon, f 269), C. australis auct. (Tryon,
Man. of Conch. VI, p. 73) and C. (Leptoconus) saecularis
Melvill (Manch. Mem. XLII, 1898, No. 4, p. 10 of Sep¬
tember, t. 1, Fig. 23 from the Persian Gulf).

Comments. This form of Conus aculeiformis Reeve,
1844 is considered a synonym of Conasprella elegans
(G.B. Sowerby III, 1895) (Rockel et al. 1995).

Conusplaniliratus f. batheon Sturany, 1903

Figure 27

Sturany, 1903: 227-228, plate IV, figures 6a-c, 7a-b.

Original localities. Stations 127,128,143,145 (21 - 800 m)
(Eritrea, Red Sea; Table 1).

Type material. Figured syntype: NHMW 84227 (station
143), illustrated by Sturany (1903) in plate III, figures
6a-c, height 35.9 mm. Further syntypes: NHMW 84225
(station 127): 1 specimen, illustrated by Sturany (1903)
in plate IV, figure 7a-b; NHMW 84226 (station 128):
1 specimen; NHMW 84228 (station 143): 5 specimens;
NHMW 84229 (station 145): 2 specimens.

Original description. Von den Stationen 127, 128, 143,
145 (212—800 m).

Das milchglasartige Embryonalgewinde ist glatt, et¬
was glanzend, blasenfdrmig. Auf den darauffolgenden
Windungen ist ein wulstfbrmiger Kiel wahrzunehmen,
der anfangs in der Mitte liegt und einige Mocker trdgt,
dann aber diese letzteren verliert und, sich etwas nach
unten verschiebend, nahtstandig wird. Es erscheint mit-
hin der Umriss des Gewindes stufenformig. Zwischen
dem Hauptwulste (Kiele) und der oberen Naht liegen
3 — 4 schwdehere Langs- oder Spiralreifen. Auf der
Schlusswindung bildet jener Hauptwulst die Kante; der
Theil zwischen der Kante und der Naht ist etwas con-
cav und es entspricht ihm am Mundungsrande oben eine
einschnittartige Aushohlung; die ubrige mdchtige Par-

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Figure 26. Conus aculeiformis var. torensis Sturany, 1903, Station 88 (El Tor, Egypt, Red Sea). A-C. Figured syntype, NHMW
84223: front (A), right side (B), back (C). E-H. Syntype, NHMW 84224: front (E), right side (F), back (G), protoconch (H).
D. Original figure by Sturany (1903). Scale bars: A-C, E-G: 5 mm, H: 0.2 mm.

tie des letzten Umganges trdgt eine grofiere Anzahl von
rippenformigen Spiralreifen (und zwar sind diese gleich
stark in gleichen Zwischenrdumen gelegen oder zwei und
zwei liegen zusammengedrdngt oder es wechseln stdrkere
und schwdchere ab, ganz selten bleiben sie in der ober-
en Partie der Schlusswindung, ungefdhr von der Kante
abwdrts bis zur Hdlfte, aus, indent sich hier blofi seichte
Spiralfurchen votfinden). Die Zeichnung besteht aus dun-

kelgelben Flecken auf hellgelbem oder weifiem Grunde,
die hauptsdchlich auf dem Hauptwulste stehen, sich aber
auch quer iiber die Windungen lagern und auf der letz¬
ten Windung zu zahlreichen, unregelmdfiig gruppierten
Spiralreihen von Flecken anwachsen, von denen wieder
benachbarte verschmelzen konnen. Bei frischen Stucken
ist eine hdutige Epidermis zu finden, die aus quer iiber

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 27. Conus planiliratus var. batheon Sturany, 1903. A-C. Figured syntype, NHMW 84227, Station 143 (Harmil Island,
Dahlak Archipelago, Eritrea, Red Sea); front (A), right side (B), back (C). E-G. Figured syntype, NHMW 84225, Station 127 (Akik
Seghir, Eritrea, Red Sea): front (E), right side (F), back (G). I-L. Syntype, juvenile specimen, NHMW 84228, Station 143 (Harmil
Island, Dahlak Archipelago, Eritrea, Red Sea); front (I), right side (J), back (K), protoconch (L). D, H. Original figures by Sturany
(1903). Scale bars: A-C, E-G; 10 mm, I-K: 5 mm, L: 0.5 mm.

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die Umgdnge streichenden Lamellen besteht und dem
darunterliegenden Kalktheile die Querstreifung mittheilt.

Die Mundung ist eng, innen weifi, scharfrandig.

Es fdllt bei dieser Zusammenstellung auf, dass die Ex-
emplare aus grofieren Tiefen schlanker sind, indent das
Gewinde hoher aufgebaut ist.

Conus planiliratus wurde von Sowerby im Jahre 1870
ohne genaue Angabe eines Fundortes beschrieben (Proc.
Zool. Soc. p. 255, t. XXII, figure 1); nach der Abbildung
zu urtheilen, hatte sein Exemplar die Dimensionen 41 Y 2 :
20: 34 V 2 ,. — E. A. Smith, als Bearbeiter der »lnvesti-
gator«-Mollusken, gibt fur diese Art den Fundort „ Off
Calicut, west coast of South India, in 45 fathoms“ an
und erwdhnt, dass das grofite Exemplar ein Ausmass von
58:27 mm besitzt (Ann. Mag. Nat. Hist. (6) XIV, p. 159
[1894], pi III, fig 2).

Mit Conus sulcatus haben die beschriebenen Exemplare
der »Pola«-Expedition die Berippung des letzten Umgan-
ges gemeinsam, wahrend sie von ihm durch den geraden
Verlauf des Kieles (Wulstes) gut unterschieden sind.

Als nahestehende Form ware schliefilich auch noch
Conus fLeptoconus^ dictator Melvill zu nennen (Manch.
Mem. XLII, 1898, p. 9 des Sep., plate [figure 10), welche
im Persischen Golfe in einer Tiefe von 10 Faden an der
Sheikh Shuaib-Insel in der Grofie von 47: 20 mm ge-
funden wurde.

Translation. From stations 127,128,143,145 (212-800 m).

The milk white protoconch is smooth, slightly glossy,
bubble-shaped. On the following whorls a cord-shaped
keel can be noticed, which is initially in the middle and
bears some tubercules, but then loses these, and moves
towards the suture. The shape of the spire appears there¬
fore scalariform. Between the main cord (keels) and the
upper suture three to four weaker longitudinal or spiral
threads run. On the last whorl, that main cord forms the
keel; the part between the keel and the suture is slightly
concave, and it corresponds to a notch-like cavity on the
upper part of the lip; the rest of this massive part carries a
greater number of rib-shaped spiral cords (they are equal¬
ly spaced, or they are clustered in pairs, or they are alter¬
nately strong and weak; very rarely they are absent on the
upper part of the last whorl, roughly from the keel down
to the middle, here fine spiral threads can be found). The
pattern consists of dark yellow patches on light yellow or
white ground, these patches are mainly on the main band,
but also lay across the whorls and grow on the last whorl
to become numerous, irregularly clustered spiral rows of
spots, sometimes merging again. On fresh specimens, a
membranous periostracum can be found with transverse
lamellae crossing the whorls and overlaying on the trans¬
verse threads on the underlying calcareous shell.

The aperture is narrow, white inside, with a sharp lip.

It is remarkable that specimens from greater depths are
slimmer with a higher spire.

Conus planiliratus was described by Sowerby in 1870
without specifying a precise locality (Proc. Soc. Zool. p.
255, t. XXII, figure 1); judging from the figure, his speci¬

men had the dimensions 41.5 : 20 : 34.5 [mm]. In his de¬
scription of the “Investigator” mollusks, E.A. Smith gives
for this species the location “off Calicut, West Coast of
South India, in 45 fathoms” and noted that the largest
specimen had a size of 58 : 27 mm (Ann. Mag. Nat. Hist.
(6) XIV, p. 159 [1894], pi. Ill, figure 2). The described
specimens of the “Pola” expedition share with Conus sul¬
catus the ribbing of the last whorl, while they can be well
distinguished by the straight direction of the keel.

Finally, the closely related form Conus (Leptoconus)
dictator Melvill can be mentioned (Manch. Mem. XLII,
1898, p. 9 of September, plate 1, figure 10), which was
found in the Persian Gulf at a depth of 10 fathoms along
Sheikh Shuaib Island with the size of 47 : 20 mm.

Comments. The syntype illustrated in Figure 27E-G has
a distinctly heavier and ticker shell than the one illustrat¬
ed in Figure 27A-C. Recent authors do not recognize
the validity of this taxon (Rockel et al. 1995; Tucker and
Tenorio 2013), but disagree on to which taxon this Co¬
nus should be synonymized to: Rockel et al. 1995 sug¬
gested Conus grangeri G.B. Sowerby III, 1900, whereas
Bouchet (2015) lists it as synonym of Conus inscriptus
Reeve, 1843.

Family Raphitomidae A. Bellardi, 1875
IPleurotoma beblammena Sturany, 1903

Figure 28

Sturany, 1903: 231, plate III, figures 4a-b.

Type locality. Station 143, “nachst der Insel Harmil”
[near Harmil Island, Dahlak Archipelago, Eritrea]

17°7'N, 39°55'E, 212 m.

Type material. Holotype: NHMW 84256, height 9.2 mm.

Original description. Von der Station 143 (212 m); eine
unvollstandige Schale.

Die milchweifie, durchscheinende Schale ist spindelfbr-
mig gebaut und besteht aus 8 Umgdngen; die Mundung
ist nicht vollstandig ausgebildet. Das Embryonalgewinde
besteht aus kaum 2 Umgdngen, die zwar glatt erscheinen,
bei starker Vergrdfierung jedoch eine feine Gittersculptur
erkennen lassen. Die folgenden 4 — 5 Umgdnge besitzen
3 Starke Spiralwulste, von denen der mittlere am meisten
hervortritt, und uberdies in den Zwischenrdumen noch
je einen schwachen Spiralreifen. Durch ziemlich engste-
hende, etwas bogig verlaufende Querwulste wird eine
Durchkreuzung der Spiralsculptur, mithin eine Cancel-
lierung des Gehduses hervorgerufen. Auf der vorletzten
Windung treten zu den erwdhnten Spiralwulsten noch 2
feinere Spiralreifen unten ndchst der Naht; auf dem letz¬
ten Umgange verlaufen viele solche Spiralreifen in dem
Raume zwischen der Einlenkung des Mundsaumes und der
Basis des Gehduses, ein Abwechseln von stdrkeren Spiral¬
wulsten und zarteren Spiralreifen ist hier schon weniger
deutlich erkennbar. Die Spindelgegend ist abgegldttet, die
Basis der Spindel ist gedreht und etwas zuriickgebogen.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 28. Pleurotoma bebJammena Sturany, 1903, Station 143 (Harmil Island, Dahlak Archipelago, Eritrea, Red Sea). A. Original
figure by Sturany (1903). B-F. Holotype, NHMW 84256: front (B-C), right side (D), back (E), protoconch (F). Scale bars; B-E; 2
mm, F: 0.1 mm.

Die Hohe der Schale betrdgt 9,7, die Breite 3,6 mm.

Die systematische Stellung der beschriebenen Form
ist im Hinblick auf die mangelhaft erhaltene Mundung
problematisch.

Translation. From station 143 (212 m); an incomplete shell.

The milk-white, translucent shell is fusiform and con¬
sists of eight whorls; the aperture is incomplete. The
protoconch consists of barely two whorls, which seem
smooth, but seen under high magnification show a fine
cancellated sculpture. The following four-five whorls
show three strong spiral ridges with the median one most
prominent, and in each interstice a weak spiral thread. The
spiral sculpture is crossed by particularly narrow, slightly
curved axial cords which cause a cancellated sculpture of
the shell. On the last whorl, between the mentioned spiral
cords two more finer spiral threads are visible below the
suture; on the last whorl many spiral threads continue be¬
tween the [inner] lip and the base of the shell; here, an al¬
ternation of stronger and finer spiral threads is indistinct.

The columellar area is smooth, the base of the columella
is twisted and slightly recurved.

The height of the shell is 9.7 mm, the width 3.6 mm.
The systematic position of the described form is prob¬
lematic because of the poor condition of the aperture.

Comments. A further member of the genus Taranidaph-
ne Morassi & Bonfitto, 2001.

Clathurella dichroma Sturany, 1903

Figure 29

Sturany, 1903: 252, plate V, figures 5a-b.

Original locality: Locality 25, “Sherm Sheikh (Mersa
Sheikh)” [near Abu Ghusun, Egypt], 26°- 24°N.

Type material. Two syntypes: NHMW 37717 (locality
25), the specimen figured by Sturany (1903), plate V, fig¬
ures 5a-b has been segregated, its height is 4 mm.

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Figure 29. Clathurella dichroma Sturany, 1903, Locality 25 (Abu Ghusun, Egypt, Red Sea). A-D, F, H. Figured syntype, NHMW
31111'. front (A-B), right side (C), back (D), microsculpture (F), protoconch (H). E. Original figure by Sturany (1903). G. Original
label. Scale bars; A-D: 0.5 mm, F, H: 0.1 mm.

Original description. Von der Localitdt 25.

Die neue Art, blofi in 2 Exemplaren vorliegend, hat
grofie Ahnlichkeit und Verwandtschaft mit C. rubro-
guttata JA. Ad. (nach Tryon einem Synonym von tincta
Rve.). Die Schale besteht aus 8 Windungen, von denen
die 3 ersten einen braunen Apex bilden; auf den Apex
folgt ein Umgang in weifier Farbe, auf diesen erst die
mit dunkel- oder rothbrauner Fdrbung gezierte Ge-
hdusepartie. Fs sind hier die Knoten, welche die 3
Langs- (Spiral-) rippen mit den Querwulsten an den
Kreuzungsstellen bilden, abwechselnd weifi und roth-
braun gefdrbt. Der dufiere Mundrand trdgt oben einen

Finschnitt. Die Hohe der Schale betrdgt kaum 4 mm,
die Breite 1,7 mm, die Mundung ist nicht halb so hoch
wie das ganze Gehduse.

Translation. From locality 25.

The new species, present only in two specimens, has
great similarity and relationship with C. rubroguttata H.
Adams (according to Tryon a synonym of tincta Reeve).
The shell consists of eight whorls, of which the first
three form a brown apex; the apex is followed by a white
coloured whorl, then the dark or reddish-brown colour¬
ing on part of the shell follows. Here there are tubercles.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 30. Mangelia epicharis Sturany, 1903, Locality 16 (Jazirat Shakir, Egypt, Red Sea). A-D, F, H. Holotype, NHMW 37714:
front (A-B), right side (C), back (D), microsculpture (F), protoconch (H). E. Original figure by Sturany (1903). G. Original holo¬
type label. Scale bars; A-D: 0.5 mm, F; 0.2 mm, H; 0.1 mm.

formed by the intersection of three longitudinal (spiral)
cords with the axial ribs, coloured alternatively white and
reddish-brown. The outer lip bears an incision above. The
height of the shell is barely 4 mm, width 1.7 mm, the
mouth has less than half of the shell height.

Comments. This species clearly belongs to the genus
Pseudodaphnella Boettger, 1895 (Fedosov and Puillandre
2012). It is very closely related to Pseudodaphnella
barnardi (Brazier, 1876) and P. phaeogranulata Fedosov
& Puillandre, 2012.

Mangilia (Glyphostoma) epicharis Sturany, 1903

Figure 30

Sturany, 1903: 251, plate VII, figures 2a-b.

Type locality. Locality 16, “Shadwan-Insel” [Jazirat Sha¬
kir, Egypt], Northern Red Sea, 28°- 26°N.

Type material. Holotype: NHMW 37714, height 4.2 mm.

Original description. Von der Localitdt 16.

Das einzige Exemplar, welches zur Aufstellung der
neuen Art Anlass gegeben hat, besitzt eine grofie Ahn-

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ft f

. . Jill I

• iit

AyCt£cL^'^0rtAt^ ^

^ Si ^

fcj. 1 '. •■5Li(. I’uiji i. ti. Itufce .Ueer ioh>.»-ti u. l8H7~8

jgg.j^teifldacJmex et ^i^lieArocif*

Figure 31. Elusa halaibensis Sturany, 1903, Locality 30 (Halayeb, Egypt, Red Sea). A. Original figure by Sturany (1903). B-F. Holo-
type, NHMW 37815; front (B-C), right side (D), back (E), protoconch (F). G. Original holotype label. Scale bars; B-E; 2 mm, F; 1 mm.

lichkeit mit Glyphostoma melanoxytum Herv. von Lifou
(Journ. de Conch. XLIV, 1896, p. 78, t. 3, figure 19). Die
Fdrbung, das Embryonalgewinde und die Grofie der Her-
vier ’schen Art stimmt, wie ich mich im Berliner Museum
an einem typischen Exemplar uberzeugen konnte, mit den
entsprechenden Verhdltnissen der neuen Art vollstdn-
dig uberein, hingegen bildet das tiefe Einschneiden der
Windungen, also die tiefgelegene Naht bei G. melanoxy¬
tum ein wesentliches Unterscheidungsmerkmal. Das aus
4 Umgdngen bestehende Embryonalgewinde ist eine dem
ubrigen Gewinde gewissermafien aufgesetzte Mutze von
gelber bis brauner Earbe. Die beiden ersten heller gefdr-
bten Umgdnge sind nur scheinbar glatt, denn sie weisen,
unter dem Mikroskope betrachtet, eine feinste Punkti-
erung auf; auf sie folgen braunfdrbige Umgdnge mit ein-
er aus schief gekreuzten Linien gebildeten Gittersculptur.
Die nun folgenden 4 Hauptwindungen sind stufig abge-
setzt, mit Spiral- und Querwulsten ausgestattet, weifi
in der Grundfarbe und mit unregelmdfiig verlaufenden
braunen Quer- und Spirallinien geziert. Das ganze Ge-
hduse ist 4,6 mm hoch und 2 mm breit.

Translation. From locality 16.

The only specimen available from this new species has
a great similarity with Glyphostoma melanoxytum Her-
vier from Lifou (Journ. de Conch. XLIV, 1896, p. 78, t.
3, Fig. 19). The colour, the protoconch and the size of
Hervier’s species are identical to the newly described
species, as I was able to study type specimens in the Mu¬
seum in Berlin, but the deep incision of the whorls and
therefore the deep suture of G. melanoxytum is a signifi¬
cant distinguishing feature. The protoconch, consisting of
four whorls, is put like a yellow to brown cap on the spire.
The first two lighter coloured whorls are only apparently
smooth: viewed under the microscope, they show a fine
dotting; then brown coloured whorls follow with oblique¬
ly crossed lines forming a cancellated sculpture. The
following four main whorls are scalariform with spiral
ridges and varices, white in colour and decorated with
irregularly brown transverse and spiral lines. The entire
shell is 4.6 mm high and 2 mm wide.

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 32. Syrnola trivittata Sturany, 1903 (Bitter Lakes, Suez Canal). A-E, J. Figured syntype, NHMW 37814; front (A-B),
right side (C-D), back (E), protoconch (J). F-H. Syntype, NFIMW 37814: front (F), right side (G), back (H). I. Original figure by
Sturany (1903). K. Original label. Scale bars: A-H; 1 mm, J; 0.1 mm.

Family Pyramidellidae A. Adams, 1860
Elusa halaibensis Sturany, 1903

Figure 31

Sturany, 1903: 259, plate VI, figures 1 la-b.

Type locality. Locality 30, “Mersa Halaib” [Halayeb,
Egypt], 24°-22°N.

Type material. Holotype: NHMW 37815, height 12.2 mm.

Original description. Von der Localitdt 30: eine einzige
Schale.

Von der langgestreckten Schale sind 11 langsam
anwachsende Umgdnge erhalten, das Spitzchen fehlt.
Unregelmdfiig angeordnete Flecken von brauner bis vio-
letter Farbe, welche wohl aus aufgeldsten Spiralbinden

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Zoosyst. Evol. 93 (1) 2017, 45-94

hervorgegangen sind, finden sich uber das Gehduse
verbreitet, die violette Farbe ist besonders auf dem
letzten Umgange ausgeprdgt. Das ganze Gehduse misst
12 mm in der Hohe, 3,7 mm in der Breite, die Mundung
ist sehr schmal und 3,5 mm hoch; die Spindel ist mit einer
grofieren Falte und 2 ganz kleinen unter dieser gelegenen
Falten besetzt.

Die neue Art ist mit E. bmnneo-maculata Melv. (Mem.
Proc. Manch. Lit. et Philos. Soc. 1896/97, p. 13, plate 6,
figure 5) nahe verwandt.

Translation. From location 30: a single shell.

Elongated shell, with 11 slowly growing whorls, the
apex is missing. Irregularly arranged flammules of brown
to violet in eolour are found spread throughout the whole
shell and probably derive from a dissolved spiral band, the
purple colour is particularly prominent on the last whorl.
The whole shell measures 12 mm in height, 3.7 mm in
width, the mouth is very narrow and 3.5 mm high; the col¬
umella has one larger fold and two smaller ones below it.

The new species is closely related to E. brunneo-
maculata Melvill (Mem. Proe. Manch. Eit. et Philos. Soc.
1896-97, p. 13, plate 6, figure 5.

Syrnola trivittata Stnrany, 1903

Figure 32

Sturany, 1903: 259, plate VII, figures 8a-b.

Original locality: Bitter Fakes in the Suez Canal.

Type material. Two syntypes: NHMW 37814 (Bitter
Fakes), the speeimen figured by Sturany (1903), plate VII,
figures 8a-b has been segregated, its height is 5.2 mm.

Original description. 2 Exemplare aus dem Bittersee im
Suezcanale.

Das abgebildete Gehduse ist 5 V 2 mm hoch und 1 V 2 mm
breit und besteht aus 10flachen Umgdngen. DieAnfangs-
windungen sind glashell und geben dem Gehduse einen
kugeligen Abschluss nach oben; die darauffolgenden
Umgdnge haben eine gelblichgrune Binde auf weifiem
Grunde, der besonders oben gegen die Naht zu binden-
fbrmig hervortritt (die Naht sieht hier fadenfbrmig aus);
noch weiter nach unten treten 2, auf der Schlusswindung
sogar 3 Spiralbinden von der genannten Fdrbung auf.
Die Mundung ist ungefdhr 1 mm hoch und trdgt eine
schwache Falte auf der Spindel.

Das zweite Exemplar misst 6.2 mm hat 11 Umgdnge
und undeutliche Spiralbinden.

Die besprochene Form ist am ehesten mit S. tineta
Ang. (Australien) zu vergleichen, die ich am Berliner Mu¬
seum zu sehen Gelegenheit hatte.

Translation. Two specimens from the Bitter Fake in the
Suez Canal.

The figured shell is 5.5 mm high and 1.5 mm wide
and consists of 10 flat whorls. The protoconch is crys¬
tal clear and give the shell a globular completion on top;
the subsequent whorls have a yellowish green band on
white baekground, such white background is particularly
visible as a band close to the suture (the suture seems
filiform); further down the shell, two, on the last whorl
even three, spiral bands of the mentioned eolour appear.
The aperture is approximately 1 mm high and has a light
fold on the columella.

The second specimen is 6.2 mm and it has 11 whorls
and indistinet spiral bands.

The described form is compared best with S. tineta
Angus (Australia), which I had the opportunity to see at
the Berlin Museum.

Family Haminoeidae Pilsbry, 1895
Atys (Roxania) lithensis Sturany, 1903

Figure 33

Sturany, 1903: 235, plate VI, figures 2a-b.

Type locality. Station 114, “zwischen Suakim und Fith”
[between Suakin, Sudan, and A1 Fith, Saudi Arabia],
19°38'N, 37°55'E, 535 m.

Type material. Holotype: NHMW 84291, height 12.2 mm.

Original description. Von der Station 114 (535m); ein
einziges Exemplar.

Das kleine, weifie Gehduse, dessen Gewinde eingesenkt
ist, so dass eigentlich nur der letzte Umgang frei bleibt,
ist stichfdrmig genabelt und besitzt zahlreiche, spiral an-
geordnete Reihen von Punktehen. Die Mundung uberragt
oben ein wenig die Ebene des Gewindes und hat eine
Hohe von 3 V 2 mm die Breite der Schale betrdgt 2 V 2 mm.

In Gestalt und Sculptur erinnert diese Conchylie leb-
haft an die mediterrane Atys (Roxania) utriculus Brocchi
einerseits und an die japanische A. (Roxania) punctulata
A. Ad. anderseits, aber auch mit Cyliehna noronyensis
Watson kdnnte sie verwandt sein.

Translation. From station 114 (535m); a single specimen.

Small white shell, the spire is sunk so that only the last
whorl is visible, the umbilicus is stitch-shaped and has
numerous, spirally arranged rows of dots. The aperture
reaches slightly above the spire and has a height of 3.5
mm, the width of the shell is 2.5 mm.

In shape and sculpture this shell vividly resembles
on one hand the mediterranean Atys {Roxania) utricu¬
lus Brocchi, on the other hand the Japanese A. {Roxania)
punctulata A. Adams, but may also be related to Cyliehna
noronyensis Watson.

Comments. This species was assigned to Roxania by
Dekker and Orlin (2000: 34) and Janssen in Janssen and
Taviani (2015: 527).

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Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Figure 33. Atys lithensis Sturany, 1903, Station 144 (between Suakin, Sudan, Al Lith, Saudi Arabia, Red Sea). A. Original figure by
Sturany (1903). B-H. Holotype, NHMW 84291: front (B-C), right side (D-E), back (F), microsculpture (G-H). Scale bars: B-F; 0.5 mm,
G-H; 0.25 mm.

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Zoosyst. Evol. 93 (1) 2017, 45-94

Acknowledgments

We wish to thank Helmut Sattmann, Head of the
Zoological Department of the Natural History Museum
in Vienna, who allowed access and work on Sturany’s
types. Dan Topa helped during SEM imaging and Nesrine
Akkari gave assistance on the use of the light microscope.
Christine Zom, Natural History Museum in Berlin,
provided information on Stylifer thielei. Antonio Bonfitto,
Alexander Fedosov, Daniel Geiger, David Herbert, Alan
Kohn, Mauro Morassi, and Anders Waren contributed to
the text by writing comments or providing information
on the taxonomy of many Sturany’s taxa. Wolfgang
Brunnbauer, librarian of the Zoological Library of the
Natural History Museum in Vienna, helped tracing the
editions of Sturany’s works.

References

Adensamer W (1935a) Hofrat Dr. Rudolf Sturany. Bin Nachmf (mit
einem vollstandigen Verzeichnis seiner Arbeiten). Archiv fur Mol-
luskenkunde 67: 113-120.

Adensamer W (1935b) Nachrufe. Zum Gedachtnis an Hofrat Dr. Ru¬
dolf Sturany (mit einem vollstandigen Verzeichnis seiner Arbeiten).
Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien
85; 145-149.

Adensamer W (1935c) Necrologie, R. Sturany - In Memoriam. Journal
de Conchyliologie 79; 85-90.

Born I, von (1778) Index Rerum Naturalium Musei Cssarei Vindobon-
ensis. Pars I.ma. Testacea. VerzeichniB der nattirlichen Seltenheiten
des k. k. Naturalien Cabinets zu Wien. Erster Theil. Schalthiere.
Kraus, Vindobon® (Vienna), [1-40], 1-458, [1-82],
von Born I (1780) Testacea Musei Cssarei Vindobonensis, qu$ jussu
Maris Theresis Augusts disposuit et descripsit. Kraus, Vindobons
(Vienna), [I-XXXVI], 1-442, [1-18].

Bouchet P (2015) Conus planiliratus var. batheon Sturany, 1904.
In: MolluscaBase (2015). World Register of Marine Species.
http://www.marinespecies.org/aphia.php/aphia.php?p=taxde-
tails&id=224074 [2016-11-02]

Bouchet P, Rocroi J-P (Eds) (2005) Classification and nomenclator of
gastropod families. Malacologia 47(1-2): 1-397.

Bouchet P, Kantor YI, Sysoev A, Puillandre N (2011) A new operation¬
al classification of the Conoidea (Gastropoda). Journal of Molluscan
Studies 77; 273-308. https://doi.org/10.1093/mollus/eyr017
Broderip WJ (1832) In Sowerby GB (1821-34). The genera of fossil and
recent shells. Eondon.

Cernohorsky W (1976) The Mitridae of the world. Part I. The subfamily
Mitrinae. Indo-Pacific Mollusca 3(17): 273-528.

Cernohorsky W (1984) Systematics of the family Nassariidae (Mollu¬
sca; Gastropoda). Bulletin of the Auckland Institute and Museum
14: 1-356.

Dekker H, Orlin Z (2000) Check-list of Red Sea Mollusca. Spirula
47(suppl.): 3-46.

Eschner A (2005) Vom Sammeln zur wissenschaftlichen Sammlung -
Das Meer im Zimmer - Von Tintenschnecken und Muscheltieren.
Eandesmuseum Joanneum und Elisabeth Schlebrtlgge, Graz, 39-43.

Eschner A (2008) Georg von Frauenfeld: Die Bedeutung seiner Arbei¬
ten fur die Malakologic. Annalen des Naturhistorischen Museums in
Wien, SerieB 109: 15-31.

Fedosov AE, Puillandre N (2012) Phylogeny and taxonomy of the
Kermia - Pseudodaphnella (Mollusca: Gastropoda; Raphitomi-
dae) genus complex: a remarkable radiation via diversification of
larval development. Systematics and Biodiversity 10(4): 447-477.

Herbert DG (1987) Taxonomic studies on the Emarginulinae (Mollu¬
sca; Gastropoda: Fissurellidae) of southern Africa and Mozambique.
Hemitonia, Clypidina, Tugali, Scutus, Zeidora and two species of
Emarginula. South African Journal of Zoology 22(1): 1-13. https://
doi.org/10.1080/02541858.1987.11448013

Herbert DG (1992) Revision of the Umboniinae (Mollusca; Proso-
branchia: Trochidae) in southern Africa and Mozambique. Annals
of the Natal Museum 33(2): 379-459.

Herbert DG (1996) Observations on Clanculus tonnerrei (G. & H. Nev-
ill, 1874) (Mollusca Gastropoda Trochidae). Tropical Zoology 9;
31-45. https://doi.Org/10.1080/03946975.1996.10539301

ICZN (1999) International Code of Zoological Nomenclature. The In¬
ternational Trust for Zoological Nomenclature, 306 pp.

Janssen R, Taviani M (2015) Taxonomic, ecological and historical
considerations on the deep-water benthic mollusc fauna of the Red
Sea. In; Rasul NMA, Stewart ICE (Eds) The Red Sea. Springer,
Berlin & Heidelberg, 511-529. https://doi.org/10.1007/978-3-662-
45201-1_29

Rbckel D, Korn W, Kohn AJ (1995) Manual of the living Conidae -
Volume 1: Indo-Pacific region. Verlag Christa Hemmen, Wies¬
baden, 517 pp.

Schefbeck G (1996) The Austro-Hungarian Deep-sea Expeditions.
In: Uiblein F, Ott J, Stachowitsch M (Eds) Deep-sea and extreme
shallow-water habitats: affinities and adaptations. Osterreichische
Akademie der Wissenschaften, Biosystematics and Ecology Series
11: 1-27.

Snyder MA (2002) Fusinus dovpeledi, a new species (Gastropoda: Fa-
sciolariidae) from the Red Sea, and range extension for two other
species. The Nautilus 116(2): 56-58.

Stagl V (2012) Sturany, Rudolf (1867-1935), Zoologe. Osterreichisches
Biographisches Eexikon 1815-1950 14(63): 11.

Stagl V, Sattmann H, Dworschak PC (1996) The material of the Pola
Red Sea expeditions (1895-1898) in the collections of the Natural
History Museum in Vienna. Osterreichische Akademie der Wissen¬
schaften, Biosystematics and Ecology Series 11: 29-41.

Sturany R (1896) Berichte der Commission ftlr Tiefsee-Forschungen.
XVIII. Zoologische Ergebnisse. VIE Mollusken I (Prosobranchier
und Opisthobranchier; Scaphopoden; Eamellibranchier) gesammelt
von S.M. Schilf“Pola” 1890-1894. Denkschriften der Kaiserlichen
Akademie der Wissenschaften, Mathematisch-Naturwissenschaftli-
che Classe 63: 1-36.

Sturany R (1899) Expedition S.M. Schitf “Pola” in das Rothe Meer,
nbrdliche und stidliche Halfte. 1875/96 - 1897/98. Zoologis¬
che Ergebnisse XIV. Eamellibranchiaten des Rothen Meeres.
Denkschriften der Kaiserlichen Akademie der Wissenschaften,
Mathematisch-Naturwissenschaftliche Classe 69: 255-295. [Pre¬
print: p. 1-41]

Sturany R (1900a) Diagnosen neuer Gastropoden aus dem Rothen
Meere als Vorlaufer einer Bearbeitung der gesammten, von S. M.
Schitf “Pola” gefundenen Gastropoden. Anzeiger der Kaiserlichen

zse.pensoft.net

Albano, RG. et al.: Types of Sturany’s Red Sea gastropods

Akademie der Wissenschaften, Mathematisch-Naturwissenschaftli-
cheClasse 17; 197-201.

Sturany R (1900b) Diagnosen neuer Gastropoden aus dem Rothen
Meere als Vorlaufer einer Bearbeitung der gesammten von S. M.
Schiff “Pola” gefundenen Gastropoden (Fortsetzung). Anzeiger der
Kaiserlichen Akademie der Wissenschaften, Mathematisch-Natur-
wissenschaftliche Classe 18: 208-212.

Sturany R (1903) Expeditionen S.M. Schiff “Pola” in das Rothe Meer,
nbrdliche und sildliche Halfte, 1895/96 - 1897/98. Zoologische
Ergebnisse XXIII. Gastropoden des Rothen Meeres. Denkschrif-
ten der Kaiserlichen Akademie der Wissenschaften, Mathema-
tisch-Naturwissenschaftliche Classe 74: 210-283. [Preprint p. 1-75]

Tucker JK (2004) Catalog of recent and fossil turrids (Mollusca; Gas¬
tropoda). Zootaxa682: 1-1295.

Tucker JK, Tenorio MJ (2013) Illustrated catalog of the living cone
shells. MdM Publishing, Wellington, Florida, 517 pp.

Vinarski MV, Eschner A (2016) Examination of the type material of
freshwater mollusk species described by J.P.R. Drapamaud. An-
nalen des Naturhistorischen Museums in Wien, Serie B 118: 29-53.

Waren A (1981) Revision of the genera Apicalia A. Adams and Stila-
pex Iredale and description of two new genera (Mollusca, Proso-
branchia, Eulimidae). Zoologica Scripta 10; 133-154.

Waren A (1984) A generic revision of the family Eulimidae (Gastropoda,
Prosobranchia). Journal of Molluscan Studies 49(suppl 13): 1-96.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 95-104 | DOI 10.3897/zse.93.10794

4>yEnsPFr.

museum fur naturkunde

Diversity and taxonomy of Vietnamese Pollicaria
(Gastropoda, Pupinidae)

Russell L. Minton^ Phillip M. Harris^, Ernest North\ Do Van Tu^

1 Division of Natural Sciences, University of Houston Clear Lake, 2700 Bay Area Boulevard MC 39, Houston, Texas 77058 USA

2 Department of Biological Sciences, University of Alabama, Box 870345, Tuscaloosa, Alabama 35487 USA

3 Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Nghia Do, Can Gidy, Ha Noi, Vietnam

http://zoobank.org/07186867-987F-4661-894D-359FE9B5B4CF
Corresponding author; Russell L. Minton (minton@uhcl.edu)

Received 4 November 2016
Accepted 6 January 2017
Published 3 February 2017

Academic editor:

Matthias Glaubrecht

Key Words

Pollicaria rochehruni
Pollicaria crossei
Pollicaria mouhoti
Vietnam
pupinid

Abstract

Species in the genus Pollicaria (Gastropoda; Pupinidae) are conspicuous members of
the southeast Asian land snail fauna. Originally erected in 1856, both the genus and its
constituent species have been reorganized multiple times with the most recent treatment
published in 2013. Collections of Vietnamese Pollicaria during 2014 and 2015 raised
questions of the utility of currently used diagnostic shell characters and identification
keys in species identification. An examination of the authors’ collections, combined with
museum specimens, suggested that at least three species of Pollicaria occur or have his¬
torically occurred in Vietnam. It is suggested that P. rochehruni is a senior synonym of
P. crossei and treat both taxa as conspecific. A second species, P. mouhoti, was believed
to only occur in Cambodia, Laos, and Thailand. A possible third species, based only on
previous karyotypic work, is discussed. Our data further suggest that shell features such
as color and size lack consistent utility in species-level identifications in Pollicaria.

Introduction

The genus Pollicaria was erected by Gould (1856) to in¬
clude large pupinid snails of southeastern Asia possessing
the following characters: a thick ovate shell, distorted and
flattened in the adult; a circular aperture; and an internal
shoulder or groove inside the palatal edge of the peristome
(Pain 1974). The taxonomy and systematics of Pollicaria
have remained in flux for many years. At the same time
he erected the genus, Gould (1856) described Cyclostoma
pollex Gould, 1856 and made it the type species of Pol¬
licaria. Benson (1859) erected the genus Hybocystis with
Megalomastoma gravidum Benson, 1856 from Burma as
the type species, recognizing that C. pollex was synony¬
mous with the previously described M. gravidum. Haines
described C. myersii Haines, 1858 from Siam, and three
more species were described in Hybocystis: H mouhoti
Pfeiffer, 1862 from the Lao Mountains of Cambodia; and
H. elephas deMorgan, 1885 and//, jousseaumi deMorgan,

1885 from the Perak region of Malaysia. Benson (1860)
recognized that Hybocystis was a junior synonym of Pol¬
licaria, but the former name remained in use until Pain’s
(1974) revision. Crosse (1885) revised Hybocystis into
two sections, one with H elephas and its junior synonym
H jousseaumi and the other with H. gravida, H mouhoti,
and H. myersii. In 1887, two species of Hybocystis were
described from Tonkin (northern Vietnam), H. rochehruni
Mabille, 1887 and H. crossei Dautzenberg & d’Hammon-
ville, 1887. Dautzenberg and Fischer (1905) equated H
rochehruni and H crossei with H gravida, indicating that
any shell differences between species were not consistent
but rather existed in a continuum between extremes.

Pain (1974) revised the then six nominal Pollicaria
species into three based on shell morphology: P. gravida,
including P. rochehruni and P. crossei, P. elephas', and
P. myersii, including its junior synonym P. mouhoti.
Kongim et al. (2010) provided karyotype analyses
for P. gravida, P. elephas, and P. myersii, along with

Copyright Russell L. Minton etal. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

Minton, R.L. et al.: Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

P. mouhoti as a separate species. They found karyotype
differences between all four species and found two distinct
karyotypes in Vietnamese P. gravida, their “big brown
shell” and “small orange shell” samples differed in the
centromere position of one chromosome pair (Kongim
et al. 2010:127). However, they did not karyotype any
topotypic P. gravida from Burma. Most recently, Kongim
et al. (2013) reassessed Pollicaria using a combination of
shell, radula, and reproductive characters and recognized
six separate species: P. gravida, P. myersii, P. mouhoti,
P. elephas, P. rochebruni, and P. crossei. They correctly
recognized that not all Pollicaria possess the shouldering
inside the peristome, and assigned the different karyotypes
of Vietnamese P. gravida (Kongim et al. 2010) to
P. rochebruni (“big brown shell”) and P. crossei (“small
orange shell”). The two species were diagnosed in their
key based on shell size and color; P. rochebruni is large
(>40 mm) with a brownish shell, while P. crossei is small
(<35 mm) with a bright orange shell (Kongim et al. 2013).
Both species are thus separate from the small yellow-
shelled P. gravida from Burma. Kongim et al. (2013) also
provided revised distributions for all species and figured
type and additional material.

While identifying Vietnamese land snails collected in
2015 by PMH and DVT, we found Kongim et al. (2013) to be
problematic in identifying specimens of P. rochebruni and
P. crossei. We noted specifically that smaller (30-35 mm)
reddish-brown shells and larger (35-40 mm) orange shells
were left unidentifiable by the key, and that species-spe¬
cific characters of the key conflicted with the comparative
characters listed by Kongim et al. (2013:28). Of additional
interest were records of putative P. mouhoti from Lao Cai,
Vietnam (Solem 1966), a species that Kongim et al. (2013)
had restricted to Cambodia, Laos, and Thailand, and inter¬
net references to additional species in northeast Vietnam
and southern China. In an effort to resolve the taxonomic
and distribution issues presented by Kongim et al. (2013),
we undertook a morphological and molecular examination
of Vietnamese Pollicaria specimens, along with original
descriptions and other literature relevant to the genus, to
address two research questions. First, are P. rochebruni and
P. crossei separate valid species? Second, beyond those
specimens listed in Solem (1966), is there evidence of ad¬
ditional Pollicaria species in Vietnam?

Materials and methods

Specimens collected by the authors were vouchered at
the Carnegie Museum of Natural History (CM), Phila¬
delphia, Pennsylvania. Collection data for Vietnamese
Pollicaria came from the following museums: Chu-
lalongkorn University, Museum of Zoology, Bangkok,
Thailand (CUMZ); Museum of Comparative Zoology,
Harvard University, Cambridge, Massachusetts (MCZ);
Florida Museum of Natural History, University of Flor¬
ida, Gainesville, Florida (FLMNH); Museum National
d’Histoire Naturelle, Paris, France (MNHN), Royal Bel¬

gian Institute of Natural Sciences (RBINS), and National
Museum of Natural History, Smithsonian Institute, Wash¬
ington D.C. (USNM). Specimens from MNHN, CUMZ,
and RBINS were not made available, so we treated the
identifications and locality data given in Kongim et al.
(2013) as correct. All Vietnamese Pollicaria holdings
from FLMNH, MCZ, and USNM were borrowed, identi¬
fied by the authors based on Kongim et al. (2013), latitude
and longitude coordinates estimated, and mapped with
DIVA-GIS (Hijmans et al. 2008).

We also searched the Internet for shell dealers selling
Pollicaria specimens from Vietnam and surrounding ar¬
eas. While we lacked the funding to purchase specimens
outright, we examined shell images and locality infor¬
mation from the dealer websites. Requests to formally
include images and additional information in this manu¬
script went unanswered. We accepted that this informa¬
tion was not equivalent to that of vouchered specimens,
but could be important in determining the diversity and
distribution (Turney et al. 2015) of Pollicaria species.

Live Pollicaria specimens were collected in Vietnam by
PMH, DVT, and local farmers in 2015, preserved in ethanol,
and DNA was successfully sequenced from two of them. One
individual collected south of Hoang Lien National Park had a
reddish-brown shell we identified as P. rochebruni, the other
was collected from Cue Phuong National Park and had an or¬
ange shell that was consistent with P. crossei sensu Kongim
et al. (2013). Using foot tissue we followed a standard CTAB
and phenol/chloroform DNA extraction method (Saghai-Ma-
roof et al. 1984), then amplified one mitochondrial (16S) and
two nuclear (18S and 28S) gene fragments by PCR. Amplifi¬
cation conditions were the same for all fragments and includ¬
ed an initial denaturing step (94°C for 120 s), 30 cycles (94°C
for 60 s, 50°C for 60 s, 72°C for 120 s), and a final extension
step (72°C for 10 minutes). We employed the following prim¬
er pairs: 16Sar and 16Sbr (Palumbi et al. 1991), 18S1F and
18S4R (Giribet et al. 1996), and 28SD1F and 28SD6R (Park
and 6 Foighil 2000). Sequences were generated with the
Sanger method on an ABI 3730x1 by Genewiz (South Plains-
field. New Jersey, USA). Contigs were assembled in (Tene-
ious (BioMatters Ltd.) and combined with Cyclophoroidea
data taken from GenBank (Table 1). Each gene fragment
was aligned separately using MUSCLE (Edgar 2004) and the
appropriate substitution model selected by Bayesian infor¬
mation criterion in IQTREE (Nguyen et al. 2015). The mod¬
els chosen were HKY+G4 (Hasegawa et al. 1985) for 16S,
JC+I+G4 (Jukes and Cantor 1969) for 18S, and TN+I+G4
(Tamura and Nei 1993) for 28S. The combined three gene
dataset was analyzed under maximum likelihood in IQTREE
allowing each gene partition to be optimized under its own
model. Branch support was estimated using 10,000 ultra-fast
bootstrap replicates (Minh et al. 2013) in IQTREE.

Results

A review of the original descriptions of both P. roche¬
bruni and P. crossei suggested that Mabille (1887a) and

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Zoosyst. Evol. 93 (1) 2017, 95-104

Table 1. GenBank accession numbers for all taxa included in
the phylogenetic analysis.

Species

16S

18S

28S

Acroptychia bathiei

HM 753491

HM753437

HM753380

Acroptychia milloti

HM753492

HM753438

HM753381

Adelopoma tucma

HM753534

HM753450

HM753393

Aperostoma palmeri

DQ093479

DQ093435

DQ093458

Arinia paricostata

HM753500

HM753441

HM753384

Bellamya bengalensis

FJ405724

FJ405678

FJ405623

Cochlostoma elegans

HM 753489

HM753435

HM753378

Cochlostoma roseoli

HM753490

HM753436

HM753379

Cochlostoma septemspirale

HM753497

HM753423

HM753367

Cyclophorus aurantiacus

JX474723

KJ407088

KF319206

Cyclophorus bensoni

JX474670

KJ407082

KF319138

Cyclophorus cantor!

JX474718

KJ407089

KF319193

Cyclophorus hirasel

AY010505

AF055644

HM003647

Cyclophorus latus

HM 753484

HM753430

HM753374

Cyclotus talvanus

HM 753485

HM753431

HM753375

DIplommatIna canallculata

HM753504

HM753445

HM 753388

DIplommatIna gomantongensis

HM753509

HM753451

HM753394

DIplommatIna rublcunda

HM753520

HM753477

HM753417

DIplommatIna rubra

HM753514

HM753456

HM753399

Japonia sp.

HM 753486

HM753432

HM753376

Leptopoma vltreum

JX474741

KJ407147

KF319214

Opisthostoma austeni

KC250904

KC250930

KC250955

Opisthostoma hallel

KC250897

KC250923

KC250948

Opisthostoma mirablle

HM753529

HM753466

HM753406

Opisthostoma obllquedentatum

HM753530

HM753467

HM753407

Opisthostoma platycephalum

KC250905

KC250931

KC250956

Opisthostoma tenerum

KC250902

KC250928

KC250953

Palalna albata

HM753531

HM753469

HM 753409

Palalna strlolata

HM753533

HM753470

HM753410

Pollicaria cf. crossei

KY359073

KY359075

KY359077

Pollicaria rochebruni

KY359072

KY359074

KY359076

Pseudopomatlas eos

KP271244

n/a

Pseudopomatlas maasseni

KM 103252

n/a

Pupina hosel

HM753493

HM753439

HM753382

Pupinella swinhoel

HM753494

HM753440

HM753383

Dautzenberg and d’Hamonville (1887) described shells
of the same species from Tonkin (Figure 1). Authors of
both species provided nearly identical data for the size
and shape of the shell, aperture, apex, and sutures, and
the number of whorls (Table 2). Mabille (1887a) did not
provide information on the color of P. rochebruni, but did
note the interior shoulder of the peristome. Dautzenberg
and d’Hamonville (1887a) gave the color of P. crossei as
reddish-brown, did not mention the shouldered peristome,
but did note the triangular breathing device. The illustra¬
tion of P. rochebruni in Mabille (1887b) clearly shows
the breathing triangle, though the shouldered peristome
is not immediately apparent in the illustrated P. crossei
shell (Dautzenberg and d’Hamonville 1887). No mention
is made in either description of any small orange shells.

A total of 87 museum specimens (Figure 2) was ex¬
amined and an additional 44 specimens were collected by
PMH and DVT. Many shells were weathered and slightly
pitted, and most were light tan to medium brown in col-

Table 2. Morphological character comparison taken from the
original descriptions of Pollicaria rochebruni and P. crossei.

P. rochebruni

P. crossei

Height

39 mm

Diameter

21 mm

20 mm

Color

n/a

Reddish-brown

Peristome

Thick, upturned, with
a channel in the upper
portion of the lip

White, circular, thickened,
with a triangular air
space at the lip.

Whorls

6.5 to 7 convex,
flattened

7 convex, flattened on the
upper part

Aperture

Circular

Shell

Ovate-pupiform,
striate, and distorted

Pupiform, striate, and
distorted

Sutures

Impressed

Linear and impressed

Apex

Obtuse

or. Of the 131 total specimens, 124 possessed a shoulder
inside the peristome and seven did not. Using the key to
Pollicaria in Kongim et al. (2013:25) we were able to
identify 12 specimens to species level: three P. roche¬
bruni, two P. crossei, and seven P. mouhoti. Seventeen
specimens had a peristome with the interior shoulder, but
were between 35 and 40 mm in height and excluded by
the key. The remaining 119 specimens also had an inte¬
riorly shouldered peristome, but had shell size and color¬
ation combinations dilFerent than those given in the key.
Using the table of comparative characters given later in
Kongim et al. (2013:28), we identihed 43 P. rochebruni,
two P. crossei, and seven P. mouhoti from the same set of
131 specimens. The remaining shells did not ht any com¬
bination of characters given in the table. The seven pu¬
tative P. mouhoti specimens more closely resembled the
specimens of P. myersii hgured in Kongim et al. (2013:27)
than the lectotype of P. mouhoti hgured therein.

Pollicaria specimens are advertised for sale at hve web¬
sites: eBay.com, yhshells.com, femorale.com, conchology.
be, and topseashells.com. Taken together, these specimens
suggest that the known distribution of Pollicaria species
should be expanded to include Guangxi autonomous region
and Yunnan province in southern China. These two regions
are adjacent to the northern borders of Vietnam, Laos, and
Myanmar. Shells from these two regions were identihed by
their sellers as P. crossei, P. gravida, and P. rochebruni.
All but two Chinese specimens possessed the interiorly
shouldered perisotome; the other two possessed the hared
lip and no shoulder seen in P. mouhoti and P. myersii. Shell
sizes varied up to 45 mm in length, and shell colors varied
from light tan through orange, reddish brown, dark brown,
and dark purple. Vietnamese Pollicaria specimens varied
similarly in color and size to the Chinese samples, and all
possessed the interior shoulder in the peristome. These
specimens were labelled as P. crossei and P. rochebruni.

DNA sequences from our putative P. rochebruni and
P. crossei specimens (Figure 3) were identical for all three
genes. Alignment lengths for each gene were 566 positions
for 16S, 430 for 18S, and 838 for 28S. Our phylogenetic
analysis produced a single tree (log-likelihood -17304.7519)

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Minton, R.L. et al.: Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

Figure 1. Original illustrations and type material of Vietnamese Pollicaria. A. Pollicaria crossei from Dautzenberg and d’Hamon-
ville (1887). B. P. rochebruni from Mabille (1887b). No figure was provided in Mabille (1887a). C. P. rochebruni, lectotype MNHN
21305. D. P. crossei, lectotype MNHN 21304. Lectotype images from Kongim et al. (2013).

that recovered a monophyletic, well-supported Pupinidae
sister to Cochlostomatidae. Pollicaria was resolved as sis¬
ter to a clade of all other pupinids (Figure 4).

Discussion

Based on museum, online, and our own data, we believe
that at least two, and possibly three, species of Pollicaria
occur or have historically occurred in Vietnam. We con¬
sider the first, P. rochebruni, to comprise both P. roche¬
bruni sensu stricto andP. crossei pre-Kongin et al. (2013).
We treat P. rochebruni and P. crossei as synonyms based
on the similarity of their original descriptions, the natural
variation seen among shells of both species, and prelim¬
inary molecular evidence. The name P. rochebruni (pub¬
lication date 14 May 1887) has priority over P. crossei
(1 July 1887) and should be applied from hereon. We
follow Kongim et al. (2013) in keeping P. rochebruni

separate from P. gravida, given the lack of specimens of
Pollicaria with an internally shouldered peristome from
between Burma and Vietnam. This implies that the two
species are geographically separate; based on the under¬
lying geology, those regions separated approximately 40
million years ago (Yin 2010). However, since museum
records only document presence not absence, future col¬
lections may suggest a continuous distribution. Addition¬
al karyotype and sequence analysis is needed to confirm
or refute the separation between topotypic P. gravida and
P. rochebruni. The revised distribution of P. rochebruni
now includes Vietnam south to Da Nlng, with a possibil¬
ity of stretching northeast into southern China (Figure 5).

We identified the second Vietnamese Pollicaria spe¬
cies as P. mouhoti, based on Solem’s (1966) identifying
collections of shells with peristomes lacking an internal
shoulder and possessing a flared and partially reflexed lip
to that species. We identified seven museum specimens
which keyed out to P. mouhoti based on Kongim et al.

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Zoosyst. Evol. 93 (1) 2017, 95-104

Figure 2. Vietnamese Pollicaria from museum collections. A and B. FLMNH 130267, Pollicaria rochebruni, Tonkin Province,
36.9 mm and 34.4 mm respectively. C. FLMNH 164622 (in part), P. cf crossei sensu Kongim et al. (2013), That Khe, Tonkin Prov¬
ince. 28.5 mm. Labeled as P. rochebruni. D. FLMNH 164621 (in part), P. cf crossei sensu Kongim et al. (2013), Pak-Kha, Tonkin
Province, 24.6 mm. Labeled as P. mouhoti. E and F. FLMNH 164620, P. mouhoti, Gia Phu, Tonkin Province, 32.5 mm and 30.9 mm
respectively.

(2013). Shells of P. mouhoti were collected by Solem
(1966) in Vat Son, and we found additional museum
specimens from Thai Nguyen, Gia Phu, Muong, and Bac
Kan. Internet records suggest similar shells can be found
in southern China, but it is unknown if they are the same
species. The distribution of P. mouhoti in Vietnam ap¬
pears restricted to isolated areas in the north.

A possible third Vietnamese Pollicaria species is
based on karyotype ditferences that Kongim et al. (2010)
uncovered in nominal P. gravida from Vietnam. Kongim
et al. (2013) assigned their two P. gravida karyoptyes to
P. rochebruni and P. crossei, the former having a large
brown shell and the latter a small orange shell. We did
not generate chromosome spreads for any individuals.

but based on the figures in Kongim et al. (2010) we find
the karyotypes between the brown and orange individu¬
als to be equivocal. We also feel the radula ditferences
listed in Kongim et al. (2013) are non-diagnostic charac¬
ters. Kongim et al. (2010) believed that their small, or¬
ange-shelled snail was the result of sympatric speciation
due to chromosomal evolution as outlined in King (1993).
This hypothesis is consistent with studies of similar pat¬
terns of intra- and interspecific karyotype variation seen
elsewhere (e.g. Ayala and Coluzzi 2005). Whereas au¬
thors have provided possible selective pressures that may
accompany the karyotypic divergence (e.g. elevation and
temperature), there is insufficient data available to pose
any similar hypothesis for this Pollicaria species. Given

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Minton, R.L. et al.: Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

Figure 3. Pollicaria specimens sequenced in this study. A. CM
155302, orange phenotype (cf. P. crossei sensu Kongim et al.
[2013]), 38.6 mm. B. CM 155307, red-brown phenotype (cf. P
rochebruni), 24.7 mm.

our synonymizing of P. crossei with P. rochebruni, if the
individuals with the unique karyotype represent a new
species it will require a new name. The known distribution
of this possible taxon is limited to Cue Phuong National
Park and Huu Lien nature preserve (Kongim et al. 2013).

Our preliminary molecular evidence suggests that shell
color and size may not be reliable for consistent species
identification in Vietnamese Pollicaria. Sequences from
one small, reddish-brown shelled snail (cf P. rochebruni)
and one large, orange-shelled snail (cf P. crossei) were
identical at three genetic loci. Our orange-shelled snail
was larger than the nominal P. crossei in Kongim et al.
(2013), and was collected alongside similarly-sized indi¬
viduals with brownish and reddish shells. We feel both
of our sequenced specimens represent P. rochebruni, sup¬
porting our belief that shell color in Pollicaria species can
vary greatly. This contrasts with Kongim et al. (2013),
who felt that shell color was diagnostic for many species.

Despite our best efforts and those of Kongim et al.
(2013) to untangle the taxonomy of Pollicaria, we recog¬
nize the need for more work on the genus. Karyotypes of
topotypic P. gravida remain unknown so no comparisons
to the Vietnamese and other taxa can be made. Addition¬
al field work in southeastern Asia and southern China is
needed to determine the true ranges of each species.

Systematic accounts

Family Pupinidae

Genus Pollicaria Gould, 1856

Pollicaria rochebruni (Mabille, 1887)

Hybocystis rochebruni Mabille 1887a: 12; Mabille 1887b: 138, pi. 2,
figs 12 and 13; Dautzenberg and Fischer 1905:171
Pollicaria rochebruni - Kobe It 1902: 290; Kongim et al. 2013: 35, figs
5D and 5E

Hybocystis crossei Dautzenberg and d’Hamonville 1887: 220, pi. 8, fig.
4; Kobelt and Mbllendorf 1899: 137; Kobelt 1902: 290; Dautzen¬
berg and Fischer 1905:171
Pollicaria crossei - Kongim et al. 2013: 37, fig. 5F
Hybocystis gravida-Vdim 1974: 174.

Pollicaria gravida - Kongim et al. 2010: 127 (“big brown shell”)

Type Designation and locality. Lectotype MNHN
21305, Tonkin. Paralectotypes MNHN 25855, Tonkin
(Kongim et al. 2013).

Material examined. All material from Vietnam / Tonkin
Province. The number in parentheses is the number of shells
from each lot assigned to the species. Locality names have
been corrected wherever possible. - CM 155301, south of
QL279, Tham Duong, Van Ban District, Lao Cai (7); CM
155302, Vuon quoc gia Cue Phuong, Lac Son District, Hoa
Binh (3); CM 155303, south of QL279, Tham Duong, Van
Ban District, Lao Cai (7); CM 155304, limestone moun¬
tain at bridge into Tan Moui, near intersection of QL279
and DT234B, southwest of Chi Lang, Lang Son (6); CM
155305, ca. 60 m north of the intersection of QLIA and
DT234B, Chi Lang, Lang Son (6); CM 155306, limestone
mountain off QL279 at H9/155 road marker, ca. 1.1 km
southwest of Dong Mo and 0.9 km southwest of Chi Lang,
Lang Son (1); CM 155307, Cong An huyen Cao Phong at
QL6, Cao Phong, Hoa Binh (15); FLMNH 130259, That
Khe (4); FLMNH 130265, Phu Ly (3); FLMNH 130623,
Thai Nguyen (1); FLMNH 130258, Bdc Kan (3); FLMNH
130261, Thai Nguyen (3); FLMNH 130262, Thai Nguyen
(3); FLMNH 130624, Phi Mi (1); FLMNH 130260, Thai
Nguyen (2); FLMNH 130268 (1); FLMNH 243794, Thai
Nguyen (2); FLMNH 271764, Ninh Binh Province, Cue
Phuong National Park, path to fairy cave, primary forest
(1); FLMNH 164619, Thai Nguyen (2); FLMNH 164620,
Gia Phu (2); FLMNH 164621, Pak-Kha (2); FLMNH
164622, That Khe (3); FLMNH 164623, Chg Ra (4); FLM¬
NH 130267 (2); FLMNH 242525 (2); FLMNH 192609,
That Khe (6); FLMNH 130266 (1); MCZ 180001, vicinity
of Lake Ba Be (2); MCZ 180002 (2); MCZ 180003, That
Khe (2); MCZ 180004, vicinity of Lake Ba Bd (3); MCZ
180005, Thai Nguyen (1); MCZ 180006, Thai Nguyen (4);
MCZ 180007, Pak-Kha (4); MCZ 180008, Bao Lac (2);
MCZ 180009, Pak-Kha (1); MCZ 197272, Pak-Kha (4);
MCZ 380546 (1); USNM 207972, Ldo Cai (1); USNM
207973, Lao Cai (1); USNM 207974, Chg Ra (1); USNM
207975, Bic Kan (1); USNM 207976, Chg Ra ty); USNM
207977, Chg Ra (1); USNM 207978, Muong (1); USNM
207979, Muong (1); USNM 207980, Vdn Son (1); USNM
207981, van Son (1); USNM 220045, Ba Be (3^ USNM
335963, Bic Kan (2).

Type species. Benson, 1856(=Cy- Literature records (not examined). All from Vietnam,

clostomapollex Gould, 1856), designated by Pain (1974). taken from Kongim et al. (2013). CUMZ 1523, Phong Na

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Zoosyst. Evol. 93 (1) 2017, 95-104

101

Pupinella swinhoei
Pupina hosei
Pseudopomatias eos
Pseudopomatias maasseni
PoHicaria rochebruni
100 * Pollicaria crossei
Cochlostoma septemspirale
Cochlostoma elegans
Cochlostoma roseoli

Acroptychia bathiei
Acroptychia milloti J

Pupinidae

Cochlostomatidae

Megalostomatidae

Cyclophoridae

100 '

Cyclotus taivanus
Japonia sp.

Leptopoma vitreum
Cyclophorus latus
Cyclophorus hirasei
Cyclophorus bensoni
Cyclophorus cantori

L Palaina albata
— Palaina striolata
Diplommatina rubicunda
Diplommatina rubra
Adelopoma tucma

Diplommatina canaliculata

Diplommatina gomantongensis
Opisthostoma hailei

Opisthostoma tenerum
Opisthostoma ptatycephalum
Arinia paricostata
Opisthostoma mirabile
Opisthostoma obliquedentatum
Opisthostoma austeni

Diplommatinidae

Aperostoma palmeri ] Neocyciotidae
Bellamya bengatensis

I-1

0.1

Figure 4. Phylogenetic tree (log likelihood= -17304.7519) based on three ribosomal genes (mt 16S, nuclear 18S and 28S) showing
Pollicaria as sister to all other pupinid taxa. Values at branches are bootstrap values based on 10,000 ultrafast replicates.

National Park, Quang Binh; CUMZ 1532, Cue Phuong
National Park, Ninh Binh; CUMZ 1539, Phong Na Na¬
tional Park, Quang Binh; CUMZ 1552, Phong Na Na¬
tional Park, Quang Binh; CUMZ 1556, Bach Ma Nation¬
al Park; CUMZ 1568, Phong Na National Park, Quang
Binh; CUMZ 1568, Cue Phuong National Park, Ninh
Binh; CUMZ 1573, Cue Phuong National Park, Ninh
Binh; CUMZ 1587, Cue Phuong National Park, Ninh
Binh; CUMZ 1589, Khe Sen, Da Mng; CUMZ 1594,

Huu Lien Nature preserve; MNHN 21304, Than Moi,
Tonkin; RBINS 525390, Than Moi, Tonkin.

Description. Pupoid shell, to 45 mm length and 20 mm di¬
ameter, color varying from tan to orange, reddish-brown,
and dark brown, possibly dark purple. Old specimens are
often finely pitted. Whorls 5-7, transverse growth lines
present, sutures linear and slightly impressed, apex obtuse
and occasionally distorted to the left (assuming standard

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Minton, R.L. et al.: Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

Figure 5. Revised distribution map for North Vietnamese Pollicaria species. Pollicaria rochebruni is present at all sites shown.
Black dots indicate the presence of P. mouhoti, while gray dots indicate the presence of the putative new species of Kongim et al.
(2013). Coordinates for localities taken from museum data were estimated from historical sources.

anatomical position), spire short. Penultimate body whorl
may appear inflated relative to whorls on either side. Ap¬
erture circular with a right posterior triangular breathing
structure. Peristome thiekened, white to shell colored,
with a thin parietal declining shoulder inside; umbilicus
narrow. Operculum concentric, thick, and calcareous.

Radula with teeth in a 2-1-1-1-2 arrangement, based
on the figure in Kongim et al. (2013: Figure 6E). Cen¬
tral tooth with three cusps, the middle one longer that the

others. Lateral teeth with one large cusp and one smaller
cusp on the central side. Marginals with one large central
cusp flanked by one smaller cusp on each time. Kongim
et al. (2013) described the radula as having more cusps
per tooth than illustrated.

Distribution. Northern Vietnam south to Da Nlng (Fig¬
ure 5). Possibly in Guangxi autonomous region and Yun¬
nan Province, China.

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103

Discussion. By synonymizing P. rochebruni and P. cros-
sei, we suggest that all Pollicaria specimens from Viet¬
nam that possess an interiorly shouldered peristome are
a single species, excluding some smaller (< 35 mm) in¬
dividuals with bright orange shells. We found live spec¬
imens of P. rochebruni at the bases of and in the valleys
between karst outcrops in northern Vietnam. Reports
from local farmers indicated that snails are more abun¬
dant during the spring rains, when native residents eat
them as a delicacy. Some Chinese shells found for sale on
the Internet are consistent morphologically with P. roche¬
bruni but may represent a separate species.

Acknowledgements

RLM was supported by Faculty Research Support Funds
through UHCL. PMH was supported in part by the UA
Research Grants Committee, and a UA College Academy
of Research, Scholarship, and Creativity award. Images
of original figures {P. rochebruni and P. crossei) were
downloaded from Biodiversity Heritage Library and are
in the public domain. Images in figure 1 are reproduced
from Kongim et al. (2013) under the terms of the Creative
Commons Attribution License 3.0.

References

Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, drosophila,
and mosquitos. Proceedings of the National Academy of Sciences USA
102(S1): 6535-6542. https://doi.org/10.1073/pnas.0501847102
Benson WH (1856) Characters of seventeen new forms of the Cyclosto-
macea from the British Provinces of Burmah, collected by W. Theo¬
bald, jun.. Esq. Annals and Magazine of Natural History Series 2
17(99): 225-233. https://doi.Org/10.1080/00222935608697501
Benson WH (1859) Observations on the shell and animal of Hybo-
cystis, a new genus of Cyclostomatidae, based on Megalomasto-
ma gravidum and Otopoma blennus B.; with notes on other living
shells from India and Burmah. Annals and Magazine of Natural
History Series 3 4(20): 90-93. http://www.tandfonline.com/doi/
abs/10.1080/00222935908697091

Benson WH (1860) Notes on the subgenus Gorilla, H. and A. Ad¬
ams; and on the group Plectopylis, Benson; also on Pollicaria,
Gould, and Hybocystis, Benson. Annals and Magazine of Natural
History Series 3 6(32): 98-100. http://www.tandfonline.com/doi/
abs/10.1080/00222936008697288

Crosse H (1885) Etude monographique sur les especes du genre Hy¬
bocystis de Benson. Journal de Conchyliologie 33: 180-193. http://
biodiversitylibrary.org/page/15979546
Dautzenberg P, d’Hamonville E (1887) Description d’Especes nouvelles
du Tonkin et observations sur quelques autres Mollusques de la
meme region. Journal de Conchyliologie 35: 213-225. http://biodi-
versitylibrary.org/page/15921460

Dautzenberg P, Fischer P (1905) Eiste de Mollusques recoltes par M.
le Capitaine de Fregate Blaise au Tonkin, et descriptions d’especes
nouvelles. Journal de Conchyliologie 53 (2"‘' quarter): 85-234.
http://biodiversitylibrary.org/page/16292495

Edgar RC (2004) MUSCEE: multiple sequence alignment with high ac¬
curacy and high throughput. Nucleic Acids Research 32(5): 1792-
1797. https://doi.org/10.1093/nar/gkh340
Giribet G, Carranza S, Baguna J, Riutort M, Ribera C (1996) First
molecular evidence for the existence of a Tardigrada+Arthropoda
clade. Molecular Biology and Evolution 13(1): 76-84. https://doi.
org/10.1093/oxfordj oumals. molbev. a025573
Gould AA (1856) [Descriptions of fourteen shells]. Proceedings of the
Boston Society of Natural History 6: 11-16. http://biodiversityli-
brary.org/page/9493210

Haines WA (1858) Descriptions of four new species of terrestrial
shells from Siam. Annals of the Eyceum of Natural History of New
York 6(1): 157-158. https://doi.Org/10.llll/j.1749-6632.1858.
tb00358.x

Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human-ape
splitting by a molecular clock of mitochondrial DNA. Journal of
Molecular Evolution 22(2): 160-174. https://doi.org/10.1007/
BF02101694

Hijmans R, Guarino E, Mathur P, Jarvis A (2008) DIVA-GIS. http://
www.diva-gis.org

Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro
HN (Ed.) Mammalian Protein Metabolism (vol. 3). Academic Press,
21-132. https://doi.Org/10.1016/B978-l-4832-3211-9.50009-7
King M (1993) Species Evolution: the Role of Chromosome Change.

Cambridge University Press, Cambridge, 360 pp.

Kongim B, Sutcharit C, Tongkerd P, Tan S-HA, Quynh NX, Naggs
F, Panha S (2010) Karyotype variations in the genus Pollicaria
(Caenogastropoda: Pupinidae). Zoological Studies 49(1): 125-131.
http://zoolstud.sinica.edu.tw/Journals/49.1/125.pdf
Kongim B, Sutcharit C, Naggs F, Panha S (2013) Taxonomic revision
of the Elephant Pupinind snail genus Pollicaria Gould, 1856 (Proso-
branchia, Pupinidae). ZooKeys 287: 19-40. https://doi.org/10.3897/
zookeys.287.4617

Mabille MJ (1887a) Molluscorum Tonkinorum diagnoses. Imprime par
A. Masson, Meulan, 18 pp.

Mabille MJ (1887b) Sur quelques mollusques du Tonkin. Bulletin de
la Societe Malacologique de France 4: 73-164. http://biodiversityli-
brary. org/page/14883892

Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approxima¬
tion for phylogenetic bootstrap. Molecular Biology and Evolution
30(5): 1188-1195. https://doi.org/10.1093/molbev/mst024
de Morgan J (1885) Mollusques terrestres et fluviatiles du Royaume de
Perak et des pays voisins (Presqu’ile Malaise). Bulletin de la Societe
Zoologique de France 10: 353-428. https://doi.org/10.5962/bhl.
part. 14300

Nguyen E-T, Schmidt HA, von Haeseler A, Minh BQ (2015) Iq-tree: A
fast and effective stochastic algorithm for estimating maximum-like¬
lihood phylogenies. Molecular Biology and Evolution 32(1): 268-
274. https://doi.org/10.1093/molbev/msu300
Pain T (1974) The land operculate genus Pollicaria Gould (Gastropo¬
da), a systematic revision. Journal of Conchology 28(3): 173-178.
Park J-K, 6 Foighil D (2000) Sphaeriid and corbiculid clams represent
separate heterodont bivalve radiations into freshwater environments.
Molecular Phylogenetics and Evolution 14(1): 75-88. https://doi.
org/10.1006/mpev. 1999.0691

Palumbi S, Martin A, Romano S, McMillan W, Stice E, Grabowski G
(1991) The Simple Fool’s Guide to PCR, Version 2.0. University of
Hawaii, Honolulu.

zse.pensoft.net

104

Minton, R.L. et al.: Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

Pfeiffer L (1862) Descriptions of thirty-six new land shells, from the collec¬
tion of H. Cuming, Esq. Proceedings of the Zoological Society of Lon¬
don 3: 268-278. https://doi.Org/10.llll/j.1469-7998.1862.tb06529.x
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard R (1984) Ribo-
somal DNA spacer-length polymorphisms in barley: Mendelian in¬
heritance, chromosomal location, and population dynamics. Proceed¬
ings of the National Academy of Sciences USA 81(24): 8014-8018.
https://doi.org/10.1073/pnas.81.24.8014
Solem A (1966) Some non-marine molluscs from Thailand, with notes on
classification of the Helicarionidae. SpoliaZoologica Musei Hauniensis
24: 1-110. http://www.vhz.be/imisdocs/publications/261969.pdf

Tamura K, Nei M (1993) Estimation of the number of nucleotide sub¬
stitutions in the control region of mitochondrial DNA in humans and
chimpanzees. Molecular Biology and Evolution 10(3): 512-526.
http: //mbe. oxford) ournals. org/content/10/3/512. long
Turney S, Cameron ER, Cloutier CA, Buddie CM (2015) Non-repeat-
able science: assessing the frequency of voucher specimen deposi¬
tion reveals that most arthropod research cannot be verified. PeerJ 3:
e 116 8 . https: //doi. org/10.7717/peerj. 116 8
Yin A (2010) Cenozoic tectonic evolution of Asia: a preliminary synthe¬
sis. Tectonophysics 488(1-4): 293-325. https://doi. 0 rg/lO.lOl 6 /j.
tecto.2009.06.002

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 105-133 | DOI 10.3897/zse.93.10489

4>yEnsPFr.

museum fur naturkunde

A review of the reproductive biology of the only known matrotrophic
viviparous anuran, the West African Nimba toad,

Nimbaphrynoides occidentalis

Laura Sandberger-Loua\ Hendrik Milller^, Mark-Oliver RodeL

1 Museum fur Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrafie 43, 10115 Berlin

2 Institut fiir Spezielle Zoologie undEvolutionsbiologie mit Phyletischem Museum, Eriedrich-Schiller-Universitat Jena, Erbertstr. 1, 07743 Jena
http://zoobank.org/lA298760-DD05-466F-AD01-23BF7619426C

Corresponding author: Laura Sandberger-Loua (laura.sandberger@mfn-berlin.de)

Received 13 September 2016
Accepted 14 January 2017
Published 3 February 2017

Academic editor;

Peter Bartsch

Key Words

Amphibia

development

evolution

ovary

oviduct

pueriparity

seasonality

testes

uterus

Abstract

Amphibians, and anurans in particular, show the highest diversity of reproductive modes
among tetrapods. Nevertheless, viviparity is scarce in anurans and its occurrence is even
more often assumed rather than confirmed. Probably the best studied viviparous amphib¬
ian is the Nimba toad, Nimbaphrynoides occidentalis. During more than 40 years of re¬
search, the Nimba toad’s reproductive morphology, endocrine activity of the ovary as
well as the pituitary gland, and to some extent the ecological impact (seasonality, humid¬
ity, food availability) on reproduction was examined. Due to the Nimba toad’s unique re¬
productive mode, summaries are usually included in reviews discussing amphibian repro¬
duction and articles on reproductive biology often discuss the exceptional reproductive
system of Nimba toads. However, to our knowledge a detailed synthesis, summarising all
the different original studies on the toad’s reproduction, is so far missing. In this paper we
review and summarise all available initial publications, which often have been published
in French and/or are difficult to access. A short overview is given of the climatic and
environmental conditions experienced by Nimba toads and the key findings supporting a
“true” viviparous reproduction with matrotrophy (maternal provision of nutrition during
the gestation) and pueriparity (birth of juveniles). Then foetal development (morpho¬
logical, gonad and pituitary development), and the female (ovary, oviduct, pituitary and
their endocrine interactions) and the male reproductive system (testes and pituitary) are
reviewed. Finally, the reproductive cycle and its link to the Nimba mountains’ seasonality
and ecological/ conservation implications are discussed.

Introduction

Viviparity, in the sense of retaining developing eggs or
foetuses within the female genital tract, evolved numer¬
ous times in vertebrates and within tetrapods especially
in squamates (Blackburn 1999, 2015, Pyron and Bur-
brink 2014, van Dyke et al. 2014). Internal fertilisation is
necessary to allow oviductal egg retention and viviparity
(Wake 2015b). As most caudates (90%, Wake 2015a) and
all caecilians are internally fertilising (Gomes et al. 2012,
Wake 2015a) they show the first requirement for vivipari¬
ty (Wake 2015a, 2015b). Nineteen (2.7%, Buckley 2012)
of the ca 700 caudate species (695 AmphibiaWeb 2017,

703 Frost 2017, both accesses 11.01.2017) and about one
fourth of the ca 200 caecilian species (205 AmphibiaWeb
2017, 205 Frost 2017, both accessed 11.01.2017) are
known or assumed to be viviparous (Buckley 2012, San
Mauro et al. 2014, Wake 2015a, 2015b). Anurans (frogs
and toads), on the other hand, show a very high diversity
in reproductive modes (at least 42 modes, Haddad and
Prado 2005, Iskandar et al. 2014), but internal fertilisation
and viviparity are very rare. Of the ca 6,700 recognised
anuran species (6,714 AmphibiaWeb 2017, 6,678 Frost
2017, both accessed 11.01.2017), viviparity is only known
or assumed in 17 species (0.3%) of five genera: Craugastor
(1 species), Eleutherodactylus (1), Limnonectes (1), Necto-

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which permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

106

Sandberger-Loua, L. et al.: Nimba toad reproductive biology

phrynoides (13) and Nimbaphrynoides (1). Hence, within
the Amphibia, viviparity is common in caecilians, rare in
caudates and exceptional in anurans.

Viviparous reproductive modes may differ in two fun¬
damental traits: i) at which developmental stage offspring
are born and ii) in the way foetuses receive the nutritional
energy for their development. During amphibian devel¬
opment the adult anuran body plan is only achieved after
metamorphosis is completed (Duellman and Trueb 1986,
Wells 2010). In larviparous species, offspring are born
at any larval stage before metamorphosis (Greven 2003)
and newborn larvae are dependent on open water. In pu-
eriparous species offspring are born after metamorphosis
(Greven 2003) and water independent juveniles are born.
Within caudates 14 (64%) of the viviparous species and
some subspecies of Salamandra salamandra (Buckley
et al. 2007, Wake 2015a, 2015b) and Salamandra algira
(Beukema et al. 2010, Escoriza and Ben Hasssine 2014)
are pueriparous. In anurans only one of the known 17 vi¬
viparous species is larviparous (Limnonectes larvaepar-
tus; Iskandar et al. 2014, Kusrini et al. 2015), all others
(94%) are pueriparous. Within caecilians no larviparous
species are known, nevertheless oviparous species may
lay eggs in the neurula stage (Sarasin and Sarasin 1887,
Kupfer et al. 2006, Gomes et al. 2012). Hence, pueripar-
ity is the only known viviparous mode in caecilians and
more common in anurans than in caudates.

Foetal development and growth needs energy. This
energy can be provided by the mother via yolk rich (leci-
thotrophic) eggs, or by unfertilised eggs and smaller
siblings (oophagy and embryophagy, sometimes called
adelphophagy), or the mother continuously nourishes the
foetus during gestation (matrotrophy). A good example for
lecithotrophy is direct development: large, yolk rich eggs
are deposited at humid locations, outside of water, and the
entire development takes place within the egg, exclusively
powered by yolk (Guibe and Lamotte 1958, Hanken 2003).
The best-known example for matrotrophy are mammals, in
which yolk poor eggs are fertilised and very early within
the development the nutritional needs of the foetus are pro¬
vided for by the mother via a placenta. Nutrition through
unfertilised eggs and/ or intra-oviductal cannibalism of the
offspring, is known for example from Salamandra sala¬
mandra subspecies (Buckley et al. 2007, Buckley 2012).
Matrotrophy in amphibians may be achieved through the
development of a particular intra-oviductal epithelium
(e.g. “zona trophica” in Salamandra atra) with increased
mitoses, cell growth and apoptosis (Vilter 1986, Wake
2015a, 2015b). This epithelium is consumed by the foe¬
tuses, for which they developed special dentition in sala¬
manders and caecilians (Wake 1993, 2015a, Gomes et al.
2012). In some oviparous caecilians with maternal care,
special epidermal cells are produced by the mother and eat¬
en by the offspring (skin feeding, Kupfer et al. 2006, Wake
2015a). The distinction between lecitotrophy, oophagy and
matrotrophy is not as sharp as between pueriparous and
larviparous species and the different types are not mutual¬
ly exclusive (Wake 2015a, 2015b). All eggs contain some

amount of yolk which is consumed before other nutrition is
used (Wake 2015a). The best studied viviparous salaman¬
der, Salamandra atra, for example combines lecitotrophy,
with oophagy and matrotrophy (Vilter 1986, Wake 2015a).
Within this species, only two eggs, one per oviduct, receive
all egg layers necessary for fertilisation. In each oviduct
one foetus develops, first dependent on its own yolk, af¬
ter hatching by feeding on the unfertilised eggs within the
oviduct and last by matrotrophy where foetuses feed of the
epithelium cells in a “zona trophica” (Vilter 1986, Wake
2015a). Within caecilians and caudates matrotrophy is
known from several species (San Mauro et al. 2014, Wake
2015b). In anurans, only a single species is known in which
most energy for foetal development derives from matrotro¬
phy (Xavier 1971, Wake 1993, 2015a, 2015b). This spe¬
cies is Nimbaphrynoides occidentalis (Xavier 1977, 1986,
Wake 2015b).

This unique matrotrophic (and pueriparous) anuran is a
small (snout vent length (SVL) 15-27 mm, Lamotte 1959,
Xavier 1971) West African bufonid, endemic to a few
square kilometres (4 km^, Lamotte 1959) of the high al¬
titude grasslands of the Nimba mountains (Lamotte 1959,
Lamotte and Sanchez-Lamotte 1999, Hillers et al. 2008,
Sandberger-Loua et al. 2016a), a small mountain chain in
the tri-border area of Guinea, Ivory Coast and Liberia (Fig¬
ure 1). Shortly after its description as Nectophrynoides oc¬
cidentalis Angel, 1943, its unique viviparous reproductive
mode was recognised (Angel and Lamotte 1944a, 1944b)
and led to numerous, partly very detailed studies. After
the internal fertilisation of very tiny (~500 pm) yolk-poor
eggs (Angel and Lamotte 1944b, Lamotte and Rey 1957,
Vilter and Lugand 1959a, Xavier 1971), the eggs are re¬
tained within the lower part of the oviduct (Angel and La¬
motte 1944a, Vilter and Lamotte 1956, Xavier 1971), the
oviductal epithelium secrets liquid mucoproteins to nour¬
ish the foetuses (Vilter and Lugand 1959b, Xavier 1971,
1977, 1986), which are bom after nine months as fully
developed Juveniles (e.g. Angel and Lamotte 1947, La¬
motte et al. 1956, Lamotte 1959, Xavier 1971). Fran^oise
Xavier summarised her own large body of work in two
book chapters (Xavier 1977, 1986) and summaries are
included e.g. in reviews by M. Wake (e.g.: Wake 1993,
2015a, 2015b) and in K.D. Wells’ book (2010). Within
this review we synthesise all the extensive work by F. Xa¬
vier, but as well the studies of M. Zuber-Vogeli, M. La¬
motte, J. Gavaud, V. Vilter and others.

A short history of the taxonomy of
Nimbaphrynoides occidentalis

The Nimba toad was described as Nectophrynoides occi¬
dentalis Angel, 1943, due to its similarity to the then two
known East African Noble, 1926 species,

N. viviparous (Tomier, 1905) and V. tornieri (Roux, 1906).
For the same reason the new species was assumed to be
pueriparous and lecitotrophic (Angel 1943). Later it was
even hypothesised to be parthenogenetic, as during the

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first field survey M. Lamotte had not recorded any males
(Angel and Lamotte 1944a, 1944b). During a second field
period males and matings were observed and subsequently
matrotrophy assumed (Angel and Lamotte 1944b). Dubois
(1986) revised the genus Nectophrynoides, which at that
time comprised oviparous, lecitotrophic viviparous and
matrotrophic viviparous species and placed them, accord¬
ing to their reproductive mode, into four different genera:
Spinophrynoides (for the oviparous Ethiopian S. osgoodi,
now placed in Altiphrynoides and feared to be extinct;
Gower et al. 2013), Altiphrynoides (for the direct develop¬
ing A. malcolmi from Ethiopia), Nectophrynoides (now 13
lecitotrophic pueriparous species all from Tanzania, one ex¬
tinct in the wild), and Nimbaphrynoides (now one species
from the Nimba mountains in Guinea, Ivory Coast and Ei-
beria). The Nimbaphrynoides population from Eiberia was
described as a separate species (Xavier 1978), but because
of high genetic and acoustic similarity is now considered
to be a sub-species of N. occidentalis (Sandberger et al.
2010). Based on morphological data it was assumed that N.
occidentalis is more closely related to Altiphrynoides than
to Nectophrynoides (Wake 1980b, Grandison 1981), and
most closely related to Didynamipus sjostedti (Grandison
1981, Graybeal and Cannatella 1995), a small, probably
direct developing forest toad from Cameroon (Gonwouo
et al. 2013). A recent, comprehensive phylogenetic study
by Eiedtke et al. (2016) confirmed Didynamipus as sister-
group to Nimba toads. Interestingly, while Altiphrynoides,
Nectophrynoides and Nimbaphrynoides are part of the
same clade, none of these form a sistergroup relationship
with each other. This suggests that direct development and
viviparity seen in these taxa possibly evolved independent¬
ly of each other (Eiedtke et al. 2016).

The habitat of the Nimba toad

Nimba toads are endemic to the Nimba mountains, which
are a south-west, north-east oriented mountain chain in
Eiberia, Ivory Coast and Guinea (see Figure 1). This

steep-sided mountain chain is about 40 km long and in
parts up to 12 km wide (Schnell 1952). The surround¬
ing lowlands are at about 500 m asl, whereas the high¬
est peak, Richard-Molard, reaches 1,762 m asl (Schnell
1952, Eeclerc et al. 1955, Eamotte 1959, Eamotte et al.
2003). In its southern, Eiberian part the mountain ridge
is lower (Eamotte et al. 2003), and after mining activi¬
ties now only rarely exceeds 1,200 m asl. In the northern,
Guinean part the main ridge undulates between 1,200 m
asl and 1,762 m asl (Eeclerc et al. 1955). It consists of
banded iron formations (Billa et al. 1999), which are of
high global economic importance (Berge 1974, Eamotte
1983, Schnell 1987). The presence of Nimba toads and
chimpanzees as part of a rich and endemic fauna and flora
led to the declaration of the Nimba mountains as a World
Heritage Site in Guinea in 1981 and Ivory Coast in 1982
(UNESCO July 22, 2015/2015). Due to increasing min¬
ing exploration activities, the WHS has been listed as in
danger since 1992 (Poilecot and Eoua 2009, UNESCO
July 22, 2015/2015). In 2014 its outlook was considered
to be “critical” (lUCN January 11, 2017/2014).

The climate of the area is characterised by first rains
in March/ April, a rainy season from May to October and
a dry season from November to February/ March. Mean
yearly temperature is 25°C in the lowlands (550 m asl)
and 19°C at high altitudes (Eeclerc et al. 1955, Eamotte
1958, Eamotte and Roy 1962, Eamotte et al. 2003). Mean
annual precipitation is 2,093 mm, but is estimated to
range from 1,500 mm in the lowlands to 3,000 mm on
the ridges (Eamotte 1959, Eamotte et al. 2003). The rainy
season at high altitude is characterised by nearly constant
fog and rather continuous, but not very heavy, rain (Ea¬
motte 1959). The dry season is characterised by larger
temperature fluctuations, low humidity, little rain and dry
season fires (see Figure 2, Schnell 1952, Eamotte 1958,
1959). The change from one season to the other is cha¬
racterised by tornadoes and thunderstorms (Schnell 1952,
Eeclerc et al. 1955, Eamotte 1959). The first rains after
the dry season may arrive between the end of February
and April, whereas the very humid rainy season does not

Figure 1. The Nimba mountains. Left: elevation map of the Nimba mountains, with an inset map showing the position of the Nimba
mountains within West Africa. Right: a large part of the Nimba mountains showing the steep slopes, the high altitude grasslands,
the forests in the lowlands and the ravines.

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108

Sandberger-Loua, L. et al.: Nimba toad reproductive biology

Figure 2. Rainy and dry season at Nimba. The rainy season (top) is characterised by persistent fog and rain, whereas the dry season
(middle) is characterised by little rain, high temperature fluctuations and dry season fires. After dry season fires the grasses sprout
very fast (bottom, © Nema Soua Loua).

start before June (Schnell 1952, Leclerc et al. 1955, La-
motte 1959). The transition between the rainy and the dry
season is much faster and happens during a few weeks
between October and November (Lamotte 1959). High
elevations receive more rain than the lowlands during the
rainy season, but less rain during the intermittent and dry
seasons (Lamotte 1959, Lamotte and Roy 1962).

The areas outside the World Heritage Site are almost
exclusively anthropogenically altered landscapes (Schnell
1952, 1987, Fournier 1987, Lamotte et al. 2003). Within
the reserve the lower flanks and lowlands of the Nimba
mountains are mainly covered in evergreen forests. In
the South forests naturally grow as well on the mountain
ridges, whereas in the North they are restricted to ravines
(Lamotte et al. 1962, Fournier 1987). The lowland forests
are a mosaic of primary and secondary forests (Lamotte
1947b, Schnell 1952, 1987, Fournier 1987). At higher al¬
titudes the lowland forests transition into a montane for¬
est characterised by lower tree diversity, the presence of
Parinari excelsa, many epiphytes and less lianas (Schnell
1952). Savannas are mostly found in the lowlands on the
eastern sides of the mountain chain, growing on thinner
top-soils than forests (Schnell 1952, 1987, Fournier 1987,
Lamotte et al. 2003). Within Guinea the largest parts of
the high altitudes are covered in montane grasslands (La¬
motte 1947a, 1947b, 1958, 1959, Schnell 1952, 1987, La¬

motte and Roy 1961a, 1962, Lamotte et al. 1962, 2003a,
Fournier 1987). These grasslands are characterised by the
high abundance of the grass Loudetia kagerensis (Schnell
1952, 1987, Fournier 1987), fast regrowth after fires and
despite their thin layer of top soil a large herbaceous bio¬
mass (Fournier 1987). Depending on the soil characteris¬
tics and anthropogenic impacts (e.g.: mining roads) slight¬
ly differing plant assemblages can be recognised (Fournier
1987, Schnell 1987). Standing open water is present only
at two locations on the mountain top and only for some
months during the rainy season (June/ July-September).
These ponds are very shallow (< 5 cm). Due to the rarity
of open water, the harsh climatic conditions and the iso¬
lation of the mountain a high percentage of the species in
the high altitude grasslands is endemic (Lamotte and Roy
1961a), such as the Nimba toad, which occurs exclusively
in the high altitude grasslands above 1,200 m asl (Lamotte
1959, Hillers et al. 2008, Sandberger-Loua et al. 2016a).

Annual seasonality and activity patterns

The very pronounced differences between the rainy and the
dry season has strong effects on the toad’s activity patterns
(Lamotte 1959, Sandberger-Loua et al. 2016a) and their
reproductive cycle (Xavier 1971, Gavaud 1977). Nimba

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109

Figure 3. Nimba toad females. Left; a young female towards the end of the rainy season. Right; a large gestating female in June,
shortly before parturition.

toads are only active during the rainy season (Lamotte
1959, Sandberger-Loua et al. 2016a). With the first rains
gestating females emerge from the aestivation sites, later
joined by virgin females and males (Lamotte 1959, Xavier
1971, Lamotte and Sanchez-Lamotte 1999). When rains
become more permanent and humidity rarely drops below
saturation, juveniles are bom (compare Figure 3, Angel and
Lamotte 1947, Lamotte 1959). Nimba toads mate at the end
of the rainy season, in September/ October, rarely Novem¬
ber (Angel and Lamotte 1947, Lamotte 1959, Xavier 1971,
Lamotte and Xavier 1976b, Lamotte and Sanchez-Lamotte
1999). Mated females go underground, whereas unmated
females and males may stay as long above ground as the
rains continue (Lamotte 1959, Xavier 1971). During the
dry season toads are dormant underground (Angel and La¬
motte 1947, Vilter 1955, Lamotte and Xavier 1976a), hid¬
ing under rocks and within crevices (Vilter 1955), where
humidity is higher and temperature less variable (Lamotte
1959). Nimba toads have a gestation period of nine months
(October-June, e.g. Angel and Lamotte 1947, Lamotte et
al. 1956, Lamotte 1959, Xavier 1971), of which they spend
about the first six months (may vary between 4—7 months,
October/ November to February/ March/ April) dormant
underground and only the last 3 months (2-5 months, Feb¬
ruary/ March/ April to June) active above ground (e.g.: An¬
gel and Lamotte 1947, Lamotte 1959).

Nimba toad females have a life expectancy of three to
four, rarely five years; males reach even only up to three
years (Castanet et al. 2000). On average, females give
birth to nine young per gestation (range 4-20, Angel 1943,
Angel and Lamotte 1944a, 1944b, Vilter 1956a, Lamotte
and Xavier 1976a). However, the number of offspring
bom per gestation increases with age and hence, with size
(Lamotte 1959, Xavier 1971). The average number of off¬
spring per female in their first year is four, in the second
6.5, in their third 9.4 and in their fourth year 12 young
(Xavier 1971). Assuming a life expectancy of three years.

each female may give birth to about 20 offspring during
her lifetime (32 if females survive four years). For a toad
this is a very small number (Liedtke et al. 2014). This
even assumes that females are mature three months after
their birth and mate at the end of the rainy season of the
same year. Depending on the length of the rainy season,
between 30% and 70% of the respective year’s newborn
females become mature, nevertheless, the range indicates
that an equal number of females become mature only the
following year (Angel and Lamotte 1947, Lamotte and
Rey 1957, Lamotte 1959). Average female lifetime repro¬
ductive output may thus even be much smaller.

In summary: Nimba toads are endemic to the high al¬
titude grasslands above 1,200 m asl of the Nimba moun¬
tains in West Africa. Their sexual cycle and their activity
are strongly linked to the local seasonality. They spend
the dry season underground (4-7, on average 6 months)
and they are active only during the rainy season. The ac¬
tive time covers the last three months (range 2-5 months)
of the gestation and about three months between gesta¬
tions. All Nimba toad males and 30-70% of females be¬
come mature within three months, the remaining females
within 15 months. The female life-time reproductive out¬
put is very low with a maximum of 20-32 offspring.

Mating

Generally females are larger than males (females: SVL:
15-27 mm, Xavier 1971, 1986, 2009, Lamotte and Xavi¬
er 1976b, males: SVL: 15-23 mm, Lamotte and Xavier
1976b, Xavier 1986,2009). Males have a darker back (Le
Quang Trong 1967) and during most of their active above
ground life recognisable nuptial pads (Angel and Lamotte
1947, 1948). Nuptial pad development is linked to sper¬
matogenesis (Zuber-Vogeli and Xavier 1965, Zuber-Vo-
geli 1966), and can be observed in males with an SVL of

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

Figure 4. Female and male cloaca of Nimba toads and a pair in
amplexus. The female cloaca (top left) is close to the urostyle,
whereas the male cloaca (top right) is ventrally oriented. During
mating it swells and encloses the female cloaca. During the am¬
plexus lumbalis the female is constantly horizontally swaying
(bottom).

only 13 to 14 mm (Angel and Lamotte 1948). The most
important secondary sex ditference, however, is the posi¬
tion of the cloaca (Angel and Lamotte 1947, Xavier 1971,
1986). The female cloaca is very close to the urostyle,
whereas the male cloaca is more ventrally positioned and
the distance to the urostyle is larger (Figure 4; Angel and
Lamotte 1947, 1948, Xavier 1971).

Mating occurs without a copulatory organ (Angel and
Lamotte 1947, Xavier 1971, 1986). Sperm transfer is as¬
certained by cloacal apposition (Xavier 1971), in which
the male cloaca swells and encloses the female cloaca
(Angel and Lamotte 1948, Xavier 1971). In contrast to all
other bufonids amplexus is lumbal and is accompanied by
a particular behavioural repertoire, described by Xavier
(1971): males crouch on their front legs and as soon as
the female moves, follow her and grab her tightly in the
groin. This is supported by the spines of the nuptial pads
on the males’ thumbs and first fingers. Females are often
injured by these nuptial pads during mating. As soon as
the female is grabbed she starts swaying from one side
to the other without cease. Mating occurs mainly during
the day and may take several hours to more than one day
(Xavier 1971). If mating occurs during the night it is in¬
terrupted by torch light (Angel and Lamotte 1948).

Due to the long duration of mating, it was assumed
that Nimba toads may ovulate during this time (Lamotte
et al. 1956). However, it was later shown that females,
if kept without males, also ovulate (Xavier 1974). The
unfertilised eggs are kept within the enlarged distal end
of the oviduct and a pseudo-gestation develops (Xavier
1969, 1971, 1974). In some other amphibians with inter¬
nal fertilisation, a receptaculum seminis (spermatheca)
can be found (Wake 2015a). In Nimba toads fertilisation
quite likely occurs within the upper part of the oviduct,
but no receptaculum seminis nor any other accumulation

of sperm in any part of the oviducts was found (Xavier
1971). Nevertheless, in 25% of Nimba toad litters more
than one sire is needed to explain the genotypes found
(Sandberger-Loua et al. 2016b).

In summary: mating occurs without specialised copu¬
latory organs and sperm transfer is achieved through di¬
rect contact of the morphologically differently positioned
male and female cloacae. Mating position is an amplexus
lumbalis, being exceptional within Bufonidae. No recep¬
taculum was found, nor any other accumulation of sperm,
nor indication of ovulation induced by mating. Mating
takes several hours and polyandry occurs.

Matrotrophy

Nimba toad eggs are very yolk poor and with a diameter
of 500-600 pm (on average 540 pm, Vilter and Lamotte
1956, Vilter and Lugand 1959b, Lamotte et al. 1964, Xavi¬
er 1971, 1986) and a weight of 220 pg (Xavier 1971), par¬
ticularly small. Newborn toadlets on the other hand, have
an average SVL of 7.5 mm (Lamotte and Xavier 1976a,
Xavier 1977, range: 6-10 mm, Angel and Lamotte 1944b,
Lamotte and Rey 1957, Xavier 1971), this is one third of
the mother’s SVL (Lamotte et al. 1956, Xavier 1971), and
an average weight of 45 mg (range: 30-60 mg, Xavier
1971,1977, Lamotte and Xavier 1976a, 1976b). In a fami¬
ly-wide analysis of African bufonid egg sizes, Nimba toad
eggs were described as being exceptionally small and well
below the average egg size for other species of compara¬
ble adult size (Liedtke et al. 2014). Two anurans of similar
adult size are, for example, the direct developing Arthro-
leptis crusculum (SVL < 20 mm, Guibe and Lamotte 1958)
and the lecitotrophic Nectophrynoides tornieri (SVL: 25-
27 mm, Angel and Lamotte 1948). In Arthroleptis crus¬
culum, eggs are 3.5 mm in diameter (Guibe and Lamotte
1958, 7x the size of a Nimba toad egg) and newly hatched
juveniles have a SVL of 5 mm (0.67x the size of Nimba
toad toadlets). In Nectophrynoides tornieri, eggs measure 2
mm in diameter (4x the size of a Nimba toad egg) and new¬
born juveniles 5.4 mm (Lamotte and Xavier 1972a, 0.72 x
of Nimba toad toadlets). Hence, metamorphs in the direct
developing species are 1.4 times larger than the egg, in the
viviparous, lecitotrophic toad 2.7 times larger and in the
matrotrophic Nimba toad 15 times larger than the egg. This
huge increase in size from egg to juvenile and particularly
in weight (Nimba toad juveniles are > 200 times heavier
than the eggs, Vilter and Lugand 1959b, Xavier 1971), re¬
quires energy, which has to be provided by the mother.

Matrotrophy is characterized by the transport of (nu¬
tritional) energy from the mother to the foetus. It is chal¬
lenging to prove this process, nevertheless matrotrophy
was very early (Vilter and Lugand 1959b) assumed in
Nimba toads. No placentation occurs (Xavier 1971, Lam¬
otte and Xavier 1976b), but matrotrophy was first linked
to the observation that within the oviductal liquid micro¬
scopic whitish droplets were observed (“uterine milk”,
Vilter and Lugand 1959b). These were likewise found in
the vacuoles within oviductal epithelium cells (Vilter and

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Figure 5. Foetal labial papillae. Labial papillae are forming
during stage la (left) and are well developed at stage Ib (right).
See foetal development for more information on developmental
stages. Redrawn after Lamotte and Xavier (1972b).

Lugand 1959b). Additionally it was observed that very
early during the foetal development labial papillae appear
(Figure 5) and foetuses have well developed intestines
and livers very similar to adults early on (Angel and Lam¬
otte 1944b). The hypothesis thus was that foetuses feed on
the liquid “uterine milk” via the labial papillae (Vilter and
Lugand 1959b, Xavier 1971, Lamotte and Xavier 1976b).
To prove the nutritional transfer from mother to foetus,
Xavier (1971) injected radioactively marked amino acids
into gestating females. Six percent of these radioactively
marked amino acids could be detected within 30 hours in
the foetuses. They first were detectable in the digestive
system, then in the very large liver and after 48 hours, in
foetal muscle and brain tissue (Xavier 1971, 1977, 1986).
This indicates that amino acids from the mother are trans¬
ferred to the foetus and that they enter the foetus through
the digestive system. This supports the hypothesis that
mucoproteins are synthesised and released by the distal
oviduct epithelium cells that form nutrients that are being
fed upon by the foetuses with their labial papillae. The
exact function of the papillae is unknown. Nevertheless,
temporally they are linked to the presence of white drop¬
lets and it can be speculated that they are used to mechani¬
cally induce the mucoprotein secretion. It was also shown
that well-nourished females gave birth to larger juveniles
than under-nourished females (Xavier 1971), which pro¬
vides additional supporting evidence for the importance
of maternal nutrient transfer to the developing foetuses.

Another possibility to transfer nutrients from the
mother to the foetuses is the ovulation of unfertilised
eggs, or intra-oviductal cannibalism of other foetuses
(Wake 2015a). Nimba toad follicles develop into cor¬
pora lutea after ovulation and persist for the time of
gestation (Lamotte and Rey 1954, Lamotte et al. 1956,
1964, Xavier 1970b) and hence, the number of ovulated
eggs can be compared with the number of foetuses in
the oviduct (Lamotte et al. 1964). Usually all of the ovu¬
lated eggs develop into foetuses, but up to three more
corpora lutea than foetuses were observed (Lamotte et
al. 1964). While cannibalism or feeding on unfertilised
eggs and other foetuses cannot be completely ruled out,
it is unlikely to constitute a major source of nutrients to
the developing foetuses.

In summary: newborn Nimba toads are 15 times larg¬
er and > 200 times heavier than the egg. It was shown
that marked amino acids injected into mothers are detect¬
able within 30 hours in the foetal digestive system and
liver. This supports the hypothesis that foetuses take up
their nutrition through the very early developed digestive

system and nutrition is provided by oviductal epithelial
mucous cells. Additionally, matrotrophy is supported as
foetal size at birth is linked to environmental conditions
during the last third of the gestation period, during which
females are active and most of the foetal growth occurs.

Parturition

Parturition may take several hours to over two days, de¬
pending on the number of offspring (Xavier 1971, La¬
motte 1982). Juveniles are either born legs or head first,
on their venter or on their back, depending on the position
they had within the distal end of the oviduct (Xavier 1971,
1986). At the end of gestation nearly all of the body cavity
of the female is occupied by the oviducts (compare Fig¬
ures 3 and 6a), severely restricting all other organs (Angel
and Lamotte 1944a, Vilter 1956a, Xavier 1971). At this
stage, the distal end of the oviduct becomes very stretched
and the wall, especially the muscle layer, is very thin and
supposedly too thin and weak to induce labour (Angel and
Lamotte 1944a, Vilter 1956a, Xavier 1971). In any case,
the injection of labour inducing pharmaceuticals had no
effect on gravid N. occidentalis (Vilter 1956a). V. Vilter
(1956a) was the first to observe females giving birth and
developed a scenario on how birthing is achieved. Fe¬
males press their thighs to their flanks, the feet are further
away from the body, the two legs building a double W and
are in that way supporting the pressure on the flanks (Fig¬
ure 6b, c). V. Vilter (1956a) hypothesised that with their
lungs (possibly too small and simple, Angel and Lamotte
1944b, compare Figure 7) and with some muscle support
they are at the same time increasing the intraperitoneal
pressure on the distal end of the oviduct from the crani¬
al direction. The whole body is pressed to the ground,
barring oviductal extension towards the ground. Vilter’s
(1956a) hypothesis is that with this posture the female is
restricting the space within the oviduct and forces the ju¬
veniles to take the “only possible way out”, through the
cloaca. As support for his idea he claims that females just
before or after giving birth are more sensitive to light
(smaller pupils when exposed to light than females sever¬
al weeks before giving birth). This would make them seek
out shelters offering suitable support for the “birthing pos¬
ture” and protecting them during birthing (Vilter 1956b).

There is indication that first all juveniles from one and
only thereafter from the other oviduct are born (Xavier
1971). The passage through the cloaca is very fast (a few
seconds), but if parturition is interrupted at this stage the
juvenile dies, if juveniles already die within the oviduct
they will stay there until the mother dies of sepsis (Xavier
1971). These latter observations indicate an active part of
the juveniles during parturition.

In summary: Nimba toad females have not enough
muscle power in their oviducts to induce labour. Hence,
they induce birth through a unique “birthing posture”. If
foetuses die within the oviduct or during parturition, they
may not be evacuated, hinting at necessary juvenile activ¬
ity during parturition.

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

Figure 6. “Birthing posture” in Nimba toads. A: gestating Nim¬
ba toad; the grey shading indicates the size and position of the
enlarged distal parts of the oviduct (uterus), B: shows the “birth¬
ing posture”, in which females build a double W with their legs
and increase pressure on their uteri. Compare the position of
legs on the photograph on the right (C) of a female giving birth,
showing likewise the double W, of the legs. A and B are re¬
drawn after Vilter (1956a).

Foetal development

Aquatic tadpoles of other anurans generally have a tail,
with more or less pronounced fins, first external and later
internal gills, a coiled gut, a spiracle, and mouth parts (i.e.
homy beaks, labial teeth (keratodonts) and labial papil¬
lae, Altig and McDiarmid 1999, Channing et al. 2012).
Nimba toad foetuses have a large square head and large
eyes (Angel and Lamotte 1944a). They have neither in¬
ternal nor external gills, nor spiracle, nor coiled gut and
neither keratodonts nor horny beaks at any time during
their development (Angel and Lamotte 1944a, 1944b,
Xavier 1971, 1986, Lamotte and Xavier 1976a, 1976b).
Their tails have very narrow fins and for most of the time
they possess labial papillae (Angel and Lamotte 1944a,
1944b, Xavier 1971, 1977, 1986). The gut and the large
and well developed liver are already adult-like relatively
early during development (Figure 7, Angel and Lamotte
1944b). These peculiarities of the foetal morphology pre¬
clude the application of Gosner stages (Gosner 1960) usu¬
ally used to describe early anuran development (Xavier
1971). Therefore, we use herein the eight stages for the
foetal development defined and used by Zuber-Vogeli and
Bihoues-Louis (1971), Lamotte and Xavier (1972b) and
Lamotte et al. (1973). For the different stages see Figure 8.

Figure 7. Foetal digestive system. Exceptional for an anuran
foetus is the straight and differentiated gut, with an oesophagus,
the transparent and the dark intestines (stomach) and a rectum,
as well as the large liver lobes. Additionally, shown are small
lungs (as well small in adults), the heart, kidney and gonads.
Redrawn after Angel and Lamotte (1944a).

Stage 0

Stage 0 is the earliest described stage; it has a duration
of less than two months. At stage 0 foetuses have a tail,
some yolk is still visible, no eyes, no pigmentation and
no cloacal opening. During this stage the intestines are
forming. Foetus size varies between 1.0-2.7 mm (body:
0.6-1.4 mm, tail: 0.4-1.3 mm, Lamotte and Prum 1957,
Lamotte and Xavier 1972b). Gonocytes (foetal germ
cells) are already identifiable and large (range 25-55 pm,
most 30^0 pm), and they assemble in a line between the
aorta and the Wolffian ducts (Lamotte et al. 1973).

Stage la

Stage la has a duration of less than two months. Some
yolk is still visible in early stage la foetuses but com¬
pletely resorbed in older specimens. During this stage
the head develops fast, the eyes appear and become
pigmented, the mouth, first visible as a depression, de¬
velops into a slit and connects to the oesophagus, and
papillae appear on the lower and upper lip (Lamotte and
Xavier 1972b). The lobes of the liver become visible
and the first pigmentation appears, hind limb buds are
still absent (Lamotte and Xavier 1972b). Body size is
on average 1.6 mm, tail length 1.9 mm. All gonocytes
migrate into the periphery of the primordial gonads. Go¬
nads are longer than wide and built stalks. A renal stalk
protrudes into the gonad. At the end of stage la sex dif¬
ferentiation occurs, and all intracellular vitelline flakes

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113

1 1

i;:’

)

2 mm

1 V

y -

■ /'

1 '

1 1 "

2 mm

stage 0

• »

stage la

2 mi

stage lb

3 mm

)

I y I

y !
/

\ " \
\

stage 2a

< b 3 mm

stage 2 b

3 mm

4A ^

stage 3b

3 mm

stage 3a

0.0 mm

1.0 mm

• 2.0 mm

■ 3.0 mm

5.0 mm

3 mm

stage 4

10 mm

Figure 8. Embryonic development. Shown are the eight stages as found in the literature. Redrawn after Lamotte and Xavier (1972b).

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

are resorbed (Lamotte et al. 1973). Within the pituitary
gland the pars distalis, pars intermedia, pars tuberalis
and the nervous lobe are differentiated (Zuber-Vogeli
and Bihoues-Louis 1971).

Stage Ib

Stage Ib has the longest duration (about two months). It is
eharaeterised by the appearanee of the hind limb buds and
their separation into thigh and lower leg. Front limbs de¬
velop under the transparent opercular skin fold. Pigment
cells start to appear on the flanks. The digestive system
and large liver-lobes are well developed (Lamotte and
Xavier 1972b). Total length of foetuses varies between
3.8-6.2 mm (body: 1.8-2.4 mm, tail: 2-4 mm, Lamotte
and Xavier 1972b). The small ovaries (200-300 pm) are
pear-shaped and stalked, sometimes with a central ca¬
vity. They contain oocytes and oogonia in pre-meiosis,
which are arranged in the periphery of the ovary. During
this stage the first follicle cells appear and some oogonia
start growing. The testes have a compact appearance, are
small (300 x 70 pm) and become more elongated. The
cells within the testes show no apparent order, but large
spermatogonia can be observed (Lamotte et al. 1973).
Within the pituitary gland the first glycoprotein type 1, 2
and 3 cells, and protein type 1 cells appear (Zuber-Vogeli
and Bihoues-Louis 1971, Zuber-Vogeli and Doerr-Schott
1984). The latter are distributed in all areas of the pars
distalis (Zuber-Vogeli and Doerr-Schott 1984). For cell
type descriptions see the section on the (female) pituitary
gland below.

Stage Ila

This stage has a duration of about one month and its be¬
ginning coincides with the emergence of females from
their underground aestivation sites. It is characterised by
the further differentiation of the hind limbs into thigh,
lower leg and foot. The limbs are still short, and at the
end of this stage the toes appear but are not separated.
Foetuses of this stage have a large liver and the cloacal
tail piece (sensu Gosner 1960) is still present. A clear
boundary between body and tail becomes apparent; the
eyes protrude and increase in size. Pigment cells increase
in number; the pigmentation starts intensifying at the
head and the darker colour arrives in the middle of the
back at the end of this stage, the dark circles at the flanks
persist. The hind limbs begin to be dorsally pigmented
(Lamotte and Xavier 1972b). Foetus size varies between
6.4 and 12.5 mm (body 2.4-5.3 mm, tail 4-7.5 mm, hind
limbs: 0.9-3.4 mm, Lamotte and Xavier 1972b). The ova¬
ry continues increasing in size, oocytes increase in num¬
ber and their cytoplasm increases in volume (Lamotte
et al. 1973). During this stage glycoprotein type 2 cells
(corticotropic cells) and melanotropic cells are present in
the pars distalis and pars intermedia. Protein type 2 cells
(somatotropic cells) were rare before but appear in this
stage in the dorso-caudal region of the pars distalis (Zu¬
ber-Vogeli and Bihoues-Louis 1971).

Stage Ilb

This stage has a duration of less than one month. It is
characterised by the elongation of the limb and to a less¬
er extent by their differentiation. The metatarsal tubercle
appears, toes become separated and the front limbs con¬
tinue developing beneath the opercular skin fold and start
distending the thin membrane. The eyes grow quickly
and the pupil appears. The mouth is still surrounded by
papillae (Lamotte and Xavier 1972b). At this stage the
pituitary gland changes, becomes spherical, the sinus of
the pars distalis becomes extended; the position of the
pars intermedia is modified as the median protuberance
is thickening. Mitoses of the glycoprotein type 1 cells are
observed (Zuber-Vogeli and Bihoues-Louis 1971). About
1/10 of the surface of the thyroid gland becomes vascu-
larised (Lamotte and Prum 1957).

Stage Ilia

This stage has a duration of a few weeks. It is
characterised by the start of the tail resorption, the
rupture of the opercular skin fold and the breaking
through of the front limbs. Front and hind limbs are
coloured dorsally with the species-specific stripes. The
head elongates, nares are visible, the pupils are further
developed and the labial papillae start to decrease in
size (Lamotte and Xavier 1972b). Some of the oogonia
continue growing until the first ovulation. Within testes
spermatocytes start maturing, conjunctive tissue appears
which builds the basis of the future seminiferous lobules.
The intra-testicular oocytes, present in low numbers until
that stage, start decreasing in size (Lamotte et al. 1973).
Protein type 1 cells and glycoprotein type 1 cells are still
visible and distributed in all areas of the pars distalis, but
for the latter secretory activity is reduced (Zuber-Vogeli
and Doerr-Schott 1984).

Stage mb

This stage has a duration of a few weeks. It is character¬
ised by the resorption of the tail and the labial papillae.
The head becomes more elongated; the pupils are fully de¬
veloped. Foetuses already show the characteristic juvenile
colouration (Lamotte and Xavier 1972b). The ovaries are
large (300-600 pm, Lamotte et al. 1973). The activity of
the glycoprotein type 1 cells is reduced, glycoprotein type
3 cells are very active and protein type 1 cells, melanotrop¬
ic and protein type 2 cells still present (Lamotte et al. 1973,
Zuber-Vogeli and Doerr-Schott 1984). The thyroid is high¬
ly vascularised (1/3 of the surface) and the colloid amount
reduced drastically (Lamotte and Prum 1957).

Stage IV

This stage has a duration of just a few days. At this stage
foetal development is completed, the juvenile toads are
a bit stockier and have slightly longer extremities and
proportionately larger eyes compared to adults. Labial
papillae are absent, the nares moved lateral. SVL rang-

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115

es between 6-10 mm, hind legs ca. 9 mm, front legs,
5.6 mm and on the feet all tubercles are visible (Lamotte
and Prum 1957, Lamotte and Xavier 1972b). Large oo¬
cytes grow particularly fast before birth. Some lobes are
present in testes; the first vascularised interstitial tissue
appears; Sertoli cells appear at the beginning of the sec¬
ond cycle of meiosis. Most often spermatocyte matura¬
tion begins with birth, nevertheless spermatogenesis was
observed even before birth (Lamotte and Prum 1957, La¬
motte et al. 1973). Thyroid activity increases again within
this stage (Lamotte and Prum 1957). The pituitary gland
of newborn toads does not differ from the pituitary gland
of adults (Zuber-Vogeli and Bihoues-Louis 1971).

In summary: Nimba toad foetuses are characterised by
the absence of a coiled gut, internal and external gills,
spiracle, horny bill and labial teeth, and the presence of
a gut similar to those of adults, large livers, a large head
with large eyes, a mouth with papillae and the early de¬
velopment of the reproductive, locomotor, digestive, and
respiratory systems. The foetal development is linked to
the different seasons experienced by the adults. During
the first 5-6 months, the time mothers spend underground
during the dry season, development is slow (stages 0-IIa,
Xavier 1971, 1986, Lamotte et al. 1973, Lamotte and
Xavier 1976b). Foetal development and growth is accel¬
erated from the moment of emergence and the start of the
active life of females (Xavier 1971, 1986, Lamotte et al.
1973, Lamotte and Xavier 1976a).

Figure 9. The female reproductive system. Redrawn after La¬
motte et al. (1964).

Female reproductive system

Within this section the morphology and temporary chang¬
es of the oviduct, ovary and the pituitary gland are de¬
scribed and their possible interactions are discussed. The
most complete description of the female reproductive
system is given in the doctoral thesis of Xavier (1971).

Oviduct

The oviduct is rather simple, it consists of two parallel
strings (Figure 9, Lamotte and Tuchmann-Dubplessis
1948, Xavier 1971, 1986), which can be separated into
three parts: each string in the tube or oviduct sensu stric-
to, the uterus, which is the lower enlarged part, in which
the foetuses develop (non-homologous to the mammalian
uterus) and the common tube, a short tube which unites
the lower-most part of both uteri (Xavier 1971, 1976).

Tube or oviduct sensu stricto. The tube consists of an
inner epithelium, a connective tissue, a thin muscle layer
and is surrounded by a thin envelop (Xavier 1971). The
epithelium is ragged and two cell types can be distin¬
guished, ciliated cells and mucous cells. Based on histol¬
ogy and the epithelial secretions produced, the tube can
be separated into four parts (from anterior to posterior): i)
a ciliated part, ii) a part in which mainly acidic secretions
occur, iii) an acidic and neutral part, in which acidic and
neutral secretions are observed and iv) a neutral part with
exclusively neutral secretions (Xavier 1971, 1973).

Within a reproductive cycle the tube changes little. It
is hypertrophic and active only before and during ovula¬
tion (diameter between 350-450 pm, Vilter 1957) at the
end of the rainy season (Vilter 1957, Xavier 1971, 1973,
1974,1976,1986, Lamotte and Xavier 1976a). After ovu¬
lation activity stops and the tube diameter decreases in
size until it reaches its thinnest diameter during dormancy
(Vilter 1957, Xavier 1971). Some weeks after emergence,
activity is slowly taken up again, but only speeds up some
weeks after parturition (diameter at parturition: 100-110
pm) for the preparation of the new ovulation (Vilter 1957,
Xavier 1971, 1974). During gestation the tube does not
change much (Lamotte and Tuchmann-Dubplessis 1948,
Xavier 1971).

Uterus. As a modification of the tubular oviduct sensu
stricto, the uterus also consists of an epithelium, connec¬
tive tissue, a thin muscle layer and an envelope (Lamotte
and Tuchmann-Dubplessis 1948, Xavier 1971). Depend¬
ing on the season only mucous cells or mucous and ci¬
liated cells can be recognised (Angel and Lamotte 1948,
Lamotte and Tuchmann-Dubplessis 1948, Xavier 1971,
1973, 1986). Some weeks after birthing the uterus is 2-3
mm long, 0.5-1 mm wide and 0.5 mm high (Xavier 1971),
just before ovulation it already increased in size to 3-4
mm length, 1-2 mm width and 0.5-2 mm height (Angel
and Lamotte 1948, Lamotte and Tuchmann-Dubplessis
1948, Xavier 1971). During the last months of gestation
the uterus is very large, filling most of the abdomen and
squeezing all other organs (Lamotte and Tuchmann-Dub-

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

plessis 1948, Xavier 1971). Within one reproductive cycle
three phases can be distinguished: a proliferation phase,
starting 12 days after parturition and lasting until ovula¬
tion, a secretion phase, starting with ovulation and ending
with parturition and an apoptosis phase during the first 12
days after parturition (Xavier 1971, 1973, 1977, 1986).

The proliferation phase starts in July/ August when the
new epithelium is built from the connective tissue (Xavier
et al. 1970, Xavier 1971), at first ciliated and mucous cells
are present and within mucous cells mitoses can be ob¬
served (Xavier 1971, 1973, 1986). At the same time blood
vessels appear during the first gestation and increase in
number in the following gestations (Xavier 1971, 1986).
In September, shortly before ovulation, the ciliated cells
disappear, the epithelium is folded into longitudinal ridges,
blood vessels form within the ridges of the epithelium, be¬
tween the connective tissue and epithelium (Xavier 1971).

The secretion phase lasts the entire gestation period
and is characterised by the secretion of mucoproteins by
all mucous cells. Nevertheless, the importance of various
factors changes over the duration of the gestation. During
the first part of the gestation, mainly within the first part
of dormancy, the muscle layer increases, the vascularisa-
tion of the connective tissue increases and mitoses can be
observed (Angel and Lamotte 1948, Xavier 1971, 1977,
1986, Lamotte and Xavier 1976a). At the end of the ges¬
tation, when foetuses are at stages III and IV (the time the
labial papillae start being resorbed, Xavier 1971, Lamotte
and Xavier 1972b) the secretion of mucoproteins decreas¬
es and glycoproteins are secreted and the blood vessels
open into the uterine cavity (Xavier 1971, 1973, 1986).

The apoptosis phase is the shortest and lasts only for
about 12 days (Xavier 1971, 1973, 1986), nevertheless it
has the largest impact on the uterus. After parturition the
uterus collapses, the muscle layer and the connective tis¬
sue are arranged in lateral folds, but the epithelium shows
no structure after collapse (Vilter and Lamotte 1956). The
reason for the different reactions is that the epithelium de¬
taches from the connective tissue and is finally phagocyt-
ised within the uterine cavity (Xavier 1971, 1973, 1976,
1977, 1986). The secretion of glycoproteins, starting al¬
ready at the end of the secretion phase, is intensified and
this leads to the disconnection of the epithelium (Xavier
1971,1973,1977,1986). At the same time, the bloodves¬
sels are surrounded and phagocytised by many mast cells,
and from the connective tissue a new epithelium is build¬
ing (Xavier 1971, 1973, 1977, 1986). After 12 days the
uterus has the same appearance as that of virgin females,
the epithelium is ragged, contains mucous and ciliated
cells, and some mitoses can be observed.

Common tube. The common tube consists of an epi¬
thelium, connective tissue, a muscle layer and an enve¬
lope. The muscle layer is thicker than in the oviduct sensu
stricto. It follows the cyclic changes of the uterus, with
the only exception that the apoptosis phase and the gly¬
coprotein secretion are missing. The transition from the
secretion to the proliferation phase is achieved as ciliated
cells appear (Xavier 1971).

In summary: the oviduct is separated into the tube,
the uterus (distal end of the oviduct) and the common
tube. The tube is only active before ovulation and hence,
changes the least of the three parts. The uterus supports
the foetuses during gestation, undergoes the largest size
changes, and rebuilds its epithelium after every gestation.
The common tube follows a similar development as the
uterus, but is missing the apoptosis phase, in which the
epithelium is completely exchanged.

Ovary

The ovaries are situated in the posterior third of the body
(Xavier 1971). They are small, of irregular shape (1-2.5
mm wide and 0.5-1 mm large, Xavier 1971, 1974) and
have a weight of 0.15-0.75 mg (Xavier and Ozon 1971).
They contain oogonia and follicles of different sizes, the
total number rarely exceeding 60 (Angel and Lamotte
1944b, Lamotte and Rey 1954,1957, Lamotte et al. 1964,
Xavier et al. 1970, Xavier 1974). Not all eggs are ovulat¬
ed at the same time; 4-20 eggs, most often 8-9 eggs, per
ovulation were observed (Angel and Lamotte 1944b, La¬
motte et al. 1964, Xavier 1971, 1977, 1986). The number
of ovulated eggs depends on the female’s size (age), with
larger females ovulating more eggs. First-gestating fe¬
males may ovulate 1-8 eggs, whereas older females may
ovulate between 14-18, and the largest females up to 20
eggs (Lamotte et al. 1964, Xavier 1971, 1986).

Follicles consist of a theca layer and granulosa cells
(Xavier 1971, 1977, 1986). Most follicles in an ovary
have a size between 150-200 pm diameter (Angel and
Lamotte 1944a, 1944b); mature follicles on the other
hand are larger with a diameter of 500-650 pm (Lamotte
and Rey 1954, Lamotte et al. 1956, Xavier 1971). At birth
oocytes all have the same size (< 220 pm) but within
fast-developing females during mating season two types
of follicles can be observed, the majority is < 300 pm
and a few are mature with a size between 500-620 pm
(Lamotte and Rey 1957).

After ovulation, follicles decrease slightly in size
(280-320 pm diameter, Lamotte and Rey 1954) and
develop into corpora lutea (Lamotte and Rey 1954,
Lamotte et al. 1956, Vilter and Lugand 1959a, Xavier et
al. 1970, Xavier 1971, 1974, Lamotte and Xavier 1976a).
A corpus luteum develops when granulosa cells invade
the follicle cavity and the theca thickens (Lamotte and
Rey 1954, Xavier 1971, 1974). The corpora lutea persist
during the entire gestation (Lamotte and Rey 1954,
Lamotte et al. 1956, Vilter and Lugand 1959a, Xavier et
al. 1970, Xavier 1971), nevertheless they decrease in size
after emergence (Lamotte and Rey 1954, Lamotte et al.
1956, Xavier 1971, 1977, 1986). Large follicles that did
not reach maturity in time, and did not ovulate their ova,
undergo atresia (Xavier et al. 1970, Xavier 1971).

Hence, within the ovary two phases can be observed, a
follicular phase, which is characterised by follicle growth,
and a luteal phase, during which the corpora lutea are pres¬
ent (Xavier and Ozon 1971, Xavier 1971, 1986, Lamotte
and Xavier 1976a). The follicular phase starts slowly with

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117

emergence, vitellogenesis takes place after parturition, and
the phase ends with ovulation (Lamotte et al. 1964, Xavi¬
er 1971, 1977, 1986). This phase is characterised by the
growth of the follicles involved in the next ovulation and
vitellogenesis (Xavier and Ozon 1971, Xavier 1971,1977,
1986). The presence and activity of 17a-hydroxylase and
3P-hydroxy-steroid dehydrogenase (Sp-HSD) was ob¬
served within the follicles, particularly before ovulation
(Ozon and Xavier 1968, Xavier et al. 1970, Xavier 1971).
Only before ovulation the theca cells of the follicles show
enzymatic activity (Xavier et al. 1970), during which oes-
trogens are produced until ovulation (Xavier 1971, 1986).
During the same time granulosa cells of the follicles pro¬
duce progesterone (Xavier and Ozon 1971, Xavier 1971,
1986). Pre-ovulation oestrogen, progesterone, as well as
4-adrostenedione and testosterone are produced within the
granulosa or theca cells of mature follicles (Xavier 1976).

The luteal phase starts with the gestation. Corpora lu-
tea decrease in size during the active life of females after
emergence, and are rapidly disappearing after parturition
(Vilter and Lugand 1959a, Lamotte et al. 1964, Xavier
1970a, 1970b, 1971,1976,1977,1986, Xavier etal. 1970,
Xavier and Ozon 1971). During the luteal phase proges¬
terone, but no oestrogen is produced (Ozon and Xavier
1968, Xavier et al. 1970, Xavier and Ozon 1971, Xavier
1971,1986). Progesterone levels are linked to number and
size of corpora lutea and hence, decrease after emergence
(Xavier et al. 1970, Xavier and Ozon 1971, Xavier 1971,
Lamotte and Xavier 1976a). Larger females with more
corpora lutea have higher progesterone levels (Xavier and
Ozon 1971, Xavier 1971). During the dry season corpora
lutea are larger and progesterone levels are high and this
time coincides with the time of slow foetal growth and
the absence of follicle growth. The two ovarian phases are
non-exclusive as both are overlapping from emergence
until parturition. Nevertheless, during this overlapping
time corpora lutea decrease in size, and follicle growth is
slow (Ozon and Xavier 1968, Xavier 1970a, 1970b, 1971,
1986, Xavier et al. 1970, Xavier and Ozon 1971).

In summary: Nimba toads have small ovaries, which
contain only few follicles (< 60), of which a small propor¬
tion (4-20) reaches maturity every year. After ovulation
follicles develop into corpora lutea, which are present
during the entire gestation period. Within follicles andro¬
gens (oestrogen and testosterone) are produced within the
theca cells, whereas the granulosa cells produce proges¬
terone. During the luteal phase, exclusively progesterone
is produced by the granulosa cells. Progesterone levels
are highest during the dry season, when foetal and follicle
development is slow or absent.

Pituitary gland

The pituitary gland is comparatively small (Vilter et al.
1959), and does not differ between virgin females and
males after emergence (Zuber-Vogeli 1968). After parturi¬
tion the volume of the pituitary decreases dramatically, but
increases again after emergence and is maximal just before
birthing (Vilter et al. 1959). Three types of glycoprotein

cells (in some publications called basophilic, amphophilic
or cyanophilic cells) and two types of protein cells (some¬
times termed acidic cells) were determined (Zuber-Vogeli
1968). Different names were used for the same pituitary cell
types, between different as well as within the same publica¬
tions. To avoid confusion and standardise usage, we use the
following names: glycoprotein type 1 cells (other names:
gonadotropic cells, basophilic PAS purple cells, gonad¬
otropic type I and FSH-cells), glycoprotein type 2 cells
(corticotropic cells, basophilic PAS red cells, gamma cells,
gonadotropic cells II), glycoprotein type 3 cells (thyrotropic
cells), protein type 1 cells (prolactin-like cells, somatotropic
cells, orangeophilic cells, alpha cells), protein type 2 cells
(prolactin-like cells, somatotropic cells, erythrosonophilic
cells). Within the two protein cell types, the challenge is
that it was first assumed that the protein type 2 cells are the
prolactin-like cells, but it was later demonstrated that they
produce somatotropin (STH, Zuber-Vogeli et al. 1975).

The glycoprotein type 1 cells are widely distributed
within the pituitary gland (Zuber-Vogeli 1968, Xavier
1971), these cells and their mitochondria are large (Zu¬
ber-Vogeli and Doerr-Schott 1976). During dormancy
glycoprotein type 1 cells are small or even absent (Zu¬
ber-Vogeli 1968, Xavier 1971, Zuber-Vogeli and Xavier
1973, Zuber-Vogeli et al. 1975). They increase in size and
activity after emergence and are most active between par¬
turition and ovulation (Zuber-Vogeli and Herlant 1964,
Zuber-Vogeli 1968, Zuber-Vogeli and Xavier 1973, Zu¬
ber-Vogeli et al. 1975). In females they are active during
the follicular phase (Xavier 1971) and in males during
spermatogenesis (Zuber-Vogeli etal. 1975). Hence, it was
assumed that they are equivalent to the gonadotropic cells.
The glycoprotein type 2 cells are scarcely found with¬
in the rostro-ventral part of the pituitary (Zuber-Vogeli
and Herlant 1964, Zuber-Vogeli and Doerr-Schott 1976),
have a well-developed Golgi apparatus and endoplasmic
reticulum (Zuber-Vogeli and Doerr-Schott 1976). These
cells are not visible during dormancy, are few and small
at emergence, and most prominent in July/ August (Zu¬
ber-Vogeli 1966, 1968). In females it was assumed either
that they may have no function (Zuber-Vogeli and Xavier
1973), or that they are corticotropic cells (Zuber-Vogeli
et al. 1975, Zuber-Vogeli and Doerr-Schott 1976). The
least is known about the glycoprotein type 3 cells. They
are scarce and had to be excluded from many studies due
to this fact (e.g. Zuber-Vogeli and Doerr-Schott 1976),
the only thing known is that they are distributed through¬
out the gland (Zuber-Vogeli and Herlant 1964).

Protein type 1 cells are large, widely distributed cells
within the pituitary gland (Zuber-Vogeli and Herlant
1964, Zuber-Vogeli et al. 1975) and are often ciliated
(Zuber-Vogeli et al. 1975, Zuber-Vogeli 1978), their
cytoplasm contains many granules (Zuber-Vogeli 1978)
and their Golgi apparatus shows activity (Zuber-Vogeli
and Doerr-Schott 1976). In the presence of artificially in¬
jected bromocriptine, the cells are smaller, have smaller
nuclei and the present granules increase homogeneous¬
ly within the cytoplasm, and M. Zuber-Vogeli (1978)

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

assumed that bromocriptine is hindering the exocytosis
of prolactin. Within non-gestating females protein type
1 cells increase in number after emergence (Zuber-Vo-
geli 1968). In gestating females protein type 1 cells are
abundant during dormancy and abundant at emergence
(Zuber-Vogeli 1968). After birth they increase in number
and have a large nucleus, large Golgi apparatus, many
mitochondria, a well-developed endoplasmic reticulum
and exocytose was observed 16 days after parturition
(Zuber-Vogeli 1978). One month after parturition they
are abundant and well developed (Zuber-Vogeli 1978).
Protein type 2 cells are more localised at the dorsal and
caudal poles of the pituitary gland (Zuber-Vogeli and
Herlant 1964, Zuber-Vogeli 1968, Zuber-Vogeli and Do-
err-Schott 1976). At the beginning of gestation the Golgi
apparatus is well visible (Zuber-Vogeli and Doerr-Schott
1976). Protein type 2 cells are abundant during dormancy,
decrease in number with emergence and disappear with
parturition (Zuber-Vogeli and Xavier 1973, Zuber-Vo¬
geli 1978). Hence, it was assumed that their presence is
linked to the presence of corpora lutea and it was wrongly
assumed that they are prolactin-like cells (Zuber-Vogeli
1968, Xavier 1971, Zuber-Vogeli and Xavier 1973). Later
it was found that they are somatotropic cells (Zuber-Vo¬
geli et al. 1975, Zuber-Vogeli and Doerr-Schott 1976).

Within one sexual cycle this means that at the be¬
ginning of the gestation glycoprotein and protein type 1
cells are present and protein type 2 cells are appearing.
Glycoprotein type 2 cells are less abundant but easily
and brightly stainable (Zuber-Vogeli and Xavier 1973).
At emergence of the females from their dormancy sites
protein type 1 cells are present, protein type 2 cells dis¬
appear, glycoprotein type 1 cells restart activity, glycopro¬
tein type 2 cells are present, and glycoprotein type 3 cells
are scarce (Zuber-Vogeli and Xavier 1973). Twenty days
after parturition protein type 1 cells increase in number
and glycoprotein type 1 cells are secreting (Zuber-Voge¬
li and Xavier 1973). One month after parturition protein
type 1 cells are abundant and the glycoprotein type 1 cells
are large and well granulated (Zuber-Vogeli and Xavier
1973). It was concluded that the pituitary is controlling the
follicle growth, ovulation and corpora lutea development
and maintenance (Vilter and Lugand 1959a, Xavier 1986).

In summary: five different cell types can be distin¬
guished within the pituitary gland, three glycoprotein cell
types and two protein cell types. The glycoprotein type 1
cells are visible and active during the toad’s active life,
follicle development and vitellogenesis. This indicates a
connection between the glycoprotein type 1 cells and the
ovarian follicular phase, which makes them gonadotropic
cells. The protein type 1 cells are well visible and active
during most of the time, with a slight decrease in activity
for some time after emergence. They had been shown to
secret prolactin.

Interaction between different organs

Within the female reproductive cycle three time periods
lead to changes within the reproductive system: i) before

toads become dormant ovulation and mating occur and
gestation starts. Within the oviduct this leads to the cease
of activity within the tube, the start of the secretion phase
within the uterus and within the ovary to the start of the
luteal phase, in the pituitary glycoprotein type 1 cells
become scarcer and protein type 2 cells appear; ii) With
emergence at the beginning of the rainy season, the uter¬
us starts to increase considerably in size as foetal growth
and development takes up speed, within the ovaries the
corpora lutea start decreasing in size, the follicles slowly
start development and within the pituitary the glycopro¬
tein type 1 cells start to appear, protein type 1 and 2 cells
become less abundant; hi) With the birth of juveniles in
June the tube increases developmental speed, the uterus
collapses and rebuilds a new epithelium, within the ova¬
ry the corpora lutea disappear and follicle growth inten¬
sifies, within the pituitary the glycoprotein type 1 cells
show very high activity, the protein type 1 cells increase
their activity as well and protein type 2 cells are absent.
Hence, the question arises, whether these changes in the
different organs are coincidences or one change is trigger¬
ing the change in another organ. To answer this question
several experiments were carried out. If not stated other¬
wise studies are described in Xavier (1971).

Ovary and foetus development. During the dry sea¬
son corpora lutea are present, large and active, and it was
shown that they produce progesterone. Foetal develop¬
ment is slow during dormancy (Xavier 1976). Ovariec¬
tomy (the surgical removal of ovaries) of females early
during gestation leads in 50% of females to parturition of
normally developed foetuses three months earlier than in
non-ovariectomised females (Xavier et al. 1970, Xavier
and Ozon 1971, Xavier 1971). In the other 50%, which
are assumed to be first-gestating females, ovariectomy
leads to abortion (see below). Implantation of proges¬
terone into gestating females after emergence leads to
normally developed foetuses, but parturition occurs 2-3
months later than in non-progesterone treated females.
This indicates that progesterone produced by the corpora
lutea slows down developmental speed of foetuses natu¬
rally during dormancy and experimentally during the ac¬
tive life of gestating females (Xavier 1970a, 1970b, 1971,
1976, 1986).

If females are separated from males during the mating
season, ovulation occurs and a “pseudo-gestation” de¬
velops (Xavier 1969, 1974). Within the first four months
the uteri are long bags (5x3 mm) containing separat¬
ed eggs and within the ovary corpora lutea develop nor¬
mally (stage 1, summarised from: Vilter and Lugand
1959a, Xavier 1969, 1971, 1974). Within the next 1 to
1V 2 months the eggs are still separated but the corpora
lutea decrease and follicles increase in size (stage 2). Af¬
ter emergence uteri are thinner (epithelium, connective
tissue and muscle layer), less transparent and the mucous
cells reduce production and later ciliated cells appear, and
the unfertilised eggs start accumulating (stage 3). The
accumulated eggs are then lysed, the mucous cells stop
secreting and the uterus changes into the same stage as

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119

for virgin females (stage 4). In general, the mucous lay¬
er is less thick and less ragged than in gestating females
and the uterus does not substantially change. The pseu¬
do-gestation is shorter than a gestation and leads to ovu¬
lation 3-4 months earlier (June) than in gestating females
(September/ October). If no fertilisation occurs a new
pseudo-gestation is established (Xavier 1974). Hence,
the absence of fertilisation and with that of foetuses leads
at first to normal developments within the ovary and the
uterus, but particularly after emergence the pseudo-ges¬
tation cycle is faster and shorter. This may indicate that
the presence of foetuses is needed for normal uterus and
ovary cycles during that period.

Ovary and oviduct. The tube’s endocrine cycle is syn¬
chronised with the follicular phase of the ovary. Follicles
and tube start slowly developing after emergence and are
most active before and during ovulation, and are not ac¬
tive during dormancy. In females ovariectomised after
parturition the tube does not show any activity towards
the end of the rainy season, usually the time of highest
activity. In females ovariectomised at about the time of
ovulation, the tube maintains high activity for the next
6 months and activity is terminated only after two years.
This indicates that the ovary is controlling tube activity
(Xavier 1971). At the time of ovulation within the folli¬
cles oestrogen is secreted by the theca cells and proges¬
terone by the granulosa cells. One year after ovariectomy
Xavier (1971) injected oestrogen, testosterone and pro¬
gesterone at the time of ovulation. She made the follow¬
ing observations: oestrogen (oestradiol) and testosterone
initiated hypertrophy and development of the epithelial
cells within the tube, the injection of progesterone initi¬
ated the thickening of the muscle layer. Only if oestro¬
gen and progesterone were injected simultaneously the
tube did show normal development during ovulation. If
first oestrogen and three weeks later progesterone was
injected this triggered the secretion of the mucous cells
within the tube. If first oestrogen and after one-month
progesterone was injected this triggered the decrease in
tube activity. Hence, oestrogen and progesterone together
are needed for normal tube development during ovulation
and progesterone is needed to stop tube activity (Xavier
1971, 1986).

Another connection between ovary and tube became
apparent by an observation of Lamotte et al. (1964). The
number of ovulated eggs in one ovary corresponds very
closely to the number of foetuses developing within the
uterus of the same side. In unilaterally ovariectomised fe¬
males, most eggs developed into foetuses in the uterus of
that side on which the ovary was still present (Figure lOA,
Xavier 1971). If one tube was closed (bound) of the same
side as the ovary was still present, most eggs developed
into foetuses in the uterus of the non-manipulated side,
and very few ended up in the bound oviduct or within the
body cavity (Figure lOB). If one uterus was removed and
females were unilaterally ovariectomised (Figure IOC) or
kept both ovaries (Figure lOD), most eggs were found
in the remaining uterus (Xavier 1971). This indicates a

Figure 10. Experiments on female ovary, oviduct and uterus
removal. Shown are the positions of eggs in the uteri after uni¬
lateral ovariectomy (A), after unilateral ovariectomy and the
connection between oviduct and uteri bound at the side with the
still present ovary (B), unilateral ovariectomy and the oviduct
and utems at the side of the still present ovary removed (C)
and the unilateral removal of the oviduct and the utems without
ovariectomy (D). The red cross indicates the ovary removed,
the red lines indicate positions where either oviduct (B) or the
uterus (C and D) were bound. The two-headed arrow with the
two red lines indicates that eggs apparently do not wander from
one uterus to the other passing the common tube. Redrawn after
Xavier (1971).

preference of eggs to be present in the uterus of the same
side than the ovary they came from. Additionally, one
uterus may host all eggs ovulated from two ovaries, and
that foetuses are not able to pass from one uterus into
the other passing the common tube, as in that case eggs
should have been present in both uteri in the experiment
shown in lOB (Xavier 1971, 1977, 1986).

The uterus does not follow the same cycle as the folli¬
cles and the tube. The largest change of the uterus is dur¬
ing gestation. Nevertheless, during the follicular phase
after parturition in ovariectomised females the injection
of oestrogen initiated the development of the mucous
layer and some blood vessels, the injection of testoster¬
one the development of the connective tissue and some
blood vessels, and the injection of progesterone the de¬
velopment of the muscle layer and an epithelium without
ciliated cells. Only if oestrogen and three weeks later pro¬
gesterone were injected together, did the uterus develop
as in non-ovariectomised females (Xavier 1971, 1986).
This indicates that the hormones produced by the ovary
are controlling uterus development between gestations.

The removal of ovaries at the beginning of gesta¬
tion leads to abortion 3-4 months after the operation in
50% of gestating females. Whether ovariectomy leads
to abortion depends on the female’s age. In all females
3-4 months old (hence, born the same year) and within
50% of females 15-16 months old, ovariectomy resulted
in abortion. In all older females the gestation continued.
As females may either get mature within 3-4 months, or

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

one year later, females 15-16 months of age may be ges-
tating for the first or the second time. Fran^oise Xavier
(1971) concludes that ovariectomy leads to abortion only
in females gestating for the first time. She links this to
the progesterone levels produced by the ovaries, before
ovariectomy. Older females show 4x higher progesterone
levels than females gestating for the first time. Fran 9 oise
Xavier assumes that a progesterone threshold needs to
be reached to trigger uterus development. Additionally,
within the uterus structures needed for gestation are in
part still present (e.g.: blood vessels) in older females, but
need to build in first-gestating females. Fran 9 oise Xavier
assumed that foetuses develop faster as progesterone is
missing and on the other hand the uterus development is
hindered. This leads to asynchrony between foetuses and
uterus in females gestating for the first time and finally to
abortion (Xavier 1970a, 1971, 1977, 1986).

After emergence, ovariectomy of gestating females
never results in abortion, irrespective of the female’s age.
This indicates that at this stage of the gestation the ovary
has no longer an important effect on gestation (Xavier
1971, 1986, Zuber-Vogeli and Xavier 1973).

Hysterectomy (the removal of uteri) at the beginning
of the gestation leads to atresia of small follicles and
the corpora lutea disappear faster. After ovulation in
non-hysterectomised females only nearly mature follicles
are destroyed by atresia. Hence, ovary and uterus are in¬
fluencing each other. To examine whether this connection
is linked to the uterus, or to the developing foetuses, foe¬
tuses were removed by caesarean section (Xavier 1971).
During early gestation the same modifications of the ova¬
ry are observed, but caesarean section after emergence
leads to a collapse and apoptosis of the uterus, similar to
that after birth, but does not change the ovaries (Xavier
1971). Considering that hysterectomy and caesarean sec¬
tion lead to atresia of small follicles, but pseudo-gesta¬
tion (see above) does not, this raises the question whether
atresia of small follicles is triggered by the traumata of
the operations, or if mating (which is missing in pseu-
do-gestating females) triggers some other development
which is similarly changed.

Ovary and pituitary gland. After ovariectomy at the be¬
ginning of gestation the glycoprotein type 1 cells are con¬
tracted and de-granulated. The protein type 2 cells, which
are normally appearing with the corpora lutea, are absent,
but protein type 1 cells are very abundant. Ovariectomy
after emergence does not lead to large changes within the
pituitary gland. Ovariectomy one month after parturition
leads to the degranulation of the glycoprotein type 1 cells
and they develop into “castration cells”. Hence, the ab¬
sence of the ovary has the largest effect on the pituitary at
the beginning of the gestation and after parturition during
vitellogenesis (Zuber-Vogeli and Xavier 1973).

Examining the effect of the pituitary on the ovary is
much more problematic, as females die within the next
15-25 days after the flattening (destruction) of the pitui¬
tary, indicating that the pituitary has other vital functions
in Nimba toads (Xavier 1971). Destruction of the pitui¬

tary at the beginning of the gestation, leads to atresia of
small follicles >180 pm and smaller corpora lutea de¬
velop, but does not lead to abortion within 15-25 days.
Destruction of the pituitary gland after emergence leads
to abortion within the next six days. As the destruction of
the pituitary obviously has lethal effects on the female,
F. Xavier hypothesised that abortion might be linked to
the large energy demands of foetuses during that period,
which cannot be supplied by the injured female. Destruc¬
tion of the pituitary just before parturition has no negative
impacts on parturition or foetuses (Xavier 1971).

Summary of interactions. The ovary seems to have the
largest effect on the other reproductive organs from June
to emergence at the beginning of the rainy season. Nev¬
ertheless, the ovary has different functions between par¬
turition and ovulation (vitellogenesis) and during the first
six months of the gestation females rest underground (dor¬
mancy). During vitellogenesis follicles grow and develop
quickly and they synthesise oestrogen, testosterone and
progesterone. Ovariectomy at the beginning of this period
hinders the development of the oviduct - tube and uterus.
This non-development can be circumvented with the injec¬
tion of oestrogen and progesterone, indicating, that these
hormones are vital for oviduct development during vitel¬
logenesis. As well within the pituitary gland, glycoprotein
type 1 cells (gonadotropic cells) develop into “castration
cells” if the ovaries are removed at the beginning of vi¬
tellogenesis. During dormancy the corpora lutea are large,
numerous and active and synthesise progesterone. Proges¬
terone slows foetal development during dormancy and if
experimentally applied as well after emergence. Ovariec¬
tomy of first-gestating females leads to abortion, which
was as well linked to lower progesterone levels in first-ges¬
tating, than in older females. Within the pituitary protein
type 2 cells appear with the development of corpora lutea.
In neutered females they are absent during the whole dry
season. Hence, most of the year the ovary influences the
development of the pituitary gland, the tube and the uterus
and during dormancy as well foetus development.

Between emergence and parturition foetuses develop
quickly, stretching the uterus and restricting the other or¬
gans within the female. This development is only stopped
by the destruction of the pituitary gland, which is lethal
to females. Development can be slowed down by the in¬
jection of progesterone. On the other hand, the absence of
foetuses in pseudo-gestating females leads to faster de¬
velopment of the ovary (decrease of corpora lutea and de¬
velopment of follicles), but has no effect on the pituitary
gland. If foetuses are removed through caesarean section
after emergence, with the apoptosis phase the uterus starts
a new cycle, earlier than in normally gestating females.
These results are in accordance with the hypothesis that
the presence and development of foetuses are important
for normal development of ovaries, and through them on
the oviduct and the pituitary gland. On the other hand,
change of the females from the inactive, low nutrition life
underground to an active high nutrition life above ground
and external factors might be important too.

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Male reproductive system

The reproductive system of Nimba toad males received
less attention than that of females. Respective research fo¬
cused more on the environmental and cyclic dependencies
of the reproductive cycle than on morphology and phys¬
iology of the reproductive system. Primary publications
are by M. Zuber-Vogeli (Zuber-Vogeli and Xavier 1965,
Zuber-Vogeli 1966) and J. Gavaud (Gavaud 1976a, 1977).

Nimba toad males lose at 13 mm SVL their juvenile
colouration (Angel and Lamotte 1948) and become ma¬
ture already about 3 months after they are born. They are
much more active than females, mainly calling, fighting
with other males and harassing females (Sandberger-Loua
et al. 2016b). This more active behaviour of males could
increase their predation risk and lead to higher energetic
costs. Males have a positive energy budget only between
emergence and July. During the mating season and par¬
ticularly the dry season, males lose up to 30% of their
body weight, attributed to lower food intake rates (La¬
motte 1972).

In summary: males have been studies less than fe¬
males; are smaller, darker and at least during the mating
season more active than females. Due to their more active
life-style they may suffer from higher predation pressure
and possibly as well higher energy demands.

Testes

Nimba toad testes are small (< 2 mm) ovoid masses (Ga¬
vaud 1976a), situated in the dorsal body cavity and con¬
nected to the kidneys (Gavaud 1976a) by the mesentery
(Angel and Lamotte 1948). Testes are attached to the
fat-body and the kidneys; they contain numerous effer¬
ent canals at all times, but the space they occupy within
the testes varies with the annual cycle (Gavaud 1976a).
The seminiferous tubes are filled with gonad cells, and
all but primary spermatogonia are grouped in pyramidal
cysts (Gavaud 1976a). Cysts surround Sertoli cells and
within each cyst the mitoses and meioses are synchro¬
nised (Angel and Lamotte 1948, Gavaud 1976a). Gonad
cells are attached by the Sertoli cells to the cysts (Gavaud
1976a). Only a fraction of the primary spermatogonia
develop into spermatozoa (Gavaud 1976a). Endocrine
activity through the presence of 5a-dehydrotestosterone
(5a-DHT) was observed (Gavaud 1976b) within Serto¬
li cells and some cells of the connective tissue (Gavaud
1976a). This tissue is pigmented during the dry season
and unpigmented during the rainy season (Angel and La¬
motte 1948), giving the testes a dark appearance during
the dry and a whitish appearance during the rainy season
(Gavaud 1976a).

Most bufonids have a Bidder’s organ, a part of the tes¬
tes that contains oocytes, and which is separated from the
testes by a separate envelope. During Nimba toad foetal
development testes usually contain 1 or 2 (rarely 5 or 6)
oocytes per male (Lamotte et al. 1973). Oocytes are al¬
ways positioned at the periphery and often grouped at one
of the poles of the testes, but always within the testes and

not separated by an envelope (Lamotte et al. 1973). In-
tra-testicular oocytes are small. They are not well devel¬
oped at foetal stage la and Ib, and grow slowly until stage
Ilb. Stage III is the time of accelerated spermatogenesis
and during this stage intra-testicular oocytes decrease
rapidly in size and have disappeared by stage IV (Lam¬
otte et al. 1973). Hence, in contrast to other bufonids, the
presence of oocytes in male Nimba toads is only transito¬
ry during foetal development.

The spermatozoa show no apparent modification com¬
pared to those of other bufonids. The only differences are
that the perforatorium ends slightly posterior to the aero-
some vesicle, the distal centriole is penetrated through¬
out its length by the central singlets of the axoneme and
no mitochondrial collar is present, but mitochondria are
located around the anterior axoneme (Scheltinga and Ja¬
mieson 2003). It is assumed that due to the viviparous
reproduction (and the absence of spermatheca in females
and hence presumably low levels of sperm competition)
testes are small, cysts are few and only a few spermatozoa
are produced during each mating season (Angel and Lam¬
otte 1948, Lamotte et al. 1973, Gavaud 1976a).

In summary: Nimba toad testes are ovoid masses,
which are white during the rainy and dark during the dry
season. During embryonic development the testes may
contain a few oocytes, which disappear before birth and
are never surrounded by an envelope. The seminiferous
tubes are always numerous, but vary their size during the
reproductive cycle. Most gonad cells are grouped around
Sertoli cells and within each group development is syn¬
chronised. The spermatozoon is a typical bufonid sper¬
matozoon with little modification.

Annual reproductive cycle

Male adaptations to the viviparous reproductive mode
are less distinct than in female Nimba toads; however,
the male reproductive cycle is likewise tightly linked to
the climatic cycle of the environment. Nimba toad males
have a discontinuous reproductive cycle, (Zuber-Vogeli
and Xavier 1965, Gavaud 1976a, 1976b). In contrast to
temperate anurans spermatogenesis is not triggered by
temperature, but by humidity (Zuber-Vogeli and Xavier
1965, Gavaud 1976a).

The dry season dormancy is characterised by low me¬
tabolism (Gavaud 1976a), invisible colourless nuptial
pads without spines (Zuber-Vogeli and Xavier 1965, Zu¬
ber-Vogeli 1966, Gavaud 1976a), testes and seminiferous
ducts decrease in size during the first half of dormancy
and stay the same in the second half (testes weight 0.1-0.4
mg, Zuber-Vogeli and Xavier 1965, Zuber-Vogeli 1966,
Gavaud 1976a). Some primary spermatogonia are present
(Zuber-Vogeli 1966, Gavaud 1976a, 1977) and are with
their Sertoli cells attached to the walls of the seminiferous
tubes (Gavaud 1976a). Primary spermatogonia increase
in number during the first few months of dormancy until
in mid-January when they fill 20-35%, and Sertoli cells
15-32% of the testes volume until the end of the dry sea¬
son (Gavaud 1976a). As Sertoli cells increase in num-

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

ber they detach from the walls of the testes and migrate
into the centre of the seminiferous tubes (Gavaud 1976a).
During this time secondary spermatogonia were rarely
observed (Gavaud 1976a).

In April, when males emerge, one month after females,
testes are still black and nuptial pads are not yet visible
and their fat bodies are very small (Zuber-Vogeli and
Xavier 1965, Zuber-Vogeli 1966). Most of the primary
spermatogonia are still attached to the walls with their
Sertoli cells, so that the seminiferous tubes are hollow
(Zuber-Vogeli and Xavier 1965). Larger (SVL ca.l9
mm) males may be advanced in their reproductive de¬
velopment compared to smaller males (SVL: 17-18 mm,
Zuber-Vogeli and Xavier 1965). With emergence, the
secondary spermatogonia appear (Zuber-Vogeli 1966,
Gavaud 1976a, 1977), which continue to divide until they
fill the whole testes in June (Gavaud 1977). In May testes
start increasing in size (Zuber-Vogeli and Xavier 1965,
Gavaud 1976a), and primary spermatocytes (45%), sec¬
ondary spermatocytes (25%), and spermatids (15%) fill
most of the testes volume (Gavaud 1976a). Pyknosis of
some cells can be observed (Gavaud 1976a).

In June nuptial pads start to turn black, testes increase
further in size (Zuber-Vogeli and Xavier 1965, Zu¬
ber-Vogeli 1966) and secondary spermatogonia occupy
35-55% of the testes (Gavaud 1976a), meiosis occurs
and all stages can be observed, but no secondary sper¬
matocytes nor spermatids (Zuber-Vogeli 1966, Gavaud
1976a). July/ August is the time of spermatogenesis (Zu¬
ber-Vogeli and Xavier 1965, Gavaud 1976a, 1976b), tes¬
tes continue to increase in size (Zuber-Vogeli and Xavier
1965, Zuber-Vogeli 1966, Gavaud 1976a) and nuptial
pads become more pronounced (darker and larger spines,
Zuber-Vogeli and Xavier 1965, Zuber-Vogeli 1966). At
around this time recently born males reach 13-15 mm
SVL and spermatogenesis is accelerated (Angel and La-
motte 1948). The quantity of secondary spermatogonia
decreases dramatically from about 50% to 7% of the tes¬
tes volume (Gavaud 1976a). At the same time sperma-
tozoids mature and detach themselves from Sertoli cells
(Gavaud 1976a).

During the mating season the nuptial pads are blackest
and spiniest (Figure 11, Zuber-Vogeli and Xavier
1965, Zuber-Vogeli 1966). Within the testes, mobile
spermatozoa are abundant (Zuber-Vogeli and Xavier
1965, Gavaud 1976a) whereas cysts of spermatids and
some spermatogonia are only rarely observed (Zuber-
Vogeli and Xavier 1965, Gavaud 1976a). During the
mating season only some spermatogonia divide, but
spermatogenesis does not continue (Gavaud 1976a). After
the mating season spermatozoids degenerate, nuptial
pads become transparent, testes darken and decrease in
size (Zuber-Vogeli and Xavier 1965, Gavaud 1976a) and
only divisions of primary spermatogonia can be observed
at the beginning of the dry season (Gavaud 1976a).

Similarly to females, the male reproductive cycle is
linked to three important seasonal points, the mating sea¬
son and the subsequent dormancy underground (slow or

Figure 11 . Male during the mating season, showing pronounced
nuptial pads on the thumbs. © Joseph Doumbia

no development), emergence during the next rainy sea¬
son (beginning of spermatogenesis with the appearance
of secondary spermatogonia), and in June/ July when rain
becomes permanent spermatogenesis intensifies (appear¬
ance of spermatocytes). Despite this strong link indivi¬
dual males may finish their spermatogenesis at different
times due to individual differences in developmental
speed (Zuber-Vogeli and Xavier 1965, Gavaud 1976a).
Larger males mate earlier than smaller males older than
one year (Zuber-Vogeli and Xavier 1965). As spermato¬
genesis speed is individual, this may indicate that the re¬
productive cycle is influenced by several environmental
variables and/ or internally determined. Experimentally,
Gavaud (1977) could show that spermatogenesis and par¬
ticularly its developmental speed is strongly linked to the
annual environmental cycle. Jaqueline Gavaud conduct¬
ed two experiments, one to determine important environ¬
mental variables for the slowed or stopped spermatogen¬
esis during the dry season (Gavaud 1976a), and a second
one determining the environmental variables important
for the correct timing of spermatogenesis during the rainy
season (Gavaud 1977). In these studies, she could show
that spermatogenesis depends mainly on prey availability
and humidity levels, of which negative effects could be
intensified by reversed light intensity (1000 lux during
the dry season, or 10 lux during the rainy season). She
compared the reproductive development of males within
the experiments to wild caught males. During the dry sea¬
son, comparable testes development was achieved with
nutrition once per month (50 mg), an aerial humidity of
35% and a 12h light regime at 10 lux. During the wet sea¬
son comparable development to wild males was observed
with nutrition every second day (25 mg), 90% humidity
and a light regime of 12h with 1000 lux. Generally, little
food, low humidity and less light lead to slower or no
gonad development than much food, high humidity and
much light (Gavaud 1977). The endocrine activity of tes¬
tes is highest in July. She assumes that the beginning of
spermatogenesis after emergence and the slowing down
or stopping of spermatogenesis after the mating season is
mainly influenced by external factors (nutrition and hu-

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midity, Gavaud 1976b, 1977), whereas the onset of mi¬
toses of primary and secondary spermatogonia towards
the end of the dry season is triggered by endogenous fac¬
tors (Gavaud 1976b, 1977).

In summary: the male reproductive cycle is interrup¬
ted during the dry season, when only divisions of prima¬
ry spermatogonia are observed. Only after emergence,
which is later in males than in females, spermatogene¬
sis starts and is accelerated after June, when rain is more
permanent, and results in the presence of spermatozoids
during the mating season. During the mating season only
primary spermatogonia divide. Spermatogenesis is accel¬
erated through the availability of prey and high humidity.
Nevertheless, individual males differ in the quantity and
speed of the different gonad cell stages and larger males
develop faster and mate earlier than smaller (but never¬
theless, sufficiently old) males.

Male pituitary gland

Monique Zuber-Vogeli examined the male pituitary gland
and focused on the annual reproductive cycle (Zuber-Vo¬
geli 1966). The male pituitary gland contains the same
five cell types as in females. Following the same termi¬
nology as for the female pituitary, the protein type 1 cells
are the most abundant during the entire year. She assumed
that they are somatotropic cells as in most vertebrates. As
in females the glycoprotein type 3 cells are very rare and
difficult to find. Three cell types undergo seasonal chang¬
es: the glycoprotein type 1 and 2 cells and the protein type
2 cells. The glycoprotein type 1 cells show the largest var¬
iability and are changing in accordance to the male repro¬
ductive cycle. They are less abundant or absent during the
dry season, they are abundant and contain filled vacuoles
in July (the time of most intensive spermatogenesis) and
during the mating season (Zuber-Vogeli 1966). The glyco¬
protein type 2 cells are surrounding the anterior pole of the
pituitary and are rare at emergence, but increase in num¬
ber and activity until July/ August, when nuptial pad col¬
ouration and spermatogenesis is the strongest. Monique
Zuber-Vogeli (1966) links the glycoprotein type 1 and 2
cells to the gonadotropic and the luteinising cells, respec¬
tively, described in Rana temporaria (van Oort 1961). The
protein type 2 cells are present only in June/ July when
spermatogenesis is the most active, and function is un¬
clear. Nevertheless, it seems that within the male pituitary
gland the cell types which show the largest changes within
one year are linked to the reproductive cycle.

In summary: in the male pituitary, all five cell types
were present, but only three of these five showed tempo¬
ral modification. The glycoprotein type 1 cells are linked
in males and females to gonad development and are rare
during the dry season and most abundant during spermat¬
ogenesis/ vitellogenesis in July/ August and during the
mating season. The protein type 1 cells are always the
most abundant in males and females and show some, but
little variability. The glycoprotein type 3 cells, which are
assumed to be the thyrotropic cells, are always rare in both
sexes. The glycoprotein type 2 cells and the protein type

2 cells differ in their annual activity between the sexes.
Glycoprotein type 2 cells show no variability in females,
but in males they are absent during the dry season and
increase in number after emergence until they reach their
maximum in July/ August and they were linked to nup¬
tial pad development. The largest discrepancy is between
female and male protein type 2 cells. In females they are
abundant and active during the dry season, whereas in
males they are only present in July/ August.

Summary and discussion

Viviparity in Nimba toads

Within anurans, Nimba toads have a highly derived and
unique reproductive mode. They retain eggs and foetuses
within their oviducts and are pueriparous and matrotroph-
ic. As in other viviparous amphibian species, they have
internal fertilisation, a reduction in number of developing
eggs, and a prolonged developmental period (Wake 1992,
2015a). Several morphological and physiological adap¬
tations are present in females, foetuses and, to a lesser
extent, in males of N. occidentalis. The reproductive sys¬
tems are small. This seems to be a trend in viviparous am¬
phibians (Wake 2015a, 2015b). Oviducts are straight; the
lower end of the oviduct is enlarged. From toads of the
East African genera Altiphrynoides and Nectophrynoides
it is known that the oviducts can be divided into a thinner
anterior part (tube) and a sometimes dilated lower part,
uterus (Wake 1980, Xavier 1986). This is not surpris¬
ing for the pueriparous, lecitotrophic Nectophrynoides
tornieri, but more puzzling for the direct developing Al¬
tiphrynoides malcolmi (Wake 1980). In Nimba toads, the
uterine mucous layer first secrets mucoproteins, later gly¬
cogen. That the oviductal mucous layer is providing nu¬
trition is also known from Salamandra atra and several
caecilians (Vilter 1986, Gomes et al. 2012, Wake 2015b).
In S. atra a “zona trophica” in the (apical) pole of the ovi¬
duct is providing epithelial cells that detach from the con¬
nective tissue by apoptosis (Vilter 1986). Within studied
caecilians and Nimba toads the whole oviduct wall may
provide nutrition (Xavier 1971, Gomes et al. 2012). In S.
atra and caecilians, foetuses develop a “foetal dentition”
to scrape off the epithelial cells (Vilter 1986, Gomes et al.
2012, Wake 2015a, 2015b), whereas Nimba toad foetuses
develop labial papillae, and feed on liquids secreted by
the epithelial cells (“uterine milk”). That epithelial cells
secret mucoproteins is also known for Rhinoderma dar-
winii (Goicoechea et al. 1986). In this species males keep
their offspring within their vocal sacs from the moment
young show muscular movement until metamorphosis
(Garrido et al. 1975, Jorquera et al. 1982, Goicoechea et
al. 1986). The epithelial cells of the male vocal sac se¬
cret mucoproteins (Garrido et al. 1975), which are first
absorbed by the foetal skin, later presumably ingested
(Goicoechea et al. 1986). Recently was shown that the
pouch prooding Gastroteca excubitor transfers nutrients
from the mother to the devoping embryos (Warne and

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Catenazzi 2016). After parturition, the uterus of N. occi-
dentalis collapses, the existing mucous layer disconnects
from the connective tissue and is lysed within the uter¬
ine lumen, while a completely new mucous layer is built
from the connective tissue. An apoptotic phase exchang¬
ing the uterine mucous layer after parturition/ spawning is
absent in N. tornieri (Xavier 1986) and has not been de¬
scribed for S. atra (Vilter 1986) nor for any of the vivipa¬
rous caecilians (Gomes et al. 2012, Wake 2015a, 2015b).
Hence, at present Nimba toads are the only viviparous (in
the sense of oviductal egg retention) amphibian known
to provide liquid foetal nutrition and whose uterus has an
apoptotic phase.

In Nimba toads the ovaries are small and contain
small follicles, of which only very few mature within
each reproductive cycle. For example, in A. malcolmi
and N. tornieri ovaries are considerably larger and con¬
tain more follicles at very different developmental stages
(Wake 1980b, Xavier 1986). InDidynamipus sjostedti 18
mature and ten very small ova were observed (Grandi-
son 1981). In Nimbaphrynoides, A. malcolmi and Nec-
tophrynoides, follicles develop into corpora lutea, but
they are smaller, less persistent and less active in the
East African species than in Nimba toads (Wake 1980b,
Xavier 1986). No corpora lutea were reported for the pu-
eriparous, lecitotrophic Eleutherodactylus jasperi (Wake
1978), but are present in oviparous, as well as pueripa-
rous caecilians (Wake 1993, Gomes et al. 2012). Corpo¬
ra lutea are hypothesised to be important to determine
birthing stage (larviparous/ pueriparous) in subspecies of
S. salamandra and to maintain gestation (Wake 2015a,
2015b). In Nimba toads it was shown that the ovaries and
possibly the progesterone produced by the corpora lutea
are important in the first weeks of first-gestating females
to maintain the gestation. In older females, the observed
effect of progesterone is not to maintain the gestation, but
to decrease foetal developmental speed. In Nimba toads
and S. atra ovariectomy, and hence the removal of corpo¬
ra lutea in later stages of the gestation (after emergence
and after the first year, respectively), has no effect on
gestation duration and maintenance (Xavier 1971, Vil¬
ter 1986). At this stage the presence of foetuses in the
uteri seems to be more important in Nimba toads than the
presence of ovaries. Hence, at least in these two species,
corpora lutea are not important for the maintenance of
gestation and timing of parturition. Nevertheless, the hor¬
mones produced within the follicles (namely oestrogen
and progesterone, possibly testosterone) are important for
the preparative development of the oviduct and uterus.
In the marsupial frog Gastrotheca riobambae, oestrogen,
progesterone and the presence of foetuses are as well im¬
portant for pouch development and the maintenance of
the gestation at least for the first weeks (del Pino 1983).
In summary, the Nimba toad female reproductive system
is characterised by several adaptations to viviparity, in¬
cluding the endocrine function of the ovary. Characteris¬
tics of the ovary seem to be similar to other viviparous or
back-brooding anurans.

Nimba toad foetuses have no internal, nor external
gills, no spiracle, no coiled gut and neither labial teeth
nor horny beaks at any time during their development,
but they possess labial papillae, a gut similar in structure
to that of adults, well developed livers, and their devel¬
opment takes nine months. It was hypothesised that with¬
in viviparous amphibians metamorphosis is prolonged
(Wake 2015a). As Nimba toads lack many tadpole spe¬
cific characteristics, metamorphosis is restricted to the
development of the front limbs under the opercular skin
fold and the rupture of the latter in stage Ilia, the resorp¬
tion of the tail and the labial papillae during stage Illb.
Poorly developed mouthparts are generally found in spe¬
cies without a free swimming tadpole stage and within
direct developers gills and spiracle are only present for a
short time (Wake 1978). In N. tornieri, N. viviparus and
A. malcolmi neither beak, nor labial teeth, nor papillae
are present (Lamotte and Xavier 1972a, Wake 1980b).
The free-swimming tadpoles of Schismaderma have jaw-
sheaths, labial teeth, marginal papillae, a sinistral spiracle
midway along the body and a characteristic, half-moon
shaped fiap on the head (Channing et al. 2012). Necto-
phrynoides tornieri are known to have a sinistral spira¬
cle (Grandison 1978, Wake 1980b). The publications on
Nimba toad foetal development state that the develop¬
ment of the gut and livers is very early (e.g. Lamotte et
al. 1973). Hence, it seems that the most obvious morpho¬
logical differences of Nimba toads, the several rows of
labial papillae and early development of the gastrointes¬
tinal system in the foetus and the uterine secretion and
apoptosis in females, are linked to matrotrophy.

Based on morphology Grandison (1981) and Graybeal
and Cannatella (1995) postulated that the two viviparous
lineages, Nimbaphrynoides and Nectophrynoides, might
not be sister taxa. This was recently confirmed by Liedtke
et al. (2016), who showed that while the two viviparous
lineages are part of the same clade, they do not appear
to be very closely related, which suggests that viviparity
may have evolved independently in each of them. Here,
we have identified six characteristics linked to viviparity
specific of Nimba toads, which provide strong evidence
that viviparity evolved indeed independently in this spe¬
cies. These characteristics comprise three traits which are
common in other amphibians, but not usually found in
other viviparous species (small and yolk poor eggs, pro¬
longed mucoprotein secretion of the oviduct/ uterus epi¬
thelium after fertilisation, labial papillae of the foetuses),
two behavioural or ecologically important traits (“behav¬
ioural birthing” and the developmental break during the
dry season) and one characteristic which to our knowl¬
edge is not known of any other amphibian, but of mam¬
mals (complete apoptosis and rebuilding of the uterine
epithelium after parturition). First, small yolk-poor eggs
are common in oviparous amphibians with free swim¬
ming tadpoles, but are not known from other viviparous
anurans. Second, in amphibians the oviduct secrets mu-
coproteins to produce the egg layers prior to oviposition
and/ or fertilisation (Shivers and James 1970). In Nimba

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toads the upper part of the oviduct has the same function,
but the lower enlarged part (uterus) secrets mucoproteins
to nourish the foetuses. Hence the temporal shift of the
mucoprotein secretion within the uterus after fertilisation
and during gestation (Xavier 1986) is exceptional. Third,
foetal labial papillae are not uncommon in anurans and
several functions of the papillae were hypothesised (hor¬
monal secretion, enhancing the sucking capabilities of
lotic tadpoles etc., McDiarmid and Altig 1999). In direct
developers and lecitotrophic viviparous species foetuses
have no or only very reduced labial appendices present
for a limited duration (papillae, labial teeth etc.). Only
in matrotrophic caecilians and adelphophagous salaman¬
ders, foetuses have special foetal teeth (Wake 2015a).
Hence, the uniqueness is, that Nimba toad foetuses have
labial appendices even so they are viviparous and no
other labial feature than these papillae. The papillae are
certainly linked to feeding as they appear and disappear
with the mucoprotein secretion activity of the endometri¬
um (Lamotte and Xavier 1972b), but the exact function is
not known. Apart from the mucoprotein secretion of the
oviduct/ uterus, which is found in all amphibians (Shivers
and James 1970), these traits are more likely present in
oviparous species with free-swimming tadpoles than in
direct developing and ovoviviparous species. Didynami-
pus sjostedti and one Altiphrynoides species (A. malcol-
mi) have large yolk-rich eggs; A. osgoodi and Schisma-
derma have small eggs and are oviparous (Liedtke et al.
2016). This shows that within this clade egg sizes and
reproductive modes vary greatly.

The other three unique traits of the Nimba toad repro¬
duction can be regarded as adaptations to an unpredictable
environment and time constraints due to the seasonality.
First, the developmental break during the dry season co¬
incides with an inactive life with presumably a low ener¬
gy budget (Xavier and Ozon 1971, Lamotte 1972). The
duration of this inactivity is synchronised with the dura¬
tion of the dry season and its duration varies between 3-6
months depending on the onset of the monsoon (Lamotte
1959). Irrespective of the month with first rains (Febru¬
ary - April), Nimba toad females emerge with these first
rains, and the earlier they emerge, the larger are the juve¬
niles bom in June (Lamotte 1959, Xavier 1971). The larg¬
er the newborns, the higher is their survival probability.
Hence, the dry season duration is unpredictable and Nim¬
ba toads are fiexible in responding to this unpredictability.
Second, after parturition the endometrium is exchanged
and rebuilt. We speculate that this is due to the tempo¬
ral constraint, that a functional endometrium needs to be
present within three months after parturition to allow the
new foetuses to develop. It might be more effective and
faster to rebuild the endometrium, than to re-arrange the
old one within a collapsed uterus, additionally this may
decrease the mother offspring conflict. Whether this alone
is a sufficient explanation for the evolution of a unique
trait not described of other viviparous amphibians needs
further consideration. Additionally, determination wheth¬
er it does not occur in other viviparous amphibians is nec¬

essary. In Nimba toads the apoptosis phase lasts for 12
days only (Xavier and Ozon 1971) and probably might not
have been recorded in less well studied amphibian species.
Third, female Nimba toads are not able to expel juveniles
at the end of the gestation and hence, induce parturition
by behaviourally restricting the space for juveniles (Vil-
ter 1956a) and young are involved in the birthing process
(Xavier and Ozon 1971). Other than in mammals, no fe¬
male mechanism has evolved to end a gestation and no
morphological or physiological traits evolved to enhance
parturition. Changes in progesterone levels (e.g. produced
by the corpora lutea) are often discussed as triggers for
parturition. As in Nimba toads ovariectomy has no effect
on parturition and gestation duration, no indication exists
that corpora lutea produced progesterone is important for
parturition. Nevertheless, the glycogen secretion of the
uterine endometrium could set a time frame for parturi¬
tion. The inducing mechanism for the glycogen secretion
is unknown. The absence of known parturition inducing
mechanisms could be due to a lack of opportunity or ne¬
cessity. The Nimba toad uterus has a thin muscle layer
(Xavier 1971), and it should not be very challenging to
increase it, giving it the power to expel juveniles from the
uterus. On the other hand, the “birthing posture” allows
for parturition, and might be easier to be controlled and if
necessary interrupted by females. This may allow them to
give birth to single or few offspring and interrupt birthing,
if predators or other unpredictable threats are approaching.
The behavioural induced parturition does not allow to give
birth to dead juveniles, ending in the death by sepsis of the
mother (Xavier 1971). This may indicate that intra-uterine
death of juveniles is rare and the evolutionary advantag¬
es of behavioural parturition (temporal flexibility) might
be greater than the necessity to induce labour by muscle
power. The three traits mentioned here have a strong tem¬
poral link with the environmental unpredictability or with
the Nimba mountains seasonality. This may indicate that
the Nimba mountains environment and seasonality had a
strong influence on the evolution and/ or maintenance of
viviparity.

Ecology of Nimba toads

Within one year two important periods mainly determine
the reproductive cycle of a female: one, at the end of the
rainy season with ovulation, mating and the beginning
gestation, the second in June with the birth of juveniles.
These seasonal periods are important for males as well, as
during mating season spermatozoids are present, but dis¬
appear afterwards, in June at the time juveniles are born,
spermatogenesis is intensified. Nevertheless, one further
important period in the season is the emergence at the
beginning of the rainy season, which results as well in
changes within the reproductive system. Hence, within
one year three periods lead to important changes within
the Nimba toad reproductive system, one might be trig¬
gered by reproductive and/ or environmental clues (late
rainy season), one is characterised by environment - the
beginning of the rainy season (emergence), and one is

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Figure 12. Summary of the temporal development of the foetus and male and female reproductive system. The outer layer gives the
months as abbreviations and the seasons by colour (yellow: dry season, blue; rainy season). Toads mate between mid-September
and mid-October on average, are going underground mid-October and emerge in mid-March from their dormancy sites. Juveniles
are bom in mid-June (pictograms). Spermatogenesis shows the development within the male reproductive system. Foetal growth
gives the speed of development and growth. The uterus shows three phases: a proliferation phase in which the uterine epithelium de¬
velops, a secretion phase during the gestation and an apoptosis phase during which the uterine epithelium is completely exchanged
(old one removed and new one built). The ovary has two phases: the follicles phase, characterised by follicle growth and the luteal
phase characterised by the presence of corpora lutea. Within the female pituitary three cell types show variation within the annual
cycle, the glycoprotein type 1 cells and the protein type 1 and type 2 cells. Within the male pituitary as well three cell types show
variation (not shown), glycoprotein type 1 cells and glycoprotein type 2 cells in the same way as those of females, whereas protein
type 2 cells are only present in July/ August.

characterised by reproduction at least in females - the end
of gestation and intensification of spermatogenesis and
intensification of rains (June). In Figure 12 we summarise
the temporal changes of the male and female reproduc¬
tive and foetal development. Most developments can be
placed in either of two categories: i) linked to the active
above ground life of toads and hence, “environmentally

linked”, or ii) linked to the gestation period, “reproduc-
tively linked”. Obviously, these phases are non-exclusive,
as both overlap during the first months after emergence
and the last months of gestation.

“Environmentally linked” developments start with
emergence and end with the beginning of the dormant
life underground which coincides with mating (shown in

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127

blue in Figure 12). Within this category fall spermato¬
genesis, the follicular phase of the ovary, development
of the oviductal tube (not shown on Figure 12) and the
presence and activity of female and male glycoprotein
type 1 cells (gonadotrop cells). The glycoprotein type 1
cells were shown to produce luteinizing hormone (LH),
which is generally linked to gonad development and tes¬
tosterone and oestradiol synthesis. Human gonadotrop
cells produce as well follicle stimulating hormone (FSH),
which in turn stimulates the granulosa cells, which pro¬
duce progesterone in Nimba toads (Xavier 1971). Oestra¬
diol and progesterone together trigger oviduct develop¬
ment (Xavier 1971). Hence, all these processes lead to
ovulation, mating and finally successful establishment of
the gestation. In males, the glycoprotein type 1 and 2 cells
are linked to spermatogenesis and nuptial pad develop¬
ment; both are most developed in July and August, just
prior to the mating season. As all these processes start
with emergence, an environmental trigger for this devel¬
opment could be assumed.

“Reproductively linked” developments start with
mating and the establishment of the gestation and end with
the birth of juveniles (shown in yellow on Figure 12). This
category focusses mainly on females. The uterine secretion
phase, the ovarian luteal phase, the presence and activity
of protein type 2 cells and obviously foetal development
are within this category. The female protein type 2 cells
were classified as somatotropic cells. During the dry
season, foetal development is slow, the uterus is secreting
and stretching slowly and within the ovary corpora lutea
are producing progesterone. The developments within
this category are nevertheless as well infiuenced by the
environment, as most reproductive organs start slowly
decreasing their presence and activity after emergence,
including progesterone levels, with the exception of foetal
development, which increases in speed after emergence.

The uterine apoptosis and proliferation phases and the
presence and activity of protein type 1 cells (shown in red
in Figure 12) do not fit in either of these categories. The
uterine apoptosis phase starts slowly at the end of gestation
with the production of glycogen, which is linked to foe¬
tus development (stage III) but not with emergence. Dur¬
ing apoptosis the whole uterine mucous layer is replaced,
hence this is the phase with the most immediate impact on
the uterus. The uterine proliferation phase fits into the en¬
vironmentally linked definition in that it leads to ovulation
and mating at the end of the rainy season, but nevertheless,
contains the uterus foetuses until parturition, and prepara¬
tions for a new gestation can only start after the epithelial
cells are replaced during the apoptosis phase. Hence, the
secretion and the proliferation phase cannot overlap, as
they do in other organs. The presence and activity of the
protein type 1 cells were linked to prolactin secretion.

In Nimba toads the reproductive cycle is tightly linked
to the seasons. In most other viviparous amphibians an
environmental dependency is assumed, but detailed data
rarely exist (Wake 2015b). For oviparous caecilians it is
known that they may retain the fertilised eggs within the

oviduct until a suitable breeding site is found and timing
seems to be correlated with the onset of the rainy season
(Gomes et al. 2012, Wake 2015a, 2015b). In S. atra the
duration of gestation is longer at higher altitudes (Wun-
derer 1910) and is further prolonged by unsuitable envi¬
ronmental conditions (Vilter 1986). In squamate reptiles it
was hypothesised that the cold climate at high elevations
and high latitudes (Tinkle and Whitfield Gibbons 1977,
Watson et al. 2014) or the less variable female body tem¬
perature, compared to the surroundings (Shine 1995), fa¬
vours a viviparous reproduction. Nimba toads occur in an
environment with fiuctuating temperatures and at high el¬
evation (>1,200 asl). Likewise all Nectophrynoides occur
between 800 and 2700 m asl (Clarke 1988, Menegon et al.
2004, 2007, Channing et al. 2005, Channing and Howell
2006, Loader et al. 2009), with lower temperatures com¬
pared to the lowlands. Nevertheless, the possibly vivip¬
arous Central American C. laticeps occurs between 10
and 1,500 m asl, and E.jasperi and L. larvaepartus occur
at low elevations (Wake 1978, Iskandar et al. 2014), and
most viviparous caecilians are lowland species (Wake
1980b, 1993, Gomes et al. 2012). In caudates, high as
well as low elevation species with a viviparous reproduc¬
tion are known (Wake 2015b). For L. larvaepartus it was
hypothesised that viviparity might have evolved due to
competition avoidance (Iskandar et al. 2014). In pueri-
parous, adelphophagous subspecies of S. salamandra it
is hypothesised that scarcity of open water and harsh en¬
vironments promoted viviparity (Garcia-Paris et al. 2003,
Buckley et al. 2007, Velo-Anton et al. 2012, Escoriza and
Ben Hasssine 2014). Within the Nimba mountains high
altitude grasslands standing open water is only present
during some months during the rainy season at two loca¬
tions, temperature fiuctuations are large and competition
quite likely scarce as only two other anuran species occur
within the same area (Guibe and Lamotte 1958, L. Sand-
berger-Loua 2016a). It is likely that scarcity of open wa¬
ter and harsh environments promoted as well viviparity in
Nimba toads, or supported the survival of this unique re¬
productive mode in these special and isolated conditions.

Conservation

Most amphibian species with derived reproductive
modes are threatened (Wake 2015b). This is particularly
true for Nimba toads, which are listed under the lUCN
red list as critically endangered (lUCN SSC Amphibian
Specialist Group January 11, 2017/2016). Across a total
range of 4 km^ the total toad population was estimated to
comprise 16 million individuals in August in the 1950s
(Lamotte 1959) and 14 million in 1966 (Xavier 1971).
A calculation based on an assumed equal range size, our
annual monitoring data (2007-2016; 1,160 examined
plots of 5 X 5 m^, of those 178 in August, and 88 in
high density areas in August compare Sandberger-Loua
et al. 2016a), would result in 2.8 million toads in Au¬
gust (population size oscillates throughout season). This
translates into an 82% decrease in toad numbers since
1959, which quite likely underestimates the decrease

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Sandberger-Loua, L. et al.: Nimba toad reproductive biology

as our distribution estimate is smaller than 4 km^, and
we only included numbers from areas with high toad
abundances to calculate the average number of toads per
1 m^. The excellent studies, summarised in this review,
are based on > 3,000 females, several hundred foetuses
and an unknown number of males (F. Xavier included
about 3,000 females and several hundred foetuses and
newborns in her doctoral thesis alone, Xavier 1971).
During our ten years of field work we recorded less than
61% of the number of females sacrificed to understand
the toad’s reproduction (1,844 females in total recorded
within 29,000 m^ of high altitude grasslands searched
for 1,740 person hours). Between the 1950s and 2007
two mining exploration campaigns were carried out in
the area (Poilecot and Loua 2009), the Nimba moun¬
tains were first declared a World Heritage Site (1981/
1982) and 10 years later (1992) listed as World Heritage
Site in Danger (UNESCO 1992). Some anuran species
with derived and unique reproductive modes are already
considered extinct {Rheobatrachus situs, R. vitellinus,
E. jasperi. Wake 2015b) and hence, protection of the
reproductive diversity within anurans is important. Con¬
sidering their complex life cycle, in which reproductive
and seasonal cycles are tightly linked, understanding
and protecting the Nimba toad’s threatened environment
is of utmost importance.

Future work

The strong link between the Nimba toad’s reproductive
and life-cycle with the Nimba mountains seasonality and
other environmental factors indicates that these condi¬
tions might have favoured the evolution or at least the
maintenance of viviparity. Hence, ecological studies on
N. occidentalis and the other species within the Nimba
toad’s clade (Didynamipus, Altiphrynoides, Schismader-
ma, Nectophrynoides), several of which have derived
reproductive modes as well, may give insights into the
evolutionary drivers of viviparity in African bufonids.
Comparatively little is known about the other species
with and without derived reproductive modes within this
clade. For example, the reproductive mode of D. sjost-
edti is only assumed to be direct development (Grandi-
son 1981, Gonwouo et al. 2013) and little else is known
(Gonwouo et al. 2013). Of the two Ethiopian Altiphry-
onides species, some information exist on the reproduc¬
tive mode (Wake 1980b), but little on the ecology. ForX.
osgoodi it may be impossible to study the ecology as it
is feared to be extinct (Gower et al. 2013). Within Nec¬
tophrynoides, most ecological information exists for N.
asperginis (Channing et al. 2006), which is extinct in the
wild. This emphasises two reasons why ecological stud¬
ies are needed for all species in this clade: first, they may
give insights into the evolution of viviparity and second,
they may help to protect these threatened species from
extinction.

Conclusion

Viviparity is rare in anurans and the only known matro-
trophic anuran is the Nimba toad. In Nimba toads three
observations support matrotrophy: first, newborn Nimba
toads are 15 times larger and > 200 times heavier than the
egg. Second, amino acids injected into the mother were re¬
corded first within the digestive system and liver and later
in other areas of the foetuses. Third, foetal size at birth is
linked to environmental conditions during the last third of
the gestation period, during which females are active and
most of the foetal growth occurs. We have identified six
characteristics linked to viviparity specific of Nimba toads,
which provide strong evidence that viviparity evolved in¬
dependently in this species. These characteristics comprise
three traits which are common in other amphibians, but not
usually found in other viviparous species (small and yolk
poor eggs, mucoprotein secretion by oviduct/ uterus epi¬
thelium, labial papillae of the foetuses), two behavioural or
ecologically important traits (“behavioural birthing” and the
developmental break during the dry season) and one char¬
acteristic which to our knowledge is not known from any
other amphibian, but from mammals (complete apoptosis
and rebuilding of the uterine epithelium after parturition).
Apart from the mucoprotein secretion of the oviduct/ uterus
which is found in all amphibians before fertilisation - but in
Nimba toads additionally after fertilisation - these traits are
more likely present in oviparous species with free-swim¬
ming tadpoles than in direct developing and lecitotrophic
viviparous species. The other three unique traits can be re¬
garded as adaptations to an unpredictable environment and
time constraints due to the environments seasonality. Most
reproductive developments can be placed in either of two
categories: i) linked to the gestation period, “reproductively
linked”, or ii) linked to the active above ground life of toads
and hence, “environmentally linked”. Hence, it is likely that
the harsh unpredictable environment and scarcity of open
water promoted viviparity in Nimba toads, or supported
the survival of this unique reproductive mode in these spe¬
cial and isolated conditions. Considering their complex life
cycle, in which reproductive and seasonal cycles are tight¬
ly linked, understanding and protecting the Nimba toad’s
threatened environment is of utmost importance.

Acknowledgements

For support to receive rare and difficult to access pub¬
lications we thank Martina RiBberger and Hans-Ulrich
Raake from the MfN library. Johannes Fenner organised
access to the doctoral thesis of Frangoise Xavier. Nema
Soua Eoua provided one photograph in Figure 2. Joseph
Doumbia took the photograph of the male nuptial pads
(Figure 11). Thomas Schmid-Dankward assisted in pre¬
paring Figure 12. This support is very much appreciated!
We thank Marvalee H. Wake and an anonymous reviewer
for their valuable comments.

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Zoosyst. Evol. 93 (1) 2017, 105-133

129

References

Altig R, McDiarmid RW (1999) Body plan, development and
morphology. In: McDiarmid RW, Altig R (Eds) Tadpoles. The
biology of anuran larvae. The University of Chicago Press, Chicaco
24-51.

Angel F (1943) Description d’un nouvel amphibien anoure, ovo-vivipare,
de la Haute-Guinee Franpaise (Materiaux de la mission Famotte, an
Mont-Nimba). Bulletin du Museum National d’histoire Naturelle Par¬
is, 2e Serie 15(4): 167-169.

Angel F, Famotte M (1944a) Sur la viviparite et la parthenogenese
probable d’un Amphibien anoure nouveau d’Afrique occidentale
(Nectophrynoides occidentalis Angel). Comptes Rendus Hebdoma-
daires des Seances de I’Academie des Sciences 219: 370-372.
Angel F, Famotte M (1944b) Un crapaud vivipare d’Afrique occidentale
Nectophrynoides occidentalis Angel. Annales des Sciences Naturelles,
Zoologie 6: 63-89.

Angel F, Famotte M (1947) Note sur la biologic d’un crapaud vivipare
Nectophrynoides occidentalis Ang. Comptes Rendus Hebdomadaires
des Seances de 1’Academic des Sciences 224: 413^15.

Angel F, Famotte M (1948) Nouvelles observations mr Nectophrynoi¬
des occidentalis Angel. Remarques sur le genre Nectophrynoides.
Annales des Sciences Naturelles, Zoologie 10: 115-147.

Berge JW (1974) Geology, geochemistry, and origin of the Nimba
itabirite and associated rocks, Nimba County, Fiberia. Economic
Geology 69: 80-92. https://doi.Org/10.2113/gsecongeo.69.l.80
Beukema W, de Pous P, Donaire D, Escoriza D, Bogaerts S, Toxopeus
AG, de Bie CAJM, Roca J, Carranza S (2010) Biogeography and
contemporary climatic differentiation among Moroccan Salaman-
dra algira. Biological Journal of the Finnean Society 101: 626-641.
https://doi.Org/10.llll/j.1095-8312.2010.01506.x
Billa M, Feybesse J-F, Bronner G, Ferouge C, Milesi J-P, Traore S,
Diaby S (1999) Fes formations a quartzites rubanes ferrugineux
des Monts Nimba et du Simandou: des unites empilees tecto-
niquement, sur un “soubassemenf ’ plutonique Archeen (craton de
Kenema-Man), lors de I’orogene Ebumeen. Comptes Rendus de
I’Academie des Sciences Paris, Sciences de Fa Terre et des Planetes
329: 287-294. https://doi.org/10.1016/sl251-8050(99)80248-1
Blackburn DG (1999) Viviparity and oviparity: Evolution and repro¬
ductive strategies. Encyclopedia of Reproduction 4: 994-1003.
Blackburn DG (2015) Evolution of vertebrate viviparity and specializa¬
tions for fetal nutrition: A quantitative and qualitative analysis. Journal
of Morphology 276: 961-990. https://doi.org/10.1002/jmor.20272
Buckley D (2012) Evolution of viviparity in salamanders (Amphibia,
Caudata). Encyclopedia of Fife Sciences 2012: 1-13. https://doi.
org/10.1002/9780470015902.a0022851
Buckley D, Alcobendas M, Garcia-Paris M, Wake MH (2007) Heter¬
ochrony, cannibalism, and the evolution of viviparity in Salamandra
salamandra. Evolution and Development 9(1): 105-115. https://doi.
org/10.1111/j.l525-142X.2006.00141.x
Castanet J, Pinto S, Foth M-M, Famotte M (2000) Age individuel,
longevity et dynamique de croissance osseuse chez un amphibien
vivipare, Nectophrynoides occidentalis (Anuoure, Bufonide). An¬
nales des Sciences Naturelles, Zoologie 21(1): 11-17. https://doi.
org/10.1016/S0003-4339(00)00103-9
Channing A, Finlow-Bates KS, Haarklau SE, Hawkes PG (2006)
The biology and recent history of the critically endangered Ki-
hansi Spray Toad Nectophrynoides asperginis in Tanzania. Jour¬

nal of East African Natural History 95(2): 117-138. https://doi.
org/10.2982/0012-8317(2006)95[ 117:TBARHO]2.0.CO;2
Channing A, Howell KM (2006) Amphibians of East Africa. Cornell
University Press, New York, 432 pp.

Channing A, Menegon M, Salvidio S, Akker S (2005) A new forest toad
from the Ukaguru Mountains, Tanzania (Bufonidae: Nectophrynoi¬
des). African Journal of Herpetology 54(2): 149-157. https://doi.org
/lO. 1080/21564574.2005.9635528

Channing A, Rbdel M-0, Channing J (2012) Tadpoles of Africa, the
biology and identification of all known tadpoles in sub-Saharan Af¬
rica. Chimaira, Frankfurt a M, 402 pp.

Clarke BT (1988) The amphibian fauna of the East African rainforests,
including the description of a new species of toad, genus Necto¬
phrynoides Noble 1926 (Anura Bufonidae). Tropical Zoology 1:
169-177. https://doi.Org/10.1080/03946975.1988.10539412
del Pino EM (1983) Progesterone induces incubatory changes in the
brooding pouch of the frog Gastrotheca riobambae (Fowler). Jour¬
nal of Experimental Zoology 227: 159-163. https://doi.org/10.1002/
jez. 1402270121

Dubois A (1986) Miscellanea taxinomica batrachologica (I). Alytes
5(1-2): 7-95.

Duellman WE, Trueb F (1986) Biology of Amphibians. The Johns Hop¬
kins University Press, Baltimore.

Escoriza D, Ben Hasssine J (2014) Microclimatic variation in multiple
Salamandra algira populations along an altitudinal gradient: Phe¬
nology and reproductive strategies. Acta Herpetologica 9(1): 33-41.
Fournier A (1987) Quelques donnees quantitatives sur les formations
herbacees d’altitude des monts Nimba (Guest africain). Bulletin du
Museum National d’Histoire Naturelle Paris 4 Ser, Section B, Adan-
soni9(2): 153-166.

Frost DR (2016) Amphibian Species of the World: an Online Refer¬
ence (Version 6.0). http://research.amnh.org/herpetology/amphibia/
index.html [accessed 11 January 2017]

Garcia-Paris M, Alcobendas M, Buckley D, Wake DB (2003) Disper¬
sal of viviparity across contact zones in Iberian populations of fire
salamanders {Salamandra) inferred from discordance of genetic
and morphological traits. Evolution 57(1): 129-143. https://doi.
org/10.111 l/j.0014-3820.2003.tb00221 .X
Garrido O, Pugin E, Jorquera B (1975) Correspondance ultrastructura-
le entre la bourse gutturale du Rhinoderma darwini et le tegument
des larves. Bolletino Di Zoologia 42(2-3): 133-144. https://doi.
org/10.1080/11250007509431421

Gavaud J (1976a) Fa gemetogenese du male Aq Nectophrynoides occidenta¬
lis Angel (Amphibien Anoure vivipare). I. - Etude quantitative au cours
du cycle annuel chez I’adulte. Annales de Biologic Animale, Biochimie,
Biophysique 16(1): 1-12. https://doi.Org/10.1051/md:19760101
Gavaud J (1976b) Fe cycle sexuel male de Nectophrynoides occidentalis
Angel. Bulletin de la Societe Zoologique de France 101: 1011.
Gavaud J (1977) Fa gametogenese du male de Nectophrynoides occiden¬
talis Angel (Amphibien Anoure vivipare) II. - Etude experimentale du
role des facteurs extemes sur la spermatogenese de I’adulte, au cours
du cycle annual. Annales de Biologic Animale, Biochimie, Biophy-
sique 17(5A): 679-694. https://doi.Org/10.1051/md:19770605
Goicoechea O, Garrido O, Jorquera B (1986) Evidence for a trophic pa¬
ternal-larval relationship in the frog Rhinoderma darwinii. Journal
of Herpetology 20(2): 168-178. https://doi.org/10.2307/1563941
Gomes AD, Moreira RG, Navas CA, Antoniazzi MM, Jared C (2012)
Review of the reproductive biology of caecilians (Amphibia, Gym-

zse.pensoft.net

130

Sandberger-Loua, L. et al.: Nimba toad reproductive biology

nophiona). South American Journal of Herpetology 7(3); 191-202.
https://doi.Org/10.2994/057.007.0301

Gonwouo NL, Ndeh AD, Tapondjou WP, Noonan BP (2013) Amphib¬
ia, Bufonidae, Didynamipus sjostedti Anderson, 1903: New records
and a review of geographic distribution. Check List 9(4): 780-782.
https://doi.Org/10.15560/9.4.780

Gosner KL (1960) A simplified table for staging anuran embryos and
larvae with notes on identification. Herpetologica 1960(3): 183-
190. http://www.jstor.org/stable/3890061.

Gower DJ, Aberra RK, Schwaller S, Largen MJ, Collen B, Spawls S,
Menegon M, Zimkus BM, de Sa R, Mengistu AA, Gebresenbet F,
Moore RD, Saber SA, Loader SP (2013) Long-term data for en¬
demic frog genera reveal potential conservation crisis in the Bale
Mountains, Ethiopia. Oryx 47(1): 59-69. https://doi.org/10.1017/
S0030605311001426

Grandison AGC (1978) The occurence of Nectophrynoides (Anura Bu-
fonide) in Ethiopia. A new concept of the genus with a description of
a new species. Monitore Zoologico Italiano 6 : 119-172.

Grandison AGC (1981) Morphology and phylogenetic position of the
West African Didynamipus sjoestedti Anderson, 1903 (Anura Bu¬
fonidae). Monitore Zoologico Italiano. Supplemento 15(1); 187-215.

Graybeal A, Cannatella DC (1995) A new taxon of Bufonidae from Peru,
with descriptions of two new species and a review of the phylogenetic
status of supraspecific bufonid taxa. Herpetologica 51(2): 105-131.

Greven H (2003) Earviparity and pueriparity. In: Sever DM (Ed.) Re¬
productive biology and phylogeny of Urodela. Science Publishers,
Inc., Enfield, 447-475.

Guibe J, Eamotte M (1958) Morphologic et reproduction par develop-
pement direct d’un anoure du Mont Nimba, Arthroleptis crusculum
Angel. Bulletin du Museum National d’histoire Naturelle Paris, 2e
Serie30(2): 125-133.

Haddad CEB, Prado CPA (2005) Reproductive modes in frogs and their
unexpected diversity in the Atlantic Forest of Brazil. BioScience
55(3): 207-217. https://doi.org/10.1641/0006-3568(2005)055[020
7:RMIFAT]2.0.CO;2

Hanken J (2003) Direct development. In: Hall BK, Olson WM (Eds)
Keywords and Concepts in Evolutionary Developmental Biology.
Harvard University Press, 97-102.

Hillers A, Eoua NS, Rddel M-0 (2008) Assessment of the distribution
and conservation status of the viviparous toad Nimbaphrynoides oc-
cidentalis on Monts Nimba, Guinea. Endangered Species Research
5: 13-19. https://doi.org/10.3354/esr00099

Iskandar DT, Evans BJ, McGuire JA (2014) A novel reproductive mode
in frogs: A new species of fanged frog with internal fertilization and
birth oftadpoles. PEoS ONE 9(2): ell5884. https://doi.org/10.1371/
Journal.pone.0115884

lUCN (2014) World Heritage Outlook. http://www.worldheritageout-
look.iucn.org/search-sites/-/wdpaid/fr/2574?p_p_auth=4mS7fmc5
[Accessed January 11, 2017]

lUCN SSC Amphibian Specialist Group (2016) Nimbaphrynoides occi-
dentalis. https;//doi.org/10.2305/IUCN.UK.2014-3.RETS.T16793075-
A16793120.en [accessed January 11,2017]

Jorquera B, Garrido O, Pugin E (1982) Comparative studies of the
digestive tract development between Rhinoderma darwinii and
R. rufum. Journal of Herpetology 16(3); 204-2014. https://doi.
org/10.2307/1563714

Kupfer A, Kramer A, Himstedt W, Greven H (2006) Copulation and
egg retention in an oviparous caecilian (Amphibia: Gymnophiona).

Zoologischer Anzeiger 244; 223-228. https://doi. 0 rg/lO.lOl 6 /j.
jcz.2005.12.001

Kupfer A, Wilkinson M, Gower DJ, Muller H, Jehle R (2008) Care and
parentage in a skin-feeding caecilian amphibian. Journal of Experi¬
mental Zoology 309A: 460-467. https://doi.org/10.1002/jez.475

Kusrini MD, Rowley JJE, Khairunnisa ER, Shea GM (2015) The Re¬
productive Biology and Earvae of the First Tadpole-Bearing Frog ,
Limnonectes larvaepartus. PEoS ONE 10(1): el 16154. https://doi.
org/10.1371/journal.pone.Ol 16154

Eamotte M (1947a) Recherches ecologiques sur le cycle saisonni-
er d’une savane guineenne. Bulletin de la Societe Zoologique de
France 72: 88-90.

Eamotte M (1947b) Une reserve naturelle integrale dans le massif du
Nimba (Guinee Fran^aise). Ea Terre et Ea Vie 1: 15-34.

Eamotte M (1958) Ee cycle ecologique de la savane d’altitude du
mont Nimba (Guinee). Annales de la Societe Royale Zoologique
de Belgique 89; 119-150.

Eamotte M (1959) Observations ecologiques sur les populations na-
turelles dQ Nectophrynoides occidentalis (Fam. Bufonides). Bulletin
Biologique 4: 355-413.

Eamotte M (1972) Bilan energetique de la croissance du male de Necto¬
phrynoides occidentalis Angel, amphibien anoure. Comptes Rendus
de I’Academie des Sciences, Paris, Serie D 274: 2074-2076.

Eamotte M (1982) Ee crapaud vivipare des Monts Nimba (Guinee et
Cote d’Ivoire) Nectophrynoides occidentalis Angel. Ee Club Fran-
cais de la Medaille 76: 70-73.

Eamotte M (1983) The undermining of Mount Nimba. Ambio 12(3-4):
174-179.

Eamotte M, Aguesse P, Roy R (1962) Donnees quantitatives sur une
biocoenose Ouest-africaine: la prairie montagnarde du Nimba
(Guinee). Ea Terre et Ea Vie 4: 351-370.

Eamotte M, Glacon R, Xavier F (1973) Recherches sur le developpe-
ment embryonnaire de Nectophrynoides occidentalis Angel amphi¬
bien anoure vivipare. II Ee developpement des gonades. Annales
d’Embryologie et de Morphogenese 6(3): 271-296.

Eamotte M, Prum P (1957) Analyse quantitative du developpement de
la thyroide au cours des metamorphoses de I’embryon de Necto¬
phrynoides occidentalis Angel. Comptes Rendus des Seances de la
Societe de Biologic etde ses Filiales 151: 1187-1191.

Eamotte M, Rey P (1954) Existence de corpora lutea chez un Batracien
anoure vivipare, Nectophrynoides occidentalis Angel; leur evolution
morphologique. Comptes Rendus de FAcademic des Sciences 238:
393-395.

Eamotte M, Rey P (1957) Evolution de Fovaire chez les femelles vi-
erges de Nectophrynoides occidentalis Angel. Comptes Rendus des
Seances de la Societe de Biologic et de ses Filiales 151: 1191-1194.

Eamotte M, Rey P, Vilter V (1956) Evolution ovarienne au cours de la
gravidite chez un Batracien vivipare {Nectophrynoides occidenta¬
lis). Comptes Rendus des Seances de la Societe de Biologic et de ses
Filiales 150(2): 393-396.

Eamotte M, Rey P, Vogeli M (1964) Recherches sur Fovaire de Nec¬
tophrynoides occidentalis, Batracien anoure vivipare. Archives
d’Anatomic Microscopique et de Morphologic Experimentale
53(3): 179-224.

Eamotte M, Rougerie G, Roy R, Schnell R (2003) Ee Nimba et ses
principaux biotopes. In: Eamotte M, Roy R (Eds) Ee peuplement an¬
imals des Monts Nimba. Memoirs du Museum National d’Histoire
Naturelle 190, 29-50.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 105-133

131

Lamotte M, Roy R (1961a) L’endemisme dans la faune orophile du
mont Nimba (Guinee). Comptes Rendus Hebdomadaires des Seanc¬
es de I’Academie des Sciences 252: 4209-4210.

Lamotte M, Roy R (1961b) La zonation de la faune au mont Nim¬
ba (Guinee). Comptes Rendus Hebdomadaires des Seances de
I’Academie des Sciences 252: 4040-4042.

Lamotte M, Roy R (1962) Les traits principaux du peuplement animal de la
prairie montagnarde du Mont Nimba (Guinee). Recherches Africaines -
Etudes Guineenes 1: 11-30.

Lamotte M, Sanchez-Lamotte C (1999) Adaptation aux particularites
climatiques du cycle biologique d’un anoure tropical, Nectophrynoi-
des occidentalis Angel, 1943 (Bufonidae). Alytes 16(3-4): 111-122.

Lamotte M, Tuchmann-Dubplessis H (1948) Structure et transforma¬
tions gravidiques du tractus genital femelle chez un anoure vivipare
(Nectophrynoides occidentalis Angel). Comptes Rendus Hebdoma¬
daires des Seances de I’Academie des Sciences 226: 597-599.

Lamotte M, Xavier F (1972a) Les amphibiens anoures a developpement
direct d’Afrique. Observations sur la biologic de Nectophrynoi¬
des tornieri (Roux). Bulletin de la Societe Zoologique de Fran-
ceoologique de France 97: 413-428.

Famotte M, Xavier F (1972b) Recherches sur le developpement embry-
onnaire de Nectophrynoides occidentalis Angel, amphibien anoure
vivipare I - Fes principaux traits morphologiques et biometriques du
developpement. Annales d’Embryologie et de Morphogenese 5(4):
315-340.

Famotte M, Xavier F (1976a) Fe cycle ecologique de Nectophrynoides oc¬
cidentalis Angel. Bulletin de la Societe Zoologique de France 101:1009.

Famotte M, Xavier F (1976b) Fes modalites de la reproduction de Nec¬
tophrynoides occidentalis Angel. Bulletin de la Societe Zoologique
de France 101: 1009-1010.

Fe Quang Trong Y (1967) Structure et developpement de la peau et des
glandes cutanees de Nectophrynoides occidentalis Angel. Archives
de Zoologie Experimentale et Generale 108(4): 589-610.

Feclerc J-C, Richard-Molard J, Famotte M, Rougerie G, Porteres R
(1955) Fa reserve naturelle integrale du Mont Nimba. Fasciscule III.
Fa chaine du Nimba. Essai geographique. Memo ires de F’institut
Francais d’Afrique Noire 43(3): 1-271.

Fiedtke HC, Muller H, Hafner J, Nagel P, Foader SP (2014)
Interspecific patterns for egg and clutch sizes of African Bufonidae
(Amphibia: Anura). Zoologischer Anzeiger 253: 309-315. https://
doi.org/10.1016/j.jcz.2014.02.003

Fiedtke HC, Muller H, Rbdel M-0, Menegon M, Gonwouo FN, Bare) MF,
Gvozdik V, Schmitz A, Charming A, Nagel P, Foader SP (2016) No
Ecological Opportunity on a Continental Scale? Diversification and
Fife-History Evolution of African True Toads (Bufonidae: Anura). Evo¬
lution 70: 1717-1733.

Foader SP, Poynton JC, Davenport TRB, Rbdel M-0 (2009) Re-description
of the type series of Nectophrynoides viviparus (Bufonidae), with a tax¬
onomic reassessment. Zootaxa 2304: 41-50.

McDiarmid RW, Altig R (1999) Tadpoles. The biology of anuran larvae.
The University of Chicago Press, Chicaco.

Menegon M, Salvidio S, Foader SP (2004) Five new species of Nec¬
tophrynoides Noble 1926 (Amphibia Anura Bufonidae) from the
Eastern Arc Mountains, Tanzania. Tropical Zoology 17(1): 97-121.
https://doi.Org/10.1080/03946975.2004.10531201

Menegon M, Salvidio S, Ngalason W, Foader SP (2007) A new dwarf
forest toad (Amphibia: Bufonidae: Nectophrynoides) from the Ukaguru
Mountains, Tanzania. Zootaxa 1541: 31^0.

Ozon R, Xavier F (1968) Biosynthese in vitro des steroides par I’ovaire
de r anoure Yimpare Nectophrynoides occidentalis au cours du cycle
sexuel. Comptes Rendus de F Academic des Sciences, Serie D 266:
1173-1175.

Poilecot P, Foua NS (2009) Fes feux dans les savanes des monts Nimba,
Guinee. Bois et Forets des Tropiques 301(3): 51-66.

Pyron RA, Burbrink FT (2014) Early origin of viviparity and multi¬
ple reversions to oviparity in squamate reptiles. Ecology Fetters 17:
13-21. https://doi.org/10.llll/ele.12168
San Mauro D, Gower DJ, Muller H, Foader SP, Zardoya R, Nussbaum RA,
Wilkinson M (2014) Fife-history evolution and mitogenomic phytoge¬
ny of caecilian amphibians. Molecular Phylogenetics and Evolution 73:
177-189. https://d 0 i. 0 rg/l0.1016/j.ympev.2014.01.009
Sandberger-Foua F, Doumbia J, Rbdel M-0 (2016a) Conserving the
unique to save the diverse - Identifying key environmental deter¬
minants for the persistence of the viviparous Nimba toad in a West
African World Heritage Site. Biological Conservation 198: 15-21.
https://doi.Org/10.1016/j.biocon.2016.03.033
Sandberger-Foua F, Feldhaar H, Jehle R, Rbdel M-0 (2016b) Multiple
paternity in a viviparous toad with internal fertilisation. Science of
Nature 103: 51. https://doi.org/10.1007/s00114-016-1377-9
Sandberger F, Hillers A, Doumbia J, Foua NS, Brede C, Rbdel M-0
(2010) Rediscovery of the Fiberian Nimba toad, Nimbaphrynoides
liberiensis (Xavier, 1978) (Amphibia: Anura: Bufonidae), and reas¬
sessment of its taxonomic status. Zootaxa 2355: 56-68.

Sarasin P, Sarasin F (1887) Zur Entwicklungsgeschichte und Anatomic der
Ceylonesichen Blindwuhle Ichtyophis glutinosus. In Ergebnisse Natur-
wissenschaftlicher Forschungen auf Ceylon in den Jahre 1884-1886. C
W Kreidel’s Verlag, Wiesbaden, 1-72.

Scheltinga DM, Jamieson BGM (2003) Spermatogenesis and the mature
spermatozoon: form, function and phylogenetic implications. In: Ja¬
mieson BGM (Ed.) Reproductive biology and phylogeny of Anura.
Science Publishers Inc., Enfield, 119-251.

Schnell R (1952) Vegetation et fiore de la region montagneuse du Nimba.

Memoires de I’lnstitut Francais d’Afrique Noire 22: 1-604.

Schnell R (1987) Fes formations herbeuses montagnardes des monts
Nimba (Guest africain). Bulletin du Museum National d’Histoire
Naturelle Paris 4 Ser, Section B 9(2): 137-151.

Shine R (1995) A new hypothesis for the evolution of viviparity in
reptiles. The American Naturalist 145(5): 809-823. https://doi.
org/10.1086/285769

Shivers CA, James JM (1970) Morphology and histochemistry of the ovi¬
duct and egg-jelly layers in the frog, Rana pipiens. The Anatomical
Record 166: 541-556. https://doi.org/10.1002/ar.1091660311
Tinkle DW, Whitfield Gibbons J (1977) The distribution and evolution
of viviparity in reptiles. Miscellaneous Publications Museum of Zo¬
ology University of Michigan 154: 1-55.

UNESCO (1992) Convention concerning the protection of the world
cultural and natural heritage. World Heritage Commitee - Sixteenth
session. WHC-92/CONF.002/12.

UNESCO (2015) Mount Nimba strict nature reserve - documents. Ac¬
cessed July 22, 2015, from whc.unesco.org/en/list/155/documents/.
University of California, Berkeley (2017) AmphibiaWeb. http://www.

amphibiaweb.org/ [accessed January 11, 2017]
van Dyke JU, Brandley MC, Thompson MB (2014) The evolution of
viviparity: Molecular and genomic data from squamate reptiles ad¬
vance understanding of live birth in amniotes. Reproduction 147:
15-26. https://doi.org/10.1530/REP-13-0309

zse.pensoft.net

132

Sandberger-Loua, L. et al.: Nimba toad reproductive biology

van Oort PGWJ (1961) The gonadotrophin-producing and other cell
types in the distal lobe of the pituitary of the common frog Rana
temporaria. General and Comparative Endocrinology 1; 364-374.
https ://doi. org/10.1016/0016-6480(61 )90054-5

Velo-Anton G, Zamudio KR, Cordero-Rivera A (2012) Genetic drift and
rapid evolution of viviparity in insular fire salamanders (Salaman-
dra salamandra). Heredity 108; 410-418. https://doi.org/10.1038/
hdy.2011.91

Vilter V (1955) Ecologie de “I’hibernation saisonniere” du Necto-
phrynoides occidentalism crapaud vivipare des Monts du Nimba en
Guinee franpaise. Comptes Rendus des Seances de la Societe de Bi¬
ologic et de ses Filiales 149: 24-26.

Vilter V (1956a) Mecanismes de I’accouchement chez le Nectophrynoides
occidentalism crapaud totalement vivipare des Monts Nimba (Haute
Guinee). Comptes Rendus des Seances de la Societe de Biologic et de
ses Filiales 150(11): 1876-1878.

Vilter V (1956b) Role de la photosensibilite dans I’accouchement
ecologique chez les Nectophrynoides occidentalism crapaud vivipare
de la Haute Guinee. Comptes Rendus des Seances de la Societe de
Biologic et de ses Filiales 150(11): 1917-1919.

Vilter V (1957) Evolution saisonniere de foviducte chez les Necto¬
phrynoides occidentalism crapaud totalement vivipare de la Haute-
Guinee. Comptes Rendus des Seances de la Societe de Biologic et
de ses Filiales 151(5): 926-930.

Vilter V (1986) Fa reprodcution de la Salamandre Noire {Salamandra
atra). In: Grasse P-P, Delsol M (Eds) Traite de Zoologie - anatomic,
sysematique, biologic - Batraciens. Masson, Paris, 487-495.

Vilter V, Famotte M (1956) Evolution post-gravidique de I’uterus chez
Nectophrynoides occidentalis Ang., crapaud totalement vivipare de
la Haute-Guinee. Comptes Rendue des Sceances de la Societe de
Biologic 150(12): 2109-2113.

Vilter V, Fugand A (1959a) Recherches sur le determinisme interne et
exteme du corps jaune gestatif chez le crapaud vivipare du Mont
Nimba, le Nectophrynoides occidentalis Ang. de la Haut Guinee.
Comptes Rendus des Seances de la Societe de Biologic et de ses
Filiales 153: 294-297.

Vilter V, Fugand A (1959b) Trophisme intra-uterin et croissance embry-
onnaire chez le Nectophrynoides occidentalis Ang., crapaud totale¬
ment vivipare du Mont Nimba (Haute-Guinee). Comptes Rendus des
Seances de la Societe de Biologic et de ses Filiales 153: 29-32.

Vilter V, Schroder U, Fugand A (1959) Evolution volumetrique de I’hy-
pophyse au cours de la gestation chez le Nectophrynoides occidentalism
crapaud totalement vivipare de la Haute Guinee. Comptes Rendus des
Seances de la Societe de Biologic et de ses Filiales 153: 60-64.

Wake MH (1978) The reproductive biology of Eleutherodactylus jas-
peri (Amphibia, Anura, Feptodactylidae), with comments on the
evolution of live-bearing systems. Journal of Herpetology 12(2):
121-133. https://doi.org/10.2307/1563398

Wake MH (1980a) Reproduction, growth, and population structure of
the Central American Caecilian Dermophis mexicanus. Herpetolog-
ica 36(3): 244-256.

Wake MH (1980b) The reproductive biology of Nectorphynoides mal-
colmi (Amphibia. Bufonidae), with comments on the evolution of
reproductive modes in the genus Nectophrynoides. Copeia 1980(2):
193-209. https://doi.org/10.2307/1443998

Wake MH (1992) Evolutionary scenarios, homology and convergence of
structural specializations for vertebrate viviparity. American Zoolo¬
gist 32: 256-263. https://doi.Org/10.1093/icb/32.2.256

Wake MH (1993) Evolution of oviductal gestation in amphibians.
Journal of Experimental Zoology 266: 394-413. https://doi.
org/10.1002/jez. 1402660507

Wake MH (2015a) Fetal adaptations for viviparity in amphibians. Journal
of Morphology 276(8): 941-960. https://doi.org/10.1002/jmor.20271

Wake MH (2015b) How do homoplasies arise? Origin and maintenance
of reproductive modes in amphibians. In: Dial KP, Shubin N, Brain-
erd EF (Eds) Great Transformations in Vertebrate Evolution. The
University of Chicago Press, Chicaco, 375-394.

Wame RW, Catenaazi A (2016) Pouch brooding marsupial frogs trans¬
fer nutrients to developing embryos. Biology Fetters 12: 20160673.
https://doi.org/10.1098/rsbl.2016.0673

Watson CM, Makowsky R, Bagley JC (2014) Reproductive mode evo¬
lution in lizards revisited: Updated analyses examining geographic,
climatic and phylogenetic effects support the cold-climate hypoth¬
esis. Journal of Evolutionary Biology 27: 2767-2780. https://doi.
org/10.1111/jeb.l2536

Wells KD (2010) The Ecology and Behavior of Amphibians. The Uni¬
versity of Chicago Press, Chicaco, 1400 pp.

Wunderer H (1910) Beitrage zur Biologic und Entwicklungsgeschichte
des Alpensalamanders {Salamandra atra Faur). Zoologische Jahr-
biicher - Abeilung fiir Systeamik, Geographic und Biologic der
Tiere 28: 23-80.

Xavier F (1969) Corps jaunes de post-ovulation actifs chez les femelles
non fecondees de Nectophrynoides occidentalis (Amphibien anoure
vivipare). General and Comparative Endocrinology 13: 542.

Xavier F (1970a) Action moderatrice de la progesterone sur la croissance
des embryons chez Nectophrynoides occidentalis Angel. Comptes
Rendus de I’Academie de Sciences, Paris, Serie D 270: 2115-2117.

Xavier F (1970b) Analyse du role des corpora lutea dans le maintien
de la gestation chez Nectophrynoides occidentalis Angel. Comptes
Rendus de 1’Academic de Sciences, Serie D 270: 2018-2020.

Xavier F (1971) Recherches sur I’endocrinologie sexuelle de la femelle
de Nectophrynoides occidentalis Angel (amphibien anoure vivipare).
Faculte des sciences universite de Paris, these de doctorat d’etat es-
SciencesNaturelles, n° C.N.R.S., A.O. 6385.

Xavier F (1973) Fe cycle des voies genitales femelles dQ Nectophrynoi¬
des occidentalis Angel, amphibien anoure vivipare. Zeitschrift fiir
Zellforschung 140: 509-534. https://doi.org/10.1007/BF00306677

Xavier F (1974) Fa pseudogestation cYiqz Nectophrynoides occidentalis
Angel. General and Comparative Endocrinology 22; 98-115. https;//
doi.org/10.1016/0016-6480(74)90092-6

Xavier F (1976) Adaptations anatomiques et physiologiques a la vivi-
parite c\\qz Nectophrynoides occidentalis AngeX. Bulletin de la Societe
Zoologique de France 101: 1010-1011.

Xavier F (1977) An exceptional reproductive strategy in anura: Nec¬
tophrynoides occidentalis Angel (Bufonidae), an example of ad¬
aptation to terrestrial life by viviparity. In: Hecht MK, Goody PC,
Hecht BM (Eds) Major patterns in vertebrate evolution. NATO Ad¬
vanced Study Institude, Series A, Fife Sciences, 545-552. https://
doi.org/10.1007/978-l-4684-8851-7_19

Xavier F (1978) Une espece nouvelle de Nectophrynoides (Anoure,
Bufonide) des monts Nimba, N. liberiensis n. sp. 1. description
de I’espece. Bulletin de la Societe Zoologique de France 103(4):
431-441.

Xavier F (1986) Fa reproduction des Nectophrynoides. In: Grasse P-P,
Delsol M (Eds) Traite de Zoologie - anatomic, sysematique, biolo¬
gic - Batraciens. Masson, Paris, 497-513.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 105-133

133

Xavier F (2009) La belle histoire du petit crapaud vivipare du Mont Nimba.

Bulletin de la Societe Zoologique de France 134(1-2): 13-21.

Xavier F, Ozon R (1971) Recherches sur Factivite endocrine de I’ovaire
de Nectophrynoides occidentalis Angel (Amphibien Anoure vivipare)
II. Synthese in vitro des steroids. General and Comparative Endocri¬
nology 16: 30-40. https://doi.org/10.1016/0016-6480(71)90204-8
Xavier F, Zuber-Vogeli M, Le Quang Trong Y (1970) Recherches sur
Factivite endocrine de Fovaire de Nectophrynoides occidenta¬
lis Angel (Amphibien Anoure vivipare) - I. Etude histochimique.
General and Comparative Endocrinology 15: 425-431. https://doi.
org/10.1016/0016-6480(70)90116-4
Zuber-Vogeli M (1966) Ees variations cytologiques de Fhypophyse dis¬
tale du male de Nectophrynoides occidentalis au cours du cycle an¬
nuel. General and Comparative Endocrinology 7: 492-499. https://
doi.org/10.1016/0016-6480(66)90071 -2
Zuber-Vogeli M (1968) Ees variations cytologiques de Fhypophy¬
se distale des femelles de Nectophrynoides occidentalis. Gen¬
eral and Comparative Endocrinology 11: 495-514. https://doi.
org/10.1016/0016-6480(68)90065-8
Zuber-Vogeli M (1978) Effet de la bromocriptine sur la cellule “pro-
lactine like” de Nectophrynoides occidentalis (Amphibien Anoure
vivipare): etudes aux microscopes optique et electronique. Compt-
es Rendus de FAcademie de Sciences, Serie D 286: 1379-1381.
Zuber-Vogeli M, Bihoues-Eouis MA (1971) E’hypophyse de Necto¬
phrynoides occidentalis au cours du developpement embryonnaire.
General and Comparative Endocrinology 16: 200-216. https://doi.
org/10.1016/0016-6480(71 )90032-3

Zuber-Vogeli M, Doerr-Schott J (1976) E’ultrastructure de quatre
categories cellulaires de la pars distalis de Nectophrynoides occi¬
dentalis Angel (amphibien, anoure vivipare). General and Compar¬
ative Endocrinology 28: 299-312. https://doi.org/10.1016/0016-
6480(76)90182-9

Zuber-Vogeli M, Doerr-Schott J (1984) Eocalisation par immunofluo¬
rescence de dilFerents principes hormonaux de Fhypophyse de Nec¬
tophrynoides occidentalis Angel, au cours du developpement em¬
bryonnaire. General and Comparative Endocrinology 53: 264-271.
https ://doi. org/10.1016/0016-6480(84)90252-1

Zuber-Vogeli M, Doerr-Schott J, Dubois MP (1975) Eocalisation par
immunofluorescence des secretions apparentees aux hormones
gonadotrope, corticotrope, melanotrope et somatotrope dans Fhy¬
pophyse de Nectophrynoides occidentalis. Comptes Rendus de
FAcademie des Sciences, Serie D 280: 1595-1598.

Zuber-Vogeli M, Herlant M (1964) Etude cytologique des formes cel¬
lulaires presentes dans Fantehypophyse de Nectophrynoides occi¬
dentalis (Angel.). Comptes Rendus Hebdomadaires des Seances de
FAcademie des Sciences 258: 3367-3369.

Zuber-Vogel i M, Xavier F (1965) Ea spermatogenese de Nectophrynoides
occidentalis au cours du cycle annuel. Bulletin de la Societe
Zoologique de France 90: 261-267.

Zuber-Vogeli M, Xavier F (1973) Ees modifications cytologiques
de Fhypophyse distale des femelles de Nectophrynoides occi¬
dentalis Angel apres ovariectomie. General and Comparative
Endocrinology 20: 199-213. https://doi.org/10.1016/0016-

6480(73)90147-0

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 135-141 | DOI 10.3897/zse.93.10995

4>yEnsPFr.

museum fur naturkunde

Taxonomical study on a sample of land and freshwater snails from
caves in central Brazil, with description of a new species

Rodrigo B. Salvador^Daniel C. Cavallari^, Luiz R. L. Simone^

1 Staatliches Museum fiir Naturkunde Stuttgart. Rosenstein 1, 70191, Stuttgart, Baden-Wiirttemberg, Germany

2 Mathematisch-NaturwissenschaftlicheFakultdt, EberhardKarls UniversitdtTubingen. Sigwartstrafie 10, 72076, Tubingen, Baden-Wiirttemberg,
Germany

3 Museu de Zoologia da Universidade de Sdo Paulo. Avenida Nazare 481, 04263-000, Sao Paulo, SP, Brazil
http://zoobank. org/lED4E25 7-4CD3-4A1D-82B6-40615D5 72C91

Corresponding author: Rodrigo B. Salvador (salvador.rodrigo.b@gmail.com)

Received 31 October 2016
Accepted 1 February 2017
Published 15 February 2017

Academic editor:

Matthias Glaubrecht

Key Words

Bahia

caves

Gastropoda

Goias

Gastrocopta sharae sp. n.

stygofauna

troglofauna

Abstract

A sample of land and freshwater snails, mainly pulmonates, was recently collected in
caves in Goias and Bahia states, Brazil. Twenty-one species were found in the material.
The following species are reported for the first time for Goias state: Cecilioides consobri-
na (Ferussaciidae), Dysopeas muibum and Stenogyra octogyra (Subulinidae), Entodina
jekylli and Prohappia besckei (Scolodontidae; also reported for the first time for Bahia
state), Pupisoma dioscoricola (Valloniidae). A new species from Goias is described here¬
in: Gastrocopta sharae sp. n. (Gastrocoptidae). The new records and species addressed
here constitute important findings, helping to fill distributional gaps and improving the
knowledge of the local molluscan fauna, an essential step for future conservation efforts.

Introduction

The Brazilian continental molluscan fauna is still poor¬
ly known and is deemed to have so many undescribed
species as to triple the presently known number (Simone
1999, 2006). Since cave-dwelling invertebrates, in gener¬
al, have received scarce attention from researchers in Bra¬
zil (Trajano and Bichuette 2010), it should be no surprise
that cave-dwelling land and freshwater snails are even less
known (a few exceptions are: Bichuette and Trajano 1999,
2003, Simone 2013, Salvador et al. 2016). This lack of
study is alarming, especially from a conservationist point
of view, since caves usually have very fragile ecosystems
with a high degree of endemic species (Trajano 2000,
Gallao and Bichuette 2012, Silva and Ferreira 2015).

Some recent expeditions (April/2012-January/2013)
by Dr. M. E. Bichuette (Universidade Federal de Sao

Carlos; Sao Carlos, Brazil) and her team to cave systems
in Goias and Bahia states, central Brazil, recovered many
land and freshwater snails. This whole material was de¬
posited in the malacological collection of the Museu de
Zoologia da Universidade de Sao Paulo (MZSP, Sao Pau¬
lo, Brazil) and is studied here. The sample studied herein
includes the description of a new species and occurrence
of another twenty species, some of which are new records
for Bahia and/or Goias states.

Material and methods

All the material studied here was collected by M. E. Bi¬
chuette and her team and deposited in the MZSP. All the
specimens were collected in caves (see Table 1 for all the
localities) and comprise both empty shells and living an-

Copyright Rodrigo B. Salvadoretal. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

136

Salvador, R.B. et al.: Taxonomical study on a sample of land and freshwater snails...

Table 1. List of all localities, i.e., the caves (or “grutas” in Portuguese), where the present material was collected, alongside their
city/municipality, state, coordinates (see also Fig. 1), date of collection, the biome of the surrounding area, the microhabitat where
the snails were collected and if there is a water body inside each cave.

Locality

City

State

Coordinates

Collection date

Biome

Substrate

Water

body

Gruta Cantinho

Igatu/Andaraf

12°51’49.9”S 41°19’26.9”W

Ol/Apr/2013

Oampos

Rupestres

wet sand

yes

Gruta do Catao

Sao Desiderio

12°22’07.0”S 44°52’03.2”W

03/NOV/2012

Oerrado/

Oaatinga

wet sand, clay

yes

Gruta do Renatao

Sao Desiderio

12°26’35.6”S 44°56’26.7”W

03/NOV/2012

Oerrado/

Oaatinga

clay

Gruta das Dores

Mambai

14°24’38.0”S 46°11’35.5”W

30/Apr/2013

Oerrado

clay

yes

Gruta Fundo de Quintal

Mambai

14°29’16.0”S 46°07’08.4”W

29/Oct/2012

Oerrado

clay

yes

Gruta Judite

Mambai

14°24’26.5”S 46°11’43.7”W

Ol/May/2013

Oerrado

clay

yes

Gruta da Tarimba

Mambai

14°24’43.0”S 46°10’29.6”W

28/Oct/2012,

29/Apr/2013

Oerrado

clay

yes

Gruta Pasto de Vacas 1

Mambai

14°26’19.4”S 46°10’40.9”W

02/May/2013

Oerrado

clay

yes

Gruta Revolucionarios

Posse

14“14’03.0”S 46°20’41.8”W

30/Apr/2013,

03/May/2013

Oerrado

clay

yes

'50°W

l39“W

11°S

18°S

400 km

Figure 1. Map showing the Brazilian states of Bahia and Goias, with the cities where the caves are located (see also Table 1);
1, Igatu/Andarai; 2, Sao Desiderio; 3, Mambai; 4, Posse. Abbreviations; GO, Goias state; BA, Bahia state; DF, Distrito Federal.

imals. Brief descriptions of each locality can be found
in Table 1, alongside their precise coordinates (see also
Fig. 1). Localities from Goias all fit into the Cerrado Bi¬
ome, while those in Bahia are either Campos Rupestres
(montane subtropical savannah) or a transition between
the Cerrado and the Caatinga.

Identification was conducted based on the work of
Simone (2006), the original descriptions, and additional
material housed in the collection of the MZSP. Unfortu¬
nately, some species could not be identified beyond genus
level, either due to poor preservation of the specimens or
to very young age. The complete list of species, as well as
a relation of all the studied material, can be found in Table
2. Species that deserve further notice, such as those with
new records, are figured and discussed in the Systematics
session below. Measurements were made with a digital
caliper or with the aid of the Zeiss Axiovision SE64 Rel
4.8 imaging software. The following abbreviations are
used herein: shell dimensions: H = shell length, D = shell

greatest width, h = aperture height, d = aperture width; in¬
stitutions: NHMUK = Natural History Museum (London,
UK); NMSW = National Museum Wales (Cardiff, UK).

Systeraatics

Pulmonata

Stylommatophora

Superfamily Pupilloidea

Family Gastrocoptidae

Genus Gastrocopta Wollaston, 1878

Gastrocopta sharae sp. n.

http://zoobank.org/923AD6BA-B7BD-4ABl-A67E-35E769EE8290
Figs 2-6

Type material. Holotype: MZSP 122725 (Figs 2-A).
Paratype: MZSP 122726, from type locality (Figs 5-6).

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Zoosyst. Evol. 93 (1) 2017, 135-141

137

Table 2. List of all species found on the present material, with information on locality data, whether it is a new occurrence (species
with new records are analyzed more thoroughly in the text) and record number of the MZSP collection. Abbreviations; BA, Bahia
state; GO, Goias state; Can, Gruta Cantinho; Cat, Gruta do Catao; Dor, Gruta das Dores; FdQ, Gruta Fundo de Quintal; Jud, Gruta
Judite; PdV, Pasto de Vacas I; Ren, Gruta do Renatao; Rev, Gruta Revolucionarios; Tar, Gruta da Tarimba; hoi, holotype; par,
paratype; sh, shell; spc, specimen.

Species

Family

New

record?

Cave(s)

Collection Nr. (MZSP)

Neritimorpha

Helicina angulata Sov^erby, 1873

Helicinidae

Ren (BA)

MZSP 122761 (1 spc)

Caenogastropoda

Pomacea sp.

Ampullariidae

Gat (BA)

MZSP 122776(1 sh)

Idiopyrgus souleyetlanus Pilsbry, 1911

Pomatiopsidae

Cat (BA)

MZSP 122772 (1 sh), 122773 (5 sh),
122774(6 sh), 122775(3 sh)

Pulmonata - Hygrophila

Biomphalaria sp.

Planorbidae

Cat (BA), PdV (GO)

MZSP 122768 (17 sh), 122769 (1 sh),
122770 (5 sh), 122771 (3 sh), 122777 (1 sh)

Aplexa marmorata (Guilding, 1828)

Physidae

Jud (GO)

MZSP 122730(1 spc)

Pulmonata - Stylommatophora

Solaropsis sp.

Camaenidae

Tar (GO)

MZSP 122727 (2 spc)

Radiodiscus sp.

Charopidae

Tar, Rev (GO)

MZSP 122816 (1 sh), 122817 (9 sh),
131089 (2 sh), 131090(1 sh)

Ziichogyra sp.

Charopidae

Dor (GO)

MZSP 122734(1 sh)

Ceciiioides consobrina (d’Orb\gny, 1841)

Ferussaciidae

yes

Tar, Rev (GO)

MZSP 131578 (1 sh), 131579 (1 sh),
122756 (1 sh), 122759 (1 sh)

Gastrocopta sharae sp. nov.

Gastrocoptidae

yes

Rev (GO)

MZSP 122725 (hoi), MZSP 122726 (par)

Cyciodontina sexdentata (Spix, 1827)

Orthalicidae

Oat (BA)

MZSP 122763(1 spc)

Ringinceiia iuetzeiburgiYJeber, 1925

Orthalicidae

Ren(BA)

MZSP 122762 (2 sh)

Entodina jekyiii Baker, 1913

Scolodontidae

yes

Tar, Rev (GO)

MZSP 122735 (10 sh + 4 spc), 122757 (1
sh), 131091 (5 sh + 1 spc), 131092 (2 sh),
131093 (3 sh)

Happia sp.

Scolodontidae

Oat (BA)

MZSP 122767 (1 spc)

Happia giaberrima

Scolodontidae

Rev (GO),

Oant(BA)

MZSP 122822 (1 spc), 122824(1 sh),
122825 (2 sh), 122826 (4 spc), 1228227
(1 spc)

Rrohappia besckei (Dunker, 1847)

Scolodontidae

yes

Oan, Ren (BA);
Tar, Rev (GO)

MZSP 122736 (4 sh + 1 spc), 122758 (Ish),
122760 (4 sh + 1 spc), 122764 (1 sh),
131094 (4 sh), 131095 (7 sh), 131096 (3
sh), 131097 (3 sh), 131098 (1 spc), 131099
(1 sh)

Aiiopeas micra (d’Orbigny, 1835)

Subulinidae

FdQ (GO)

MZSP 122729 (1 sh) MZSP 122732 (1 sh)

Dysopeas muibum
(Marcus & Marcus, 1968)

Subulinidae

yes

Tar (GO)

MZSP 131100(1 sh)

Leptinaria sp.

Subulinidae

Oat, Ren (BA)

MZSP 122765 (1 sh), 122766 (1 sh)

Leptinaria concentrica (Reeve, 1849)

Subulinidae

Rev (GO)

MZSP 122828(1 spc)

Stenogyra octogyra (Pfeiffer, 1856)

Subulinidae

yes

Dor, Jud, Tar (GO)

MZSP 122728(1 sh), 122731 (1 spc),
122733 (2 sh)

Pupisoma dioscoricoia
(C.B. Adams, 1845)

Valloniidae

yes

Tar, Rev (GO)

MZSP 122737 (1 sh), 122738 (1 sh),
122739 (1 sh), 131101 (1 sh)

Type locality. BRAZIL, Goias, Mambal, Gruta Revo¬
lucionarios (col. M.E. Bichuette, J.E. Gallao, D.M. Shi-
monsky, P.P. Rizzato, R. Borghezan; 29/iv/2013).

Distribution. Known only from the type locality (Fig. 1).

Etymology. The name refers to Shar, a fictional goddess
of darkness, caverns, and secrets, from the Faerunian
pantheon of the Forgotten Realms campaign setting of
the Dungeons and Dragons role-playing game.

Diagnosis. Shell pupilloid-conical. Four apertural barri¬
ers: two lamellae and two teeth). Anguloparietal lamella
shaped like narrow gutter, bent towards palatal region.

Description. Shell minute (H < 2 mm), pupilloid-coni¬
cal; greatest width of shell on body whorl (D/H = 0.6);
body whorl ca. 1/2H; spire angle 48°. Whorl profile
greatly convex; suture well-marked. Protoconch (ca.
114 whorl) round, smooth; transition to teleoconch
clearly marked by change to teleoconch sculpture. Te¬
leoconch sculptured by strongly prosocline faint axial
riblets. Aperture rounded to lightly quadrangular (d/h =
0.8; h/H = 0.4); peristome refiexed; parietal callus dis¬
tinctive. Apertural barriers totaling four (Fig. 3): upper
palatal tooth, lower palatal tooth, columellar lamella,
anguloparietal lamella. Anguloparietal lamella shaped
like narrow gutter, bent towards palatal region. After
the anguloparietal lamella, the strongest barriers are the

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138

Salvador, R.B. et al.: Taxonomical study on a sample of land and freshwater snails...

Figures 2-20. Gastrocopta sharae sp. n., holotype (MZSP 122725, H = 1.9 mm, D = 1.1 mm). 2. Apertural view; 3. Apertural view,
SEM image; 4. Close-up of the aperture, showing dentition; scale bar = 200 pm. 5-6. Gastrocopta sharae sp. n., paratype (MZSP
122726, H = 1.9 mm, D = 1.1 mm). 5. Apertural view; 6. Apertural view, SEM image. 7-11. Other Gastrocopta spp. from Brazil,
shown in apertural view. All images in scale to one another and to G. sharae (Figs 2, 3, 5, 6). 7. G. barbadensis, from Trindade
Island, SEM image (MZSP 104736, H = 1.9 mm); 8. G. iheringi, probable syntype, from Bolacha, Rio Grande do Sul state (MZSP
7519, H = 2.5 mm); 9. G. oblonga, from Brazil, precise provenance unknown (NMSW unnumbered, H = 2 mm); 10. Gastrocopta
servilis, from Fortaleza, Ceara state (MZSP 7520, H = 2 mm); 11. Gastrocopta solitaria, possible holotype, from Fernando de No-
ronha Archipelago (NHMUK unnumbered, H = 2 mm). 12. Pupisoma dioscoricola, apertural view (MZSP 131101,H=l.6 mm, D
= 1.6 mm). 13-14. Cecilioides consobrina (MZSP 131579, H = 1.9 mm, D = 0.6 mm). 13. Apertural view; 14. Apertural view, SEM
image. 15-16. Dysopeas muibum (MZSP 131100, H = 5.4 mm, D = 2.3 mm). 15. Apertural view; 16. Apertural view, SEM image.
17. Stenogyra octogyra, apertural view (MZSP 122731, H = 14.3 mm, D = 3.7 mm). 18-19. Entodina jekylli (MZSP 131092, H
= 1.6 mm, D = 3.1 mm). 18. Apertural view, SEM image; 19. Apertural view. 20. Prohappia besckei, apertural view, SEM image
(MZSP 131096, H= 1.0 mm, D= 1.8 mm).

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139

lower palatal tooth and columellar lamella. Umbilicus
narrow, deep.

Dimensions (in mm). Holotype: 4% whorls; H = 1.9; D
= 1.1; h = 0.7; d = 0.6. Paratype: 4% whorls; H = 1.9; D
= l.l;h = 0.7;d = 0.6.

Discussion. The minute pupilloid shell and the pattern of
apertural barriers, especially the presence of an angulo-
parietal lamella (formed by the fusion of the angular and
parietal lamellae), place the present specimens in Gas-
trocopta. They are sufficiently different and easily diag-
nosable from all known Gastrocopta species in Brazil,
which warrants the description of a new species: Gas¬
trocopta sharae sp. n. Although each of the diagnostic
features of G. sharae can be found separately in conge¬
ners (e.g., Pilsbry 1916-1918), their occurrence together
is unique for this species.

Gastrocopta sharae can be easily distinguished
by its strongly conical shell (Figs 2, 3, 5, 6). Nearly
all Brazilian species have more pupiform/cylindrical
shells: G. barbadensis (Pfeiffer, 1853) (Fig. 7), known
from the Caribbean Islands, Venezuela, Fernando de
Noronha Archipelago and Trindade Island (Cunha et al.
2015); G. iheringi (Suter, 1900) (Fig. 8), known only
from Rio Grande do Sul state (Simone 2006); G. oblon-
ga (Pfeiffer, 1852) (Fig. 9), known from Suriname to
Argentina (Simone 2006); and G. servilis (Gould, 1843)
(Fig. 10), known from Ceara and Rio de Janeiro states
(Simone 2006). Gastrocopta solitaria (Smith, 1890)
(Fig. 11), from Fernando de Noronha Archipelago, is
somewhat conical, but not nearly as much as G. sharae.

Likewise, G. sharae is easily diagnosable by its nar¬
row gutter-like anguloparietal lamella (Fig. 4), slightly
bent towards the palatal region of the aperture. All the
Brazilian species present a bifid weak anguloparietal
lamella, with the single exception of G. iheringi (Fig. 8).
The latter also has a gutter-like lamella, but it is much
broader and straight (i.e., not bent towards the palatal
region). Moreover, G. iheringi is much taller than G
sharae, reaching a shell length of 2.5 mm; this might not
seem a large difference at first sight, but differences of
this magnitude are usually considered to be interspecific
in the family.

Family Valloniidae

Genus Pupisoma Stoliczka, 1873

Pupisoma dioscoricola (C.B. Adams, 1845)

Fig. 12

Synonymy see Hausdorf (2007). Complement;

Pupisoma dioscoricola. Salgado and Coelho 2003: 153.

Pupisoma discoricola [sic]; Simone 2006: 308 (fig. 9).

Pupisoma (Ptychopatula) dioscoricola. Hausdorf2007: 1483 (Figs 1-2, 6 ).

Type locality. USA, Texas, Brownsville. Paralectotypes are
from Mexico, San Luis Potosi, Valles Falls and Choy Cave.

Previously known distribution. From Florida, USA, to
southern Brazil and northern Argentina, including the Ca¬
ribbean islands (Hausdorf 2007).

New occurrence. Goias. Mambai: Gruta da Tarimba.
Posse: Gruta Revolucionarios.

Remarks. Despite the species being known throughout
the Americas, the present record fills a gap in the species
distribution (see the revision of Hausdorf 2007: fig. 6).

Superfamily Achatinoidea

Family Ferussaciidae

Genus Cecilioides Ferussac, 1814

Cecilioides consobrina (d’Orbigny, 1837)

Figs 13-14

Achatina consobrina d’Orbigny 1837: 89 (pi. 11 bis. Figs 10-12); d’Or¬
bigny 1841: 170.

Caecilioides (Caecilianopsis) consobrina. Hylton Scott 1948: 254;
Morretes 1949: 131.

Cecilioides (Karolus) consobrina. Figueiras 1963: 87; Quintana 1983: 80.
Cecilioides consobrina. Parodiz 1957: 131; Salgado and Coelho 2003:
154; Simone 2006: 182 (fig. 666 ); Aguirre et al. 2007: 10 (fig. 4.5);
Miquel et al. 2007: 114; Miquel and Aguirre 2011: 109 (fig. 8 ).

Type locality. Near Matanzas, Cuba.

Previously known distribution. From the Caribbean Is¬
lands to central-northern Argentina (Miquel and Aguirre
2011) and Uruguay (Figueiras 1963).

New occurrence. Goias. Mambai: Gruta da Tarimba.
Posse: Gruta Revolucionarios.

Remarks. The present record is the first occurrence for Goias
and fills a gap in the species distribution in Central Brazil.

Family Subulinidae
Genus Dysopeas Baker, 1927

Dysopeas muibum Marcus & Marcus, 1968

Figs 15-16

Pseudopeas {Dysopeas) muibum Marcus and Marcus 1968: 199 (Figs
11-19)

Dysopeas muibum: Simone 2006: 185 (fig. 673); Simone and Salvador
2016: 29, fig. 97, table 1.

Type locality. Sao Paulo, Sao Paulo state, Brazil.

Previously known distribution. Known only from its
type locality (Marcus and Marcus 1968; Simone 2006) and
Nanuque, Minas Gerais state (Simone and Salvador 2016).

New occurrence. Goias. Mambai: Gruta da Tarimba.

Remarks. The present record greatly expands this species
distribution: ca. 720 km to the northwest.

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Salvador, R.B. et al.: Taxonomical study on a sample of land and freshwater snails...

Genus Stenogyra Shuttleworth, 1854
Stenogyra octogyra (Pfeiffer, 1856)

Fig. 17

Bulimus octogyriis Pfeiffer 1856: 45.

Opeas octogyrum: Pilsbry 1906: 206 (pi. 29, Figs 75-79); Baker 1913:

644; Salgado and Coelho 2003: 155.

Stenogyra octogyra. Simone 2006: 188 (fig. 695).

Type locality. Caracas, Venezuela.

Previously known distribution. Venezuela and Bra¬
zil (Para, Ceara, Rio Grande do Norte and Mato Grosso
states) (Simone 2006).

New occurrence. Goias. Mambai: Gruta das Dores, Gra¬
ta Judite, Gruta da Tarimba.

Remarks. The present record fills a gap in the species’
previously known distribution in Brazil.

Superfamily Rhytidoidea
Family Scolodontidae
Genus Entodina Ancey, 1887

Entodina jekylli Baker, 1913

Figs 18-19

Entodina jekylli Baker 1913: 630 (pi. 22, Figs 11-13); Morretes 1949:
137; Baker 1963: 239; Salgado and Coelho 2003: 169; Simone
2006: 224 (fig. 851).

Type locality. Camp 39 of Stanford expedition, Ma-
deira-Mamore railway ca. 284 km above Porto Velho,
Rondonia, Brazil.

Previously known distribution. Known only from type
locality.

New occurrence. Goias. Mambai: Gruta da Tarimba.
Posse: Gruta Revolucionarios.

Remarks. There are two further possible records of
this species from Peru and Bolivia (Ituarte et al. 2008;
Ramirez et al. 2012), but the specimen figure by Ituar¬
te et al. (2008: 83, text fig.), referred to as Systrophia
{Entodina) aff. jekylli, is quite different from the type
specimen figured by Simone (2006: 244, fig. 851B). The
present specimens do compare well with the types; how¬
ever, they lack the palatal tooth typical of the species
(Baker 1913). This could be simple morphological vari¬
ation (intraspecific differences in dentition are common
in pulmonate snails), represent juvenile or sub-adult
specimens or, less likely, even be an indicative that the
present material represents a new species. The pres¬
ent record greatly extends the species distribution, ca.
2000 km southeast.

Genus Prohappia Thiele, 1927
Prohappia besckei (Bunker in Pfeiffer, 1847)

Fig. 20

Helix Besckei Dunker in Pfeiffer 1847: 81; Hidalgo 1870: 37.

Happia {Prohappia) besckei. Morretes 1949: 139.

Happia besckei Salgado and Coelho 2006: 169.

Prohappia besckei. Simone 2006: 228 (fig. 873); Simone and Salvador
2016: 29 (Figs 98-100, table 1).

Type locality. Brazil (restricted to Rio de Janeiro by Hi¬
dalgo 1870).

Previously known distribution. Brazil: Minas Gerais,
Rio de Janeiro and Santa Catarina states (Simone 2006;
Simone and Salvador 2016). Paraguay (Morretes 1949;
Simone 2006).

New occurrence. Bahia. Igatu/Andarai: Gruta Cantinho.
Sao Desiderio: Gruta do Renatao. Goias. Mambai: Gruta
da Tarimba. Posse: Gruta Revolucionarios.

Remarks. The shell morphology of the present specimens
compare very well to P. besckei, the size of the specimens
from Goias, however, is much smaller (D ~ 2 mm), slightly
larger than half the normal size. This could represent a vari¬
ation of the species in a cave environment, but the sample
is too small to be of any significance. The present record
extends the species distribution ca. 600 km to the north.

Discussion

Many records reported here are the first for either Goias
or Bahia states (Table 2). These findings are especially
important as they not only extend the geographical distri¬
bution of some species but also fill “distribution gaps” of
some others; for instance, one species, Entodina jekylli,
was previously known only from its type locality. The
present records are among the few concerning molluscan
cave fauna. Most caves in Brazil have no legal protection
and are threatened by mining activities, but still harbor
new discoveries (e.g., Simone 2013). Better known geo¬
graphical distributions, as well as the presence of endem¬
ic taxa, can improve arguments for conservation. It is our
hope that the present work is a step towards proper legal
protection of such fragile ecosystems.

Acknowledgements

We are deeply grateful to Maria E. Bichuette (UFSCar)
and her team for providing the material studied here and
the information on the collection localities, and to Karin
Wolf-Schwenninger (SMNS) for the SEM images. This
work was partly supported by a doctorate grant from Con-
selho Nacional de Desenvolvimento Cientifico e Tecno-
logico (CNPq; Brazil) to R.B.S., proc. #245575/2012-0.

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Zoosyst. Evol. 93 (1) 2017, 135-141

141

References

Aguirre ML, Miquel SE, Gonzalez CA, Krohling D, Zucol AF, Brea M,
Eastoe C (2007) Malacofauna continental holocena y paleoambien-
tes em Villa Valle Maria (Diamante, Entre Rios, Argentina). Geobios
44(1): 1-17. https://doi.Org/10.1016/j.geobios.2010.06.003

Baker F (1913) The land and freshwater mollusks of Stanford Expedi¬
tion to Brazil. Proceedings of the Academy of Natural Sciences of
Philadelphia, 65(1914): 618-672.

Baker FIB (1963) Type land shells in the Academy of Natural Scienc¬
es of Philadelphia II. Eand Pulmonata, exclusive of North America,
North of Mexico. Proceedings of the Academy of Natural Sciences
of Philadelphia 115(8): 191-259.

Bichuette ME, Trajano E (1999) Eight reaction, spontaneous and feed¬
ing behaviour in epigean and cave gastropods, Potamolithus spp.,
from Upper Ribeira karst area, southeastern Brazil (Mollusca: Gas¬
tropoda: Hydrobiidae). Memoires de Biospeologie 26: 1-6.

Bichuette ME, Trajano E (2003) Population study of epigean and sub¬
terranean Potamolithus snails from southeast Brazil (Mollusca:
Gastropoda: Hydrobiidae). Hydrobiologia505: 107-117. https://doi.
org/10.1023/B:HYDR.0000007299.26220.b8

Cunha CM, Salvador RB, Simone ERE (2015) The terrestrial microgas¬
tropods of Trindade Island, Brazil (Gastropoda: Pulmonata). Spixiana
38(1): 139-143.

Figueiras A (1963) Enumeracion sistematica de los moluscos terrestres del
Uruguay. Comunicaciones de la Sociedad Malacologica del Umguay
1(4): 79-96.

Gallao JE, Bichuette ME (2012) A lista de fauna ameapada de extinpao
e os entraves para a inclusao de especies - o exemplo dos peixes tro-
globios brasileiros. Natureza and Conservapao 10(1): 83-87. https://
doi.org/10.4322/natcon.2012.014

Hausdorf B (2007) Revision of the American Pupisoma species (Gastrop¬
oda: Pupilloidea). Journal of Natural History 41(21-24): 1481-1511.
https://doi.Org/10.1080/00222930701401069

Hidalgo JG (1870) Catalogue des coquilles terrestres recueiliis par les
naluralistes de la commission scientifique espagnole sur divers points
de 1‘Amerique meridionale. Journal de Conchyliologie 18: 27-70.

Hylton Scott MI (1948) Moluscos del noroeste argentine. Acta Zoologica
Eilloana 6: 241-274.

Ituarte C, Cuezzo G, Ramirez R (2008) Inventario preliminar de los
moluscos terrestres y de agua dulce del area de la Reserva Eos Ami¬
gos. http://www.amazonconservation.org [accessed on 15/iv/2014]

Marcus E, Marcus EBR (1968) Uber einige Subulinidae (Pulmonata
von Sao Paulo). Beitrage zur Neotropischen Fauna 5(3): 186-208.
https://doi.Org/10.1080/01650526809360407

Miquel SE, Aguirre ME (2011) Taxonomia de los gasteropodos terrestres
del Cuatemario de Argentina. Revista Espanola de Paleontologia 26(2):
101-133.

Miquel SE, Tablado A, Sodor A (2007) Curaduria en la Coleccion Na-
cional de Invertebrados de Argentina: aportes a la biodiversidad y
biogeografia de gasteropodos terrestres argentinos. Comunicaciones
de la Sociedad Malacologica del Uruguay 9(90): 113-115.

Morretes FE (1949) Ensaio de catalogo dos moluscos do Brasil. Arqui-
vos do Museu Paranaense 7: 1-216.

d’Orbigny A (1834-1847) Voyage dans I’Amerique meridionale:
(le Bresil, la republique orientale de I’Uruguay, la Republique

argentine, la Patagonia, la republique du Chili, la republique de
Bolivia, la republique du Perou), execute pendant les annees 1826,
1827, 1828, 1829, 1830, 1831, 1832, et 1833. Tome Quatrieme. P.
Bertrand, Paris, 395 + 392 pp.

d’Orbigny A (1841-1845) Mollusques. In: de la Sagra R (Ed.) Histoire
Physique, Politique et Naturelle de file de Cuba. A. Bertrand, Paris,
1-264 [1], 1-380 [2].

Parodiz JJ (1957) Catalogue of the land Mollusca of Argentina. The
Nautilus 70: 127-135.

Pfeiffer E (1847) Diagnosen neuer Heliceen. Zeitschrift fur Malakozoo-
logie4: 31-32, 81-84.

Pfeiffer E (1856) Diagnosen neuer Eandschnecken. Malakozoologische
Blatter 3: 43-52.

Pilsbry HA (1906) Manual of Concho logy. Second Series. Pulmonata.
Vol. 18. Achatinidae: Stenogyrinae and Coeliaxinae. Academy of
Natural Sciences of Philadelphia, Philadelphia, 357 pp.

Pilsbry HA (1916-1918) Manual of Conchology, Second Series. Pul¬
monata. Vol. 24. Pupillidae (Gastrocoptinae). Academy of Natural
Sciences of Philadelphia, Philadelphia, 380 pp.

Quintana MG (1983) Catalogo preliminar de la malacofauna del Para¬
guay. Revista del Museo Argentine de Ciencias Naturales “Bernar¬
dino Rivadavia” (Zoologia) 1(3): 61-158.

Ramirez R, Borda V, Romero P, Ramirez J, Congrains C (2012) Biodi¬
versidad y endemismo de los caracoles terrestres Megalobulimus y
Systrophia en la Amazonia occidental. Revista Peruana de Biologia
19(1): 59-74. https://doi.org/10.15381/rpb.vl9il.798

Salgado NC, Coelho ACS (2003) Moluscos terrestres do Brasil (gas-
tropodes operculados ou nao, exclusive Veronicellidae, Milacidae
e Eimacidae). Revista de Biologia Tropical 51 (suppl. 3): 149-189.

Salvador RB, Cavallari DC, Simone ERE (2016) Taxonomical study
on a sample of land snails from Alto Ribeira State Park (Sao Pau¬
lo, Brazil), with description of a new species. Archiv ftir Molluske-
nkunde 145(1): 59-68. https://doi.org/10.1127/arch.moll/1869-
0963/145/059-068

Simone ERE (1999) Mollusca Terrestres. In Brandao CR, Cancello EM
(Eds). Invertebrados Terrestres, Vol. 5. Biodiversidade do Estado de
Sao Paulo, Brasil: sintese do conhecimento ao final do seculo XX.
FAPESP, Sao Paulo, 3-8.

Simone ERE (2006) Eand and freshwater mollusks of Brazil. EGB/
FAPESP, Sao Paulo, 390 pp.

Simone ERE (2013) Habeas, a new genus of Diplommatinidae from
Central Bahia, Brazil (Caenogastropoda), with description of three
new species. Journal of Conchology 41(4): 519-525.

Simone ERE, Salvador RB (2016) Taxonomical study on a sample of
land snails from Nanuque (Minas Gerais, Brazil), with description
of three new species. Stuttgarter Beitrage zur Naturkunde A, Neue
Serie 9: 9-30. https://doi.org/10.18476/sbna.v9.a2

Souza-Silva M, Ferreira RE (2015) Cave invertebrates in Espirito San¬
to state, Brazil: a primary analysis of endemism, threats and con¬
servation priorities. Subterranean Biology 16: 79-102. https://doi.
org/10.3897/subtbiol. 16.5227

Trajano E (2000) Cave faunas in the Atlantic tropical rain forest: com¬
position, ecology, and conservation. Biotropica 32(4b): 882-893.

Trajano E, Bichuette ME (2010) Diversity of Brazilian subterranean in¬
vertebrates, with a list of troglomorphic taxa. Subterranean Biology
7: 1-16. https://doi.Org/10.llll/j.1744-7429.2000.tb00626.x

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 143-155 | DOI 10.3897/zse.93.10188

4>yEnsPFr.

museum fur naturkunde

Diamond in the rough: a new species of fossorial diamond frog
{Rhombophryne) from Ranomafana National Park,
southeastern Madagascar

Shea M. Lambert^ Carl R. Hutter^, Mark D. Scherz^

1 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA

2 Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045-7561, USA

3 Zoologische Staatssammlung Munchen (ZSM-SNSB), Munchhausenstr. 21, 81247 Munich, Germany

http://zoobank.org/ACD2A947-BlB8-4B12-8FDF-1260C94B0AF8
Corresponding author: SheaM. (slambertl@email.arizona.edu)

Received 15 August 2016
Accepted 22 December 2016
Published 24 February 2017

Academic editor;

Johannes Penner

Key Words

Amphibia

Anura

Microhylidae

Rhombophryne nilevina

taxonomy

osteology

micro-CT

endemicity

herpetology

Abstract

We describe a new species from the cophyline microhylid genus Rhombophryne, a group
of fossorial and terrestrial frogs endemic to Madagascar. Found during herpetofaunal sur¬
veys of moist montane forest in the remote north of Ranomafana National Park, Rhom¬
bophryne nilevina sp. n. exemplifies two difficulties that hinder taxonomic progress in
Malagasy cophyline frogs; micro-endemicity and highly secretive habits. Known from
only two adult male specimens, this new species is nonetheless easily distinguishable
from all other known Rhombophryne using morphological data, and osteological data
collected here via X-ray Micro-Computed Tomography, or “micro-CT”. This species is
now the largest known Rhombophryne, and the only one known from Ranomafana Na¬
tional Park, which will make it the southern-most member of the genus pending a forth¬
coming taxonomic revision involving Plethodontohyla and Rhombophryne. Pairwise
distances of the mitochondrial 16s rRNA marker show a minimum genetic distance of
4.9% from other nominal Rhombophryne. We also describe recordings of an advertise¬
ment call, emitted from a burrow by the holotype. Rhombophryne nilevina sp. n. is not
known to be found syntopically with other Rhombophryne, nor to be present elsewhere in
Ranomafana National Park, but it probably does co-occur with a few ecologically similar
Plethodontohyla species. Although the type locality is within a protected area, we suggest
an lUCN listing of Data Deficient fori?, nilevina sp. n., as its area of occupancy is largely
undetermined within the park.

Introduction

Over the past several decades, integrative approaches to
taxonomy have shown that Madagascar’s anuran fauna
is one of the most spectacular on earth, with current es¬
timates approaching 600 species; 99.9% of which are en¬
demic to the island (reviewed in Vieites et al. 2009, Perl et
al. 2014). This estimate continues to rise as more candidate
species are newly discovered, with -465 species estimated
in Vietes et al. (2009), and -530 in Perl et al. (2014). Many
recent candidate species have been found from very few
localities, and are presumably restricted to small ranges
(e.g., Rosa et al. 2014, Hutter et al. 2015). Among clades

of Malagasy frogs, the subfamily Cophylinae Cope, 1889
(family Microhylidae Gunther, 1858) faces one of the
steepest taxonomic gaps, with more candidate species ex¬
isting than described species (Vieites et al. 2009, Perl et
al. 2014, Scherz et al. 2016a). This phenomenon is likely
explicable by the many challenges they present to system-
atists, including secretive habits, small range sizes, and
numerous morphologically cryptic species.

Rhombophryne Boettger, 1880 is a particularly enig¬
matic cophyline genus consisting of 16 valid nominal spe¬
cies (Scherz et al. 2016a,b), found primarily in rainforest
habitats of northern and eastern Madagascar. In addition
to fossorial or otherwise secretive habits, the apparently

Copyright Shea M. Lambert et al. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

144

Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

Rhombophryne laevipes unknown FGZC 1052
Rhombophryne laevipes Montagne d’Ambre ZSM 218/2004

r- Rhombophryne cf. mangabensis Antsiranana Andapa AMNH Al 81903

- Rhombophryne mangabensis Nosy Mangabe ZCMV 886

Rhombophryne savaka Marojejy ZCMV 2065
Rhombophryne mafai/y Foret d'Ambre FGZC 1888
Rhombophryne mafavy Foret d’Ambre FGZC 1890
Rhombophryne testudo Nosy Be ZSM 475/2000
— Rhombophryne testudo Nosy Be ZSM 474/2000
Rhombophryne botaboia ZCMV 11473

Rhombophryne botabota Ambolokopatrika MRSN A2640
Rhombophryne botabota Marojejy FGZC 2866
Rhombophryne botabota Marojejy ZCMV 2065
Rhombophryne nilevina Andemaka KU 340893
Rhombophryne sp CaOSTsaratanana MRSN A2631
Rhombophryne sp CaOSTsaratanana 2001 F5 FJ559296
Rhombophryne alluaudi Andasibe ZSM 3/2002
Rhombophryne a/Zoaod/Torotorofotsy ZC968
Rhombophryne alluaudiTsararano MRSN A2620

Rhombophryne sp CaOl tiampy FAZC 10314

r- Rhombophryne sp Ca09 Masoala MRSN A2115

Rhombophryne coudreaui Betampona fAZC 13887

-# Rhombophryne coudreaui Betampona MRSN A6347

Rhombophryne coudreaui Betampona MRSN A6271
Rhombophryne sp Ca10 llampy MRSN A2610

Rhombophryne sp Ca07 Tsaratanana 2001 G46

Rhombophryne longicrus Sorata forest FGZC 3651
A Rhombophryne minuta Marojejy FGZC 2897
^ Rhombophryne minuta Marojejy FGZC 2899
Rhombophryne sp Ambolokopatrika FAZC 7292
Rhombophryne vavenfy Antsiranana AMNH Al67315
Rhombophryne vaventy Marojejy FGZC 2842

_j- Rhombophryne coronata Mandraka ZSM 694/2001

^- Rhombophryne cf coronata KU 340732

Rhombophryne guentherpetersiTsaratanana ZCMV 12401

Rhombophryne /any Tsaratanana Camp 2 Matsaborimaika ZCMV 12359
Rhombophryne omafa Tsaratanana Camp 2 Matsaborimaika ZCMV 12384
Rhombophryne ornata Tsaratanana Camp 2 Matsaborimaika ZCMV 12382
Rhombophryne ornafa Tsaratanana Camp 2 Matsaborimaika DRV 6456

0.25

0.2 0.15 0.1

Substitutions per site

~r“

0.05

Black circle > 90% bootstrap
Gray circle < 90% bootstrap
White circle < 70% bootstrap

Figure 1. Phylogenetic relationships between Rhombophryne species estimated using maximum likelhood in RaxML using the mi¬
tochondrial 16S rRNA barcode fragment. Rhombophryne nilevina sp. n. is highlighted with blue bold text. Outgroups are removed
from the tree figure for aesthetic purposes.

small ranges of many species have historically impeded
data collection, and thus taxonomic progress, in the genus
(Glaw et al. 2010). However, fueled by the application
of integrative taxonomic approaches, the number of de¬
scribed Rhombophryne has swelled in recent years, with 8
species described since 2010 (D’Cruze et al. 2010, Glaw
et al. 2010, Scherz et al. 2014, 2015a,b, 2016b), and only
a few already-published candidate species left to be de¬
scribed (Scherz et al. 2016b), although several more have
been identified and will be described soon (Fig. 1 and
Scherz, Crottini, et al. unpubl. data).

We herein describe Rhombophryne nilevina sp. n., dis¬
covered during herpetofaunal surveys of moist montane
forest in the remote north-western corner of Ranomafa-
na National Park, southeastern Madagascar, in January of
2015. We diagnose R. nilevina sp. n. from its congeners
using morphological and osteological characters collect¬
ed with the help of X-ray Micro-Computed Tomography
(micro-CT). We also describe the male advertisement call
of the new species, which is distinct from all other known
vocalizations in the genus.

Methods

Specimen collection

We collected specimens during the day through targeted
searching, using the advertisement call to locate males. We

euthanized specimens using 20% benzocaine, fixed them
in -10% formalin solution buffered with sodium phosphate
to pH 7.0, and hansferred them to 70% ethanol for long¬
term storage after approximately two weeks. We deposited
the holotype in the Biodiversity Institute of the University
of Kansas (KU) and a paratype in the Mention Zoologie
et Biodiversite Animal, Faculte des Sciences, Universite
d’Antananarivo (formerly Departement de Biologic Ani-
male of the Universitee d’Antananarivo; UADBA).

DNA barcoding and phylogenetic analysis

Immediately following euthanasia, we removed the
tongue and placed it in 95% EtOH. We extracted genomic
DNA using standard phenol-chloroform extraction proto¬
col and amplified a fragment of the mitochondrial rRNA
marker 16S using a previously published protocol (Hutter
et al. 2015). We include a total of seven newly generated
16S sequences in this study; one of R. nilevina sp. n., one
tentatively assigned to R. coronata, and five outgroup se¬
quences (Table 1). We acquired sequences of the same 16S
fragment for other Rhombophryne from Genbank. Prior
to alignment, we removed identical sequences using the
“Find Duplicates” option in Geneious version 6 (Kearse
et al. 2012). All retained sequences and their accession
numbers are listed in Table 1. We aligned sequences with
the MAFFT (Katoh and Standley 2013) plugin version
1.3 for Geneious, using the the “E-INS-i” algorithm and
otherwise default settings. We inferred phylogenetic re-

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145

Table 1. GenBank Accession numbers for all sequences used in phylogenetic analysis. Asterisks indicate newly generated sequences.

Species

Locality

Voucher number

Accession

Platypelis barbouri*

Ambatomandondona

KU 340681

KY288471

Platypelis pollicaris*

Torotorofotsy

KU 340614

KY288472

Platypelis tuberlfera*

Vohidrazana

CRH 286

KY288470

Plethodontohyla inguinalis*

Vohidrazana

KU 340642

KY288474

Rhombophryne alluaudi

Andasibe

ZSM 3/2002

DQ019606

Rhombophryne alluaudi

Torotorofotsy

ZCMV 968

FU341105

Rhombophryne alluaudi

Tsararano

MRSN A 2620

AY594105

Rhombophryne cf. coronata*

Vohidrazana

KU 340732

KY288476

Rhombophryne coronata

Mandraka

ZSM 694/2001

FU341103

Rhombophryne coudreaul

Betampona

FAZC 13887

FJ559299

Rhombophryne coudreaul

Betampona

MRSN A 6271

HM364771

Rhombophryne coudreaul

Betampona

MRSN A 6347

HM364772

Rhombophryne guentherpetersi

Tsaratanana

ZCMV 12401

KU937796

Rhombophryne laevipes

Montagne d’Ambre

ZSM 218/2004

FU341104

Rhombophryne laevipes

Montagne d’Ambre

FGZC 1052

KM509189

Rhombophryne longicrus

Sorata forest

FGZC 3651

KR025897

Rhombophryne mangabensis

Nosy Mangabe

ZCMV 886

KU724181

Rhombophryne matavy

Foret’d Ambre

FGZC 1888

FJ559298

Rhombophryne matavy

Foret’d Ambre

FGZC 1890

GU195641

Rhombophryne cf. mangabensis

Antsiranana, Andapa

AMNH 181903

KM509192

Rhombophryne minuta

Marojejy

FGZC 2897

FU341100

Rhombophryne minuta

Marojejy

FGZC 2899

FU341106

Rhombophryne ornata

Tsaratanana Camp Matsaborimaika

DRV 6456

KP895582

Rhombophryne ornata

Tsaratanana Camp Matsaborimaika

ZCMV 12382

KP895583

Rhombophryne ornata

Tsaratanana Camp Matsaborimaika

ZCMV 12384

KP895584

Rhombophryne savaka

Marojejy

ZCMV 2065

KU724176

Rhombophryne serratopalpebrosa

Ambolokopatrika

FAZC 7292

FU341111

Rhombophryne sp. CaOl

llampy

FAZC 10314

FJ559295

Rhombophryne sp. Ca03

Tsaratanana

MRSN A 2631

AY594107

Rhombophryne sp. Ca03

Tsaratanana

ZSM 667/2001

FJ559296

Rhombophryne botabota

Ambolokopatrika

MRSN A 2640

AY594104

Rhombophryne botabota

Marojejy

FGZC 2866

FU341102

Rhombophryne botabota

Marojejy

ZCMV 2065

FJ559297

Rhombophryne sp. Ca07

Tsaratanana

2001 G46

FU341108

Rhombophryne sp. Ca09

Masoala

MRSN A 2115

AY594110

Rhombophryne sp. CalO

llampy

MRSN A 2610

AY594111

Rhombophryne nllevina sp. n. *

Andemaka

KU 340893

KY288475

Rhombophryne botabota

Makira

ZCMV 11473

KU724173

Rhombophryne tany

Tsaratanana Camp Matsaborimaika

ZCMV 12359

KP895585

Rhombophryne testudo

Nosy Be

ZSM 474/2000

KC180070

Rhombophryne testudo

Nosy Be

ZSM 475/2000

FU341110

Rhombophryne vaventy

Antsiranana

AMNH A167315

DQ283409

Rhombophryne vaventy

Marojejy

FGZC 2842

FU341107

Scaphlophryne marmorata*

Torotorofotsy

KU 340620

KY288473

lationships with RaxML 8.2.6 (Fig. 1; Stamatakis 2014),
using the -f a option to search for a maximum likelihood
tree and conduct 1000 rapid bootstrap replicates, under the
GTR model of sequence evolution and with gamma dis¬
tributed rate variation. Finally, we calculated raw pairwise
genetic distances from the alignment using the dist.dna
function of the ape package in R (Table 2, Paradis et al.
2004, R Development Core Team 2016).

Morphology

We took morphological measurements using a digital cali¬
per to 0.01 mm, rounded to 0.1 mm. We note that only the

holotype was measured, as the paratype was unavailable
for study. Measurements follow the standard for this genus
and are repeated here verbatim from Scherz et al. (2015b):
“SVL (snout-vent length), HW (maximum head width),
HL (head length, from the maxillary commissure to the
anterior-most point of the mouth), ED (horizontal eye di¬
ameter), END (eye-nostril distance), NSD (nostril-snout
tip distance), NND (intemarial distance), TDK (horizontal
tympanum diameter), TDV (vertical tympanum diame¬
ter), HAE (hand length, from the metacarpal-radioulnar
articulation to the tip of the longest finger), EAE (lower
arm length, from the carpal-radioulnar articulation to the

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Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

Table 2. Raw genetic distances at the 16s rRNA gene frag¬
ment between analysed taxa and Rhombophryne nilevina sp. n.
(KU 340893).

Taxon

Distance

Rhombophryne sp. Ca03 (Tsaratanana)

3.80%

Rhombophryne alluaudi
(Andasibe, Torotorofotsy, Tsararano)

4.89-5.98%

Rhombophryne botabota
(Ambolokopatrika, Marojejy, Makira)

5.98%

Rhombophryne sp. CaOl (llampy)

7.61%

Rhombophryne minuta (Marojejy)

9.78-10.32%

Rhombophryne sp. CalO (llampy)

10.87%

Rhombophryne tany

(Tsaratanana Camp 2 Matsaborimaika)

11.41%

Rhombophryne 1 aevipes (Montagne d’Ambre)

11.41%

Rhombophryne guentherpetersi (Tsaratanana)

12.50%

Rhombophryne vavenfy (Antsiranana, Marojejy)

11.96-12.50%

Rhombophryne testudo (Nosy Be)

11.96%

Rhombophryne coronata (Mandraka)

11.96%

Rhombophryne sp. Ca07 (Tsaratanana)

12.50%

Rhombophryne mangabensis (Nosy Mangabe)

13.04%

Rhombophryne sp. “Ambolokopatrika”
(Ambolokopatrika)

13.04%

Rhombophryne longicrus (Sorata)

11.96%

Rhombophryne of. mangabensis (An da pa)

12.50%

Plethodontohyla ingulnalis (Vohidrazana)

13.59%

Rhombophryne ornata

(Tsaratanana Camp 2 Matsaborimaika)

13.59%

Rhombophryne coudreaui (Betampona)

14.13%

Rhombophryne sp. Ca09 (Masoala)

13.59%

Platypelis pollicaris (Torotorofotsy)

15.76%

Rhombophryne of. coronata (Vohidrazana)

15.22%

Platypelis barbourl (Ambatomandondona)

16.30%

Rhombophryne matavy (Foret d’Ambre)

19.02%

Platypelis tuberlfera (Vohidrazana)

18.48%

Scaphiophryne marmorata (Torotorofotsy)

23.37%

center of the radioulna-humeral articulation), UAL (upper
arm length, from the center of the radioulna-humeral ar¬
ticulation to the trunk, measured along the posterior aspect
of the arm), FORL (forelimb length, given by the sum of
HAL, LAL, and UAL), FOL (foot length, from the tarsal-
metatarsal articulation to the tip of the longest toe), TARL
(tarsal length, from the tarsal-metatarsal articulation to
the tarsal-tibiofibular articulation), FOIL (foot length in¬
cluding tarsus, from the tibiotarsal articulation to the tip
of the longest toe, given by the sum of FOL and TARL),
TIBL (tibiofibula length), TIBW (tibiofibula width at
thickest point, measured in dorsal aspect), THIL (thigh
length, from the vent to the femoral-tibiofibular articula¬
tion), THIW (thigh width at thickest point, measured in
supine position), HIL (hindlimb length, given by the sum
FOL, TARL, TIBL, and THIL), IMCL (maximum length
of inner metacarpal tubercle), IMTL (maximum length
of the inner metatarsal tubercle).” A figure depicting the
measurement scheme is presented in Scherz et al. (2015b).

Osteology

We performed micro-CT scanning on a phoenix|x
nanotom m cone-beam scanner (GE Measurement &

Control, Wunstorf, Germany), using a tungsten target and
a 0.1 mm Cu filter. We employed settings of 140 kV and
80 pA, with a timing of750 ms, for 2440 projections and a
total scan time of 30 minutes. We assembled the scan files
in datos|x 2 reconstruct CT software (GE Measurement &
Control, Wunstorf, Germany), and imported them as an
unsigned 8-bit volume into VG Studio Max 2.2 (Volume
Graphics GMbH, Heidelberg, Germany). We used the
phong renderer with a custom color palate and rendering
curve to register and visualize the scan. Using the built-in
function, we took high-resolution screenshots for the pro¬
duction of figures. The osteological information present¬
ed is based on volume rendering. Only slightly calcified
cartilage can be visualized using micro-CT, so we omit
descriptions of the cartilaginous structures of the pectoral
girdle (sternal features and most of the suprascapula) and
those associated with the skull (the hyoid plate and nasal
cartilages in particular). A Digital Imaging and Commu¬
nications in Medicine (DICOM) stack of the scan files
and rotational video produced in VG Studio Max 2.2 are
available at the following MorphoSource http://morpho-
source. org/Detail/Proj ectDetail/Show/proj ect_id/263

We exported the volume as an “Analyze Volume” un¬
der standard settings in VG Studio Max 2.2, and imported
the resulting .hdr file into Amira 6.1 (FEI Visualization
Sciences Group, Burlington MA, USA), where a surface
model was produced essentially following Ruthenstein-
er and HeB (2008). This model is embedded in a Sup-
pi. material 1. The model is provided solely for reader
comprehension; surface models carry inherent bias due
to the manual thresholding are therefore less reliable for
osteological description than volume renderings (Scherz
et al. in review).

We note that skeletal comparisons to other cophylines
are based on largely unpublished micro-CT data pro¬
duced by MDS, which will be involved in revisions of
the genera of this subfamily over the next few years.
However, micro-CT-based osteological accounts for
Rhombophryne, Stumpffia, Anilany, and Plethodontohyla
are found in Scherz et al. (2016a) and for Cophyla and
Platypelis in Rakotoarison et al. (2015).

Bioacoustics

We recorded calls attributed to the holotype on two oc¬
casions using an Olympus ES-10 Einear PCM Field Re¬
corder and a Sennheiser K6-ME66 super-cardioid shot¬
gun microphone. The calls were recorded at a sampling
rate of 44.1 kHz and 16 bits resolution in WAV format.
Recordings were made at mid-day in overcast weather
conditions. No precise temperature recordings are avail¬
able, but we estimate that the ambient temperature was
approximately 20° C at the time of recording. We note
that the individual was not visible during the recordings,
as it was calling from a burrow. We therefor e cannot be
completely certain that the recordings are of the same in¬
dividual, however, only a single individual at a time was
heard calling from this location, and the collected indi¬
vidual was found with distended vocal sac shortly after

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147

Table 3. The advertisement call recorded for Rhombophryne ni-
levina in comparison with that of R. testudo. Calls were record¬
ed from males calling during the day that were subsequently
collected as vouchers. Note envelope is the ratio of the time of
peak amplitude to note duration. Data are the range and then the
mean ± two standard deviations in parentheses, when appropri¬
ate. The call recording of R. testudo is from Vences et al. (2006).

Parameters

Species

R. nilevina

R. testudo

Specimen number

KU 340897

Locality

Ranomafana

Nosy Be

N - calls

Inter-call interval duration (s)

42.5-99.5
(68.77 ± 24.0)

5.98-10.1
(8.3 ± 2.1)

Call duration (ms)

505-544
(536 ± 1.7)

828-896
(853 ± 2.9)

Call envelope

0.601-0.787
(0.663 ± 0.073)

Number of amplitude peaks

3-5

(3.4 ± 0.5)

Fundamental frequency (Hz)

236.9-279.9
(261.5 ± 22.9)

258.4-279.9
(263.8 ± 10.8)

Dominant frequency
throughout call (Hz)

528.3-538.8
(537.9 ±9.2)

538.3-555.9
(542.8 ± 8.8)

Dominant frequency
at peak amplitude (Hz)

528.3-538.8
(537.9 ±9.2)

581.4-602.9
(586.8 ± 10.8)

First Harmonic (Hz)

775.2-818.3
(796.7 ± 17.6)

775.2-796.7
(791.3 ± 10.8)

the second recordings. Additionally, the measured call
parameters from the two occasions are nearly completely
overlapping (Fig. 4; Table 3).

We follow Rakotoarison et al. (2015) and define a call
as individual temporally distinct segments separated by a
return to the background noise between each of these seg¬
ments. This definition is equivalent to single notes used in
other call definitions (Duellman and Tmeb 1994; mantel-
lids: Hutter et al. 2015). We define calls as “amplitude mod¬
ulated” when there are two or more clear amplitude peaks.

Following Rakotoarison et al. (2015) and Hutter and
Guayasamin (2015), we report the following call vari¬
ables: call duration (ms); inter-call interval (s); number
of amplitude peaks; note envelope shape (time at peak
amplitude / call duration); dominant frequency (Hz),
measured throughout call and at peak amplitude; fun¬
damental frequency (Hz); and first harmonic frequency
(Hz). Call rate was not calculated because of insufficient
sample size. We used Raven Pro 1.4 to measure tempo¬
ral and spectral call characteristics. Digital recordings are
deposited at the University of Kansas Biodiversity Insti¬
tute digital archive and are available upon request.

Registration of nomenclature

The electronic version of this article in Portable Document
Format (PDF) will represent a published work according
to the International Commission on Zoological Nomen¬
clature (ICZN), and hence the new names contained in
the electronic version are effectively published under that

Code from the electronic edition alone. This published
work and the nomenclatural acts it contains have been
registered in ZooBank, the online registration system for
the ICZN. The ZooBank LSIDs (Life Science Identifiers)
can be resolved and the associated information viewed
through any standard web browser by appending the
LSID to the prefix http://zoobank.org/. The LSID for this
publication is: urn:lsid:zoobank.org:pub:ACD2A947-
B1B8-4B12-8FDF-1260C94B0AF8. The online version
of this work will be archived and made available from the
following digital repositories: CLOCKSS and Zenodo.

Results

We discovered a large-bodied cophyline microhylid
frog near Andemaka within Ranomafana National Park
in eastern Madagascar. Several obvious differences in
morphology exist between the collected specimens and
all known described and undescribed cophyline mi-
crohylids. Analysis of a fragment of its mitochondrial
16S rRNA gene recovered it with a close relationship
to an undescribed population of Rhombophryne from
northern Madagascar (sp. Ca03 from Vieites et al. 2009;
Fig. 1). However, this population is quite distinct from
the newly collected frogs morphologically (Scherz et al.,
unpubl. data). We also note that the 16S tree is largely
unresolved, likely due to a limited number of characters
it includes. Ongoing multi-locus analyses suggest that
R. nilevina is quite phylogenetically distinct from all
known Rhombophryne, including sp. Ca03 (A. Crottini,
pers. comm.). Our 16S analysis also shows a minimum
genetic distance of 4.9% between our new taxon and
all valid, nominal Rhombophryne species (Table 2). We
therefore describe it as a new species:

Rhombophryne nilevina sp. n.

http://zoobank.org/DAD2876A-D5C4-4D7B-B712-B22013161FC4
Suggested common English name: The buried diamond frog
Suggested common Malagasy name: Sahona diamondra nilevina
Suggested common French name: La grenouille de diamant enterre

Holotype. KU 340897 (CRH 798), an adult male collect¬
ed at mid-day on February 8* 2015 by Shea Maddock
Lambert, Emile Rajeriarison, and Ralaivao Jean Ful-
gence in montane rainforest near the former village of
Andemaka in Ranomafana National Park (ca. 21.1287°S,
47.5054°E, elevation ca. 1240m a.s.l.; Fig. 2).

Paratype. UADBA-A Uncatalogued (CRH 799), an
adult male collected the morning of February 7* 2015
by Shea Maddock Eambert and Ralaivao Jean Fulgence,
otherwise with the same collection information as the
holotype.

Diagnosis. A frog assigned to the cophyline genus
Rhombophryne on the basis of its divided vomer, the

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Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

Figure 2. Map of Ranomafana National Park and the type locality of Rhombophryne nilevina sp. n.. Map is a composite of Landsat
8 satellite imagery and a hillshade layer created from SRTM 1 Arc-Second Global digital elevation data. Data available from the
U.S. Geological Survey.

possession of clavicles andknob-shapedterminal phalanges
(see Scherz et al. 2016a). This species is characterized by
the following suite of characters: large size (SVL at least
up to 57.2 mm), wide, short head (HW 180.7% of HL),
tympanum 58.6% of eye, forelimb 51.1% of SVL, tibia
42.2% of SVL, hindlimb 152.5% of SVL, large inner
metacarpal and metatarsal tubercles, supratympanic fold
distinct and raised, running from the posterior comer of
the eye straight over the tympanum, then sharply down
behind it, extending to join the front of the arm, distinct
vomerine teeth forming curved rows posteromedial to
the oblong choanae, separated medially by a small cleft,
second finger shorter than fourth finger, fifth toe distinctly
shorter than third, without finger or toe reduction, finger
and toe tips not enlarged. Additionally, R. nilevina is
separated from all nominal species of Rhombophryne by
an uncorrected pairwise distance of at least 4.9% in the
fragment of the 16S rRNA gene, and by at least 3.8% from
all known candidate species in this genus.

Rhombophryne nilevina is the largest species in the
genus Rhombophryne, and can be distinguished based on
this character alone from all other described species (SVL
57.2 mm vs. maximums of 56.3 mm and 52.9 mm for the
next two largest species, R. laevipes and R. vaventy, re¬

spectively). This species differs from all of its congeners
as follows: from all members of the R. serratopalpebrosa
group {R. serratopalpebrosa, R. coronata, R. vaventy, R.
ornata, R. tany, and R. guentherpetersi, plus two species
under description by Scherz et al. in review) by the ab¬
sence of superciliary spines (vs. presence); from R. testu-
do, R. coudreaui, and R. matavy by less wide head (HW
180.7% vs. 187.6-242.4% of HL in R. testudo and R.
matavy), longer forelimb (FORL 51.1% vs. 35.4^9.8%
of SVL), longer hindlimb (HIL 152.5% vs. 117.4-140.8%
of SVL), and the possession of a clavicle (vs. lack there¬
of); from R. longicrus and R. minima by its wider head
(HW 180.7% vs. 122.5-142.8% of HL), shorter forelimb
(FORL 51.1% vs. 70.4-74.7% of SVL), and shorter hind¬
limb (HIL 152.5% vs. 178.5-183.8% of SVL); from R.
savaka and R. mangabensis by its longer forelimb (FORL
51.1% vs. 40.9-47.9% of SVL), well ossified clavicles
(vs. poorly ossified), and absence of black inguinal spots
and a mid-vomerine diastema (vs. presence in R: savaka)-,
and from R. alluaudi, R. laevipes, and R. botabota by its
wider head (HW 180.7% vs. 144.2-173.8% of SVL), ab¬
sence of light dorsolateral stripes (vs. presence inR. allu¬
audi), absence of a stark color border between the dorsal
and lateral parts of the head (vs. presence in R. botabota).

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149

absence of inguinal ocellations (vs. presence in R. laevi-
pes and R. alluaudi).

Rhombophryne nilevina is morphologically similar
to terrestrial members of the genus Plethodontohyla, but
aside from being distinguishable from this genus by the
combination of the possession of clavicles with knob¬
shaped terminal phalanges, this species can be distin¬
guished from P. inguinalis by its smaller size (SVL 57.2
vs. 62.2-99.1 mm), the absence of enlarged fingertips,
absence of dark inguinal spots (vs. occasional presence),
and absence of a strong dorsolateral color border (vs. occa¬
sional presence); from P. notosticta, P guentheri, P fonet-
ana, and P. mihanika by the absence of enlarged fingertips,
absence a strong dorsolateral color border (vs. presence in
all but P. fonetana), and shorter forelimb (FORL 51.1% vs.
57.5-71.9% of SVL); and from P. bipunctata, P tuberata,
P brevipes, and P ocellata by the absence of inguinal spots
(vs. presence in all but P. tuberata) and larger size (SVL
57.2 vs. 24.6^4.7 mm) and from P. tuberata by the pres¬
ence of smooth skin (vs. granular skin).

Although the bioacoustic repertoires of cophylines is
far from completely known, bioacoustically, this species’
call is strongly distinct from the other known calls by be¬
ing strongly amplitude modulated (Fig. 4). To the human
ear, this call most closely resembles the genetically dis¬
tant R. testudo (Table 2), but the call of R. testudo differs
by having a much longer duration and lacking significant
amplitude modulation (Fig 4). No other known calls can
be confused with those of this species.

Description of the holotype. Morphology of the holo-
type. An adult male specimen in an excellent state of
preservation. The vocal sac is still somewhat loose and
malleable. The tongue was removed as a tissue sample.

Body rotund; dorsal and ventral skin smooth, with sub¬
tle bumps on the dorsal skin (more rugose in life). Head
considerably wider than long (HW 180.7% of HL), snout
rounded in dorsal and lateral view; nostrils protuberant, di¬
rected laterally, closer to the snout than the eye; canthus
rostralis distinct and concave; loreal region concave and
oblique; tympanum indistinct, oval, horizontally 58.6% of
eye diameter; pupil dilated in preservative but more or less
round in life (Fig. 3a, 3d); supratympanic fold distinct and
raised, running from the posterior comer of the eye straight
over the tympanum, then sharply down behind it, extend¬
ing to join the front of the arm; tongue removed as a tissue
sample, was attached anteriorly and posteriorly free; vom¬
erine teeth distinct, forming curved rows posteromedial to
the choanae; choanae relatively large, oblong.

Arms strongly built, relatively short; fingers without
webbing, short, with distinct, rounded subarticular tuber¬
cles, relative lengths 1<2<4<3, the second finger margin¬
ally shorter than the fourth (and marginally longer than the
first), without enlarged terminal discs; inner metacarpal
tubercle strong, oblong, 28.1% of hand length; outer meta¬
carpal tubercle indistinct, round. Legs relatively long and
thick (HIL 152.5% of SVL; TIBL 42.2% of SVL), posi¬
tion of the tibiotarsal articulation when adpressed along the

body not possible to assess without breaking the hindlimbs;
toes long, unwebbed, with indistinct round subarticular tu¬
bercles, relative toe lengths 1<2<5<3<4, third toe distinctly
longer than fifth; inner metatarsal tubercle present and dis¬
tinct, 12.7% of foot length; outer metatarsal tubercle absent.

Coloration of the holotype. In preservative, the holo¬
type is chocolate brown dorsally with a loosely reticulat¬
ed pattern of ebony to burnt umber markings, including
an indistinct interocular bar. There are no inguinal spots.
The loreal region has a grey marking in it. The forelimb
is as the dorsum, with dark patches on the elbow and a
crossband on the forearm. A distinct light annulus is pres¬
ent before the terminus of each finger. The hindlimb is
dorsally as the back, with three dark crossbands on the
thigh and shank. The posterodorsal thigh has weak cream
spots, as does the anterior thigh. The dorsal foot is brown
speckled with cream. The toes are even more flecked with
cream, and also possess a light annulus before the termi¬
nal phalanges. The ventral abdomen is brown with nu¬
merous small cream flecks. The chin is darker and mostly
solid dark brown. The ventral arms are as the trunk. The
subarticular and metacarpal tubercles are lighter in color
than the rest of the hand. The ventral hindlimbs are as the
abdomen. The color in life was as in preservative (Fig. 3).

Osteology of the holotype (Fig. 5, Suppl. material 1).
The skeleton of the holotype is typical of Rhombophryne.
It is well ossified and robust. The right femur shows signs
of an old break toward its distal end that has healed.

Anterior braincase laterally closed by the spheneth-
moid. Interior braincase containing calcified material.
Nasal in medial contact with contralalteral and posteri¬
or contact with frontoparietal. Frontoparietal broadening
anteriorly from narrow waist anterior to lateral flanges,
possessing a strong, posteriorly elongated dorsal process.
Prechoanal vomer simple, triradiate. Neopalatine and
postchoanal vomer distinguishable. Vomerine teeth not
medially fused, without diastemata, oriented oblique to
antero-posterior body axis, curved. Maxillary teeth min¬
ute. Otic capsule dorsally poorly ossified.

Sternum not ossified. Clavicle robust, curved. Humer¬
us proximally broad, distally rather narrow; possessing
a well-developed crista ventralis along roughly 50% of
its length; crista lateralis weak. Terminal phalanges of
fingers and toes with small distal knobs. Phalangeal for¬
mula of fingers 2-2-3-3; of toes 2-2-3-4-3. Femur without
cristae. Prepollex strong, blade-like, half length of first
metacarpal. Prehallux strong, approximately half length
of first metatarsal.

Neural spines decrease in size posteriorly, the sixth
and seventh lacking spines altogether. Neural arches of
atlas fused. Dorsal crest of urostyle running roughly 80%
along its shaft. Iliosacral articulation type IIA sensu Em¬
erson 1979. Iliac shafts with well developed dorsal tuber¬
cles and deep oblique grooves; dorsal crests running most
of their length. Pubis partially ossified.

Variation. The paratype UADBA-A Uncatalogued (CRH
799) strongly resembles the holotype, but has a slightly

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Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

Figure 3. Photos in life of Rhombophryne nilevina sp. n. (a) Dorsolateralview of the holotype (KU 340893). (b) Dorsal view of the
holotype. (c) Ventral view of the holotype. (d) Dorsolateral view of the paratype (CRH 799, UADBA-A Uncatalouged). (e) Dorsal
view of the paratype. (f) Ventral view of the paratype.

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Zoosyst. Evol. 93 (1) 2017, 143-155

151

more distinct color border between the lateral and dorsal
head (see Fig. 3 for comparison).

Bioacoustics. We analysed a total of seven calls from
R. nilevina, and compared these to the call of R. testudo
(Fig. 4; Table 3). We presume that the calls we recorded
come from one individual, the holotype (see Materials
and methods). We further assume that the recorded call
is an advertisement call, as no other call types (except dis¬
tress calls) are known from cophylines. This call sounds
like a slow groan to the human ear.

Each call is rapidly pulsed, with 3-5 (3.5 ± 0.534)
amplitude modulated peaks occurring throughout the
call, and peak amplitude occuring in the last 50% of
the call. The call duration is 505-544 (536 ± 1.7) ms
with an inter-call interval duration of 42.5-99.5 (68.8
± 24.0) s. The fundamental frequency is 236.9-279.9
(261.5 ± 22.9) Hz. The mean dominant frequency
throughout the call was 528.3-555.9 (537.9 ± 9.2) Hz
and the first harmonic frequency is 775.2-818.3 (796.8
± 17.6) Hz (Fig. 4).

Etymology. The specific epithet “nilevina” is a Malagasy
word meaning “buried.” This name was chosen to recog¬
nize the fossorial habits of this species. It is to be treated
as an invariable noun in apposition.

Available names. Due to morphological and size simi¬
larities, as well as geographic distribution, two existing
names must be considered for this species: Phryno-
cara laeve Boettger, 1883, and Plethodontohyla laevis
tsianovohensis Angel, 1936. Both of these names are
currently considered to be junior synonyms of Rhombo-
phryne alluaudi. We examined the morphology and os¬
teology of the holotypes of both of these taxa {P. laeve:
SMF 4286; P. laevis tsianovohensis: MNHN 1936.47),
and our new species differs critically from both in the
possession of a well-developed clavicle (vs. absence/
strong reduction; Scherz unpubl. data). Their taxonomy,
as well as that of Rhombophryne alluaudi, will be dis¬
cussed in a future article, and we here simply rule out
the possibility that they are conspecific with R. nilevina
sp. n. based on the presence vs. absence of a clavicle.
The type specimen of P. laevis tsianovohensis was col¬
lected from Tsianovoha, which is around 60 km south of
Ranomafana, suggesting the possibility of sympatry or
parapatry with R. nilevina.

Natural history. Both known specimens of R. nilevina
were obtained from a relatively fiat, poorly drained
section of moist montane forest adjacent to a stream,
with the holotype found along the bank of this stream.
Nearby habitats include a swamp with many large
Pandanus and steep forested slopes with relatively
smaller trees. However, the calls of R. nilevina seemed
to emanate mostly from the flatter, forested area. Males
were heard calling during the day, particularly during

overcast conditions and after rainfall. Advertisement
calls were not heard at night, however, the night-time
chorus of other frogs, including Boophis, Spinomantis,
Gephyromantis, and Anodonthyla, may have interfered
with detection. When heard from a distance, the call is
reminiscent of that of an owl. When heard from close
proximity, the call sounds like a groan, and is far less
melodic. Both specimens were both located by auditory
tracking, and found calling from underground: one
from a cavity under the roots of a large tree, and the
other from a burrow in soft, moist soil alongside the
stream. In order to collect the holotype from its burrow,
excavation was required. Based on these observations
and suggestive morphology, we presume thatR. nilevina
spend much of their lives underground, possibly
coming to the surface for short periods during rainfall,
similar to other fossorial Rhombophryne species (Glaw
and Vences 2007, D’Cruze et al. 2010). We also note
that R. nilevina was discovered in the middle of the wet
season, and after a week-long period of particularly
heavy, sustained rain.

Distribution. Rhombophryne nilevina has thus far been
detected at a single site, near the former village of An-
demaka, in the north-west of Ranomafana National Park
(Fig. 2). This locality is relatively high-elevation for
Ranomafana National Park (ca. 1240 m). To our knowl¬
edge, R. nilevina has not been detected by any previous
survey, including several conducted by CRH and SML
at similarly high-elevation sites in the northern (Miara-
nony), central (Vohiparara), and southern (Maharira) re¬
gions of Ranomafana. Nevertheless, we do not rule out
here the possibility that R. nilevina occurs elsewhere in
the park. This is in large part due to the secretive hab¬
its and potentially ephemeral activity periods of this
species (see Natural history). In addition, much of the
high-elevation forest of Ranomafana is difficult to ac¬
cess and thus remains sparsely or completely unsurveyed
for herpetofauna. Although it is possible that R. nilevina
has been overlooked in other eastern rainforest patches,
current information suggests that this species is endemic
to Ranomafana National Park, and potentially to a much
smaller area within the park.

Conservation status. Although the type locality of R.
nilevina is within Ranomafana National Park, its occu¬
pancy within the park is potentially highly restricted, ele-
vationally and geographically, as it has not been detected
in any other herpetological surveys of the park. However,
its secretive lifestyle means that it icould be easily over¬
looked. Given this large uncertainty in area of occupancy,
we suggest an initial lUCN categorization of Data Defi¬
cient. If R. nilevina is for instance, restricted to the type
locality, then habitat destruction, chytrid fungus (recently
detected in Madagascar, Bletz et al. 2015), and/or climate
change could easily place the only population of R. nile¬
vina sp. n. at risk of extinction.

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Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

sq.zr

“f^§Lprsph.cp
—spheth

povom+npl
-nasal
— prvom

y—smx

-max.pf

lax

^—angspi
angspl.cp

dentary

■prvom

■nasal-

-npl—
povom

spheth

-prsph.cp

max

pter.vr

qj.pvp-

exoc

prsph.ap

sq.zr

pmx-
smx-

max.pf

Figure 4. The osteology of Rhombophryne nilevina sp. n. Skull in (a) lateral, (b) dorsal, and (c) ventral view; and full skeleton in
(d) dorsal and (e) ventral view. Abbreviations: angspi, angulosplenial; angspl.cp, angulosplenial coronoid process; col, columella;
exoc, exoccipital; fpar, frontoparietal; fpar.dop, frontoparietal dorsal process; max, maxilla; max.pf, maxillary pars fascialis; mmk,
mentomeckelian bone; npl, neopalatine; pmx, premaxilla; povom, postschoanal vomer; proof prootic; prvom, prechoanal vomer;
prsph.ap, parasphenoid alary process; prsph.cp, parasphenoid cultriform process; pter.ar, pterygoid anterior ramus; pter.vr, pterygoid
ventral ramus; pter.mr, pterygoid medial ramus; qj, quadratojugal; qj.pvp, quadratojugal posteroventral process; smx, septomaxilla;
spheth, sphenethmoid; sq, squamosal; sq.or, squamosal otic ramus; sq.zr, squamosal zygotic ramus.

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Zoosyst. Evol. 93 (1) 2017, 143-155

153

4000

N 3000 .. »•

c 2000

9 ^ 1000

1 n

.> 3
^ = 0
0 p

-1

—I—

200

400

600

800

Relative

amplitude

I I I I

0 200 400 600 800 1000

Time (ms)

500

1000

1500

2000 0

500

1000

1500

2000

Frequency (Hz)

Figure 5. Comparative spectrograms (top), oscillograms (center) and power spectra (bottom) between the calls of (A) Rhombo-
phryne nilevina sp. n. and (B) R. testudo (from Vences et al. 2006). Spectrogram was created using a Hanning window size of 1024.

Discussion

The discovery of Rhombophryne nilevina —never pre¬
viously identified as a candidate species despite being
found in one of the most well-surveyed National Parks
of Madagascar—highlights the importance of continued
field work for the advancement of systematics in Mal¬
agasy anurans. In particular, field surveys should help
reveal diversity in clades containing species with small
ranges and secretive life histories, including Rhombo¬
phryne and other cophyline frogs. Cophylines have al¬
ready shown great promise as a model system for study¬
ing ecomorphological and reproductive mode evolution
(e.g. Andreone et al. 2005, Wollenberg et al. 2008), and
the continued discovery and description of novel species
will only further this potential.

Rhombophryne nilevina is remarkable in several re¬
spects, including its morphology. Most obvious is its
large size, the largest recorded for the genus, narrowly ex¬
ceeding R. laevipes (Glaw & Vences, 2007; Scherz et al.

unpubl. data). In addition, the relatively long legs, wide
head, and rotund body shape contribute to the distinctive
appearance of this species. In total, the morphology of R.
nilevina is sufficiently divergent from all other Rhombo¬
phryne species that it cannot be immediately assigned to
a complex or species cluster.

In addition to morphological distinctiveness, Rhombo¬
phryne nilevina is currently the southernmost distributed
species of Rhombophryne, excluding records of Rhombo¬
phryne alluaudi from the far south of Madagascar, which
are due to confusion surrounding the identity of that spe¬
cies (Scherz, Bellati, Crottini et al. unpubl data). It also
has a strongly amplitude-modulated call unlike that of
any congeners (although few call recordings are available
for this genus).

Our limited genetic data suggests that R. nilevina
may have affinities with Rhombophryne sp. Ca3 from
Tsaratanana in northern Madagascar, but we consider
this relationship tentative and ongoing multi-locus anal¬
yses suggest that R. nilevina represents a relatively ear-

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154

Lambert, S.M. et al.: A new Rhombophryne from southeastern Madagascar

ly-diverging, phylogenetically distinct species of Rhom¬
bophryne (A. Crottini, pers. comm.). Given the limited
information available at this time, the phylogenetic aflhn-
ities of R. nilevina will need to be clarified in a future
revision of the genus.

Acknowledgements

We thank the Malagasy authorities for issuing permits;
field research was conducted under permit number 303/14/
MEF/SG/DGF/DCB.SAP/SCB; specimens were exported
under 017N-EV01/MG14. We also thank MICE! and
Centre ValBio for facilitating fieldwork. Finally, SME
would like to thank Ralaivao Jean Fulgence and Emile
Rajeriarison for their exceptional work in the field during
the Andemaka expedition. If not for their dedication and
ability, R. nilevina would surely remain undiscovered.

References

Andreone F, Vences M, Vieites DR, Glaw F, Meyer A (2005) Recur¬
rent ecological adaptations revealed through a molecular analysis
of the secretive cophyline frogs of Magascar. Molecular Phyloge¬
netics and Evolution 34(2): 315-322. http://dx.doi. 0 rg/lO.lOl 6 /j.
ympev.2004.10.013

Bletz MC, Rosa GM, Andreone F, Courtois EA, Schmeller DS, Rabibisoa
NHC, Rabemananjara FCE, Raharivololoniaina E, Vences M, Wel¬
don C, Edmonds D, Raxworth CJ, Harris RN, Fisher MC, Crottini A
(2015) Widespread presence of the pathogenic fungus Batrachochy-
trium dendrobatidis in wild amphibian communities in Madagascar.
Scientific Reports 5: 8633. http://dx.doi.org/10.1038/srep08633
D’Cruze N, Kohler J, Vences M, Glaw F (2010) A new fat fossorial frog
(Microhylidae: Cophylinae: Rhombophryne) from the rainforest of
the Foret d’Ambre Special Reserve, northern Madagascar. Herpeto-
logica66(2): 182-19. http://dx.doi.Org/10.1655/09-008rl.l
Duellman WE, Trueb E (1994) Biology of Amphibians. Johns Hopkins
University Press, Eondon, U.K., 696 pp.

Emerson SB (1979) The ilio-sacral articulation in frogs: form and
function. Biological Journal of the Einnaean Society 11: 153-168.
https://doi.org/10.1111/j. 1095-8312.1979.tb00032.x
Glaw F, Vences M (2007) A Field Guide to the Amphibians and Reptiles of
Madagascar. Third Edition. Koln, Vences & Glaw Verlags GbR, 496 pp.
Glaw F, Kohler J, Vences M (2010) A new fossorial frog, genus
Rhombophryne, from Nosy Mangabe Special Reserve, Madagas¬
car. Zoosystematics and Evolution, 86(2): 235-243. http://dx.doi.
org/10.1002/zoos.201000006

Hutter CR, Guayasamin JM (2015) Cryptic diversity concealed in the
Andean cloud forests: two new species of rainfrogs (Pristimantis)
uncovered by molecular and bioacoustic data. Neotropical Biodi¬
versity 1: 36-59. https://doi.Org/10.1080/23766808.2015.1100376
Hutter CR, Eambert SM, Cobb KA, Andriampenomanana ZF, Vences
M (2015) A new species of bright-eyed treefrog (Mantellidae) from
Madagascar, with comments on call evolution and patterns of syn-
topy in the Boophis ankaratra complex. Zootaxa 4034(2): 531-555.
https://doi.org/10.11646/zootaxa.4034.3.6

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment
software version 7: improvements in performance and usability.
Molecular Biology and Evolution 30(4): 772-780. http://dx.doi.
org/10.1093/molbev/mstO 10

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S,
Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B,
Mentjies P, Drummond A (2012) Geneious Basic: an integrated and
extendable desktop software platform for the organization and anal¬
ysis of sequence data. Bioinformatics 28(12): 1647-1649. http://
dx. do i. org/10.1093/bio informatics/bts 199
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics
and evolution in R language. Bioinformatics 20(2): 289-290. http://
dx.doi.org/10.1093/bioinformatics/btg412
Perl RB, Nagy ZT, Sonet G, Glaw F, Wollenberg KC, Vences M (2014)
DNA barcoding Madagascar’s amphibian fauna. Amphibia-Reptilia,
35(2): 197-206. http://dx.doi.org/10.1163/15685381-00002942
Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia includ¬
ing over 2800 species, and a revised classification of extant frogs,
salamanders, and caecilians. Molecular Phylogenetics and Evolution
61 (2): 543-583. http://dx.doi.Org/10.1016/j.ympev.2011.06.012
R Development Core Team (2016) R: A language and environment for
statistical computing. R Foundation for Statistical Computing, Vienna,
Austria. http://www.R-project.org

Rakotoarison A, Crottini A, Muller J, Rbdel M-0, Glaw F, Vences M
(2015) Revision and phylogeny of narrow-mouthed treefrogs {Co¬
phyla) from nothern Madagscar: integration of molecular, oste-
ological, and bioacoustic data reveals three new species. Zootaxa
3937(1): 061-089. http://dx.doi.Org/10.11646/zootaxa.3937.l.3
Rosa GM, Crottini A, Noel J, Rabibisoa N, Raxworthy CJ, Andreone F
(2014) A new phytolemic species of Platypelis (Microhylidae: Co¬
phylinae) from the Betampona Reserve, eastern Madagascar. Sala-
mandra50(4): 201-214.

Ruthensteiner B, HeB M (2008) Embedding 3D models of biological
specimens in PDF publications. Microscopy Research and Tech¬
nique 71: 778-786. https://doi.org/10.1002/jemt.20618
Scherz MD, Ruthensteiner B, Vences M, Glaw F (2014) A new microhylid
frog, genus Rhombophryne, from northeastern Madagascar, and a re-de-
scription of R serratopalpebrosa using micro-computed tomography.
Zootaxa, 3860 ( 6 ): 547-560. http://dx.doi.org/10.11646/zootaxa.3860.6.3
Scherz MD, Ruthensteiner B, Vieites DR, Vences M, Glaw F (2015a)
Two new microhylid frogs of the genus Rhombophryne with super¬
ciliary spines from the Tsaratanana Massif in northern Madagascar.
Herpetologica, 71(4): 310-321. http://dx.doi.org/10.1655/HERPE-
TOEOGIC A-D-14-00048

Scherz MD, Rakotoarison A, Hawlitschek O, Vences M, Glaw F
(2015b): Reaping towards a saltatorial lifestyle? An unusually long-
legged new species of Rhombophryne (Anura, Microhylidae) from
the Sorata massif in northern Madagascar. Zoosystematics and Evo¬
lution, 91(2): 105-114. http://dx.doi.org/10.3897/zse.91.4979
Scherz MD, Vences M, Rakotoarison A, Andreone F, Kohler J, Glaw F,
Crottini A (2016a): Reconciling molecular phylogeny, morpholog¬
ical divergence and classifcation of Madagascan narrow-mouthed
frogs (Amphibia: Microhylidae). Molecular Phylogenetics and Evo¬
lution 100:372-381. http://dx.doi.Org/10.1016/j.ympev.2016.04.019
Scherz MD, Glaw F, Vences M, Andreone F, Crottini A (2016b) Two new
species of terrestrial microhylid frogs (Microhylidae: Cophylinae:
Rhombophryne) from northeastern Madagascar. Salamandra 52(2):
91-106.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 143-155

155

Scherz MD, Hawlitschek O, Andreone F, Rakotoarison A, Vences M,
Glaw F (in review) A review of the taxonomy and osteology of
the Rhombophryne serratopalpebrosa species group (Anura; Micro-
hylidae) from Madagascar, with comments on the value of volume
rendering of micro-CT data to t taxonomists. Zootaxa.

Stamatakis A (2014) RaxML version 8: a tool for phylogenetic analy¬
sis and post-analysis of large phylogenies. Bioinformatics 30 (9);
1312-1313. https://d 0 i. 0 rg/l0.1093/bioinformatics/btu033

Vences M, Glaw F, Marquez R (2006) The Calls of the Frogs of Madagascar.
3 Audio CD’s and booklet. Foneteca Zoologica, Madrid, Spain, 44 pp.

Vieites DR, Wollenberg KC, Andreone F, Kohler J, Glaw F, Vences
M (2009) Vast underestimation of Madagascar’s biodiversity evi¬
denced by an integrative amphibian inventory. Proceedings of the
National Academy of Sciences, 106(20): 8267-8272. http://dx.doi.
org/10.1073/pnas.0810821106

Wollenberg KC, Vieites DR, Van Der Meijden A, Glaw F, Canatella DC,
Vences M (2008) Patterns of endemism and species richness in Mal¬
agasy cophyline frogs support a key role of mountainous areas for
speciation. Evolution 62(8): 1890-1907. http://dx.doi.org/10.llll/
j.l558-5646.2008.00420.x

Supplementary material 1

File SI

Authors: Shea M. Lambert, Carl R. Hotter, Mark D.
Scherz

Data type: Adobe PDF file

Explanation note: This file contains a PDF-embedded in¬
teractive 3D model of the skeleton of the holotype of
Rhombophryne nilevina sp. n., KU 340897, generated
via X-ray micro-Computed Tomography. The model
can be opened in Adobe® Acrobat Pro or Reader, ver¬
sions IX and above. To activate it, click the image.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 157-166 | DOI 10.3897/zse.93.10915

4»yEnsPFr.

museum fur naturkunde

Loveridge’s Angolan geckos, Afroedura karroica bogerti
and Pachydactylus scutatus angolensis (Sauria, Gekkonidae):
new distribution records, comments on type localities
and taxonomic status

William R. Branch^-^, Wulf Haacke^, Pedro Vaz Pinto'* Werner Conradie* ®, Ninda Baptista^,
Luke Verburgt®'®, Luis Verissimo'*

1 Port Elizabeth Museum (Bayworld), P.O. Box 13147, Humewood 6013, South Africa

2 Research Associate, Department of Zoology, P.O. Box 77000, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa

3 E27 Serene Park, P.O.Box 600, Garsfontein, Pretoria 0042, South Africa

4 Fundagdo Kissama, RuaJoquim Kapango, 49 1°Luanda, Angola

5 CIBIO/InBio - Centro de Investigagdo em Biodiversidade e Recursos Geneticos, Universidade do Porto, Campus Agrdrio de Vairdo, 4485-661,
Universidade do Porto, Portugal

6 Research Associate, School of Natural Resource Management, George Campus, Nelson Mandela Metropolitan University, George, South Africa

7 Instituto Superior de Ciencias da Educagdo da Huila (ISCED), Rua Sarmento, Rodrigues, Lubango, Angola

8 Enviro-lnsight CC,132 Winterberg, Equestria Estate, Pretoria 0184, South Africa

9 Department of Zoology and Entomology, University of Pretoria, Private BagX20, Hatfield, 0028, South Africa
http://zoobank.org/B9235BB4-1615-4l8F-95CB-F5FCC2C2A976

Corresponding author: William R. Branch (williamroybranch@gmail.com)

Received 24 October 2016
Accepted 15 February 2017
Published 9 March 2017

Academic editor:

Johannes Penner

Key Words

Reptilia

cryptic diversity
mombolo
William Chapman
Angola
type locality

Abstract

In 1944 Loveridge described two new geckos from Angola, Afroedura karroica bogerti
and Pachydactylus scutatus angolensis. The descriptions of both species have vague and
confusing type localities and refinements are suggested based on early expedition reports,
historical accounts from the region, and a review of cartographic material. Numerous new
distribution records are reported for both species from expeditions undertaken from 1956-
2016 by the authors or their colleagues. The taxonomic status of both species has changed,
but new material from diverse habitats, altitudes and geological substrates indicates that
further taxonomic adjustments are likely in order to refiect additional cryptic diversity.

Resumo

Em 1944, Loveridge descreveu duas osgas novas de Angola; Afroedura karroica bogerti
e Pachydactylus scutatus angolensis. As descri^oes de ambas as especies tern locali-
dades-tipo vagas e confusas. Neste trabalho sao sugeridos mais detalhes relatives a estas
especies, com base em relatorios de expedi^oes, relates historicos da regiao e revisao
de material cartografico. Sao relatados numerosos registos novos de distribui^ao para
estas especies, com base em expedifoes levadas a cabo entre 1956 e 2016 pelos auto-
res ou colegas seus. A situagao taxonomica das duas especies alterou-se, mas material
novo proveniente de habitats, altitudes, e substrates geoldgicos diversos, indicam que
e provavel que ocorram mais ajustes taxonomicos de forma a refietir uma diversidade
criptica ainda maior.

Copyright William R. Branch etal. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

158

Branch, W.R. et al.: Loveridge’s Angolan geckos

Introduction

Studies on the herpetofauna of Angola have entered a
new phase following increased collaboration on regional
and national biodiversity surveys, multi-authored modern
taxonomic reviews, and the emergence of young Angolan
scientists (Branch 2016). Almost all recent surveys (e.g.
Huntley 2009; Brooks 2012, 2013; Ceriaco et al. 2014,
2016; Ernst et al. 2014; Huntley and Francisco 2015;
Conradie et al. 2016), have uncovered new national and
regional distribution records (Branch and McCartney
1992; Branch and Conradie 2013; Conradie and Bour-
quin 2013; Ernst et al. 2014), as well as new species of
amphibians (Conradie et al. 2012a, 2013) and reptiles
(Conradie et al. 2012b; Stanley et al. 2016). However,
problems arise when attempting to integrate these new
findings with early literature and original species descrip¬
tions. Comparison is complicated by numerous factors,
particularly the generally vague locality details for type
material in early descriptions. It is not always obvious
which localities or regions in these descriptions refer to
modem towns in different parts of the country that have
similar or identical names, and may be affected by the
variant spellings of explorers and researchers. Exacerbat¬
ing this is the loss of almost all of the material studied by
Jose Vicente Barbosa du Bocage, the father of Angolan
herpetology, in a fire that destroyed the Museu Bocage
collections in 1978. As a consequence, many type speci¬
mens are no longer available and replacement ‘topotypic’
material requires confidence in the documentation of type
localities. To illustrate these problems we consider two
recent examples, Afroedura karroica bogerti Eoveridge,
1944, and Pachydactylus scutatus angolensis Eoveridge,
1944, where knowledge of the vague type localities giv¬
en in the original description have become more defined
following recent investigation and the integration of new
and early observations. Both taxa are subsequently been
elevated to specific status (see below).

Taxonomy

Angolan Flat Gecko {Afroedura bogerti)

History. The Angolan Flat Gecko {Afroedura bogerti)
is a beautiful and zoogeographically interesting species.
For many years knowledge of the species was based on
a single specimen collected during the Vemay Angola
Expedition (VAE) in 1925. Charles Bogert, after whom
the gecko is named, was the Curator of Herpetology at
the American Museum of Natural History (AMNH), and
prepared a detailed report on the snakes collected by the
VAE (Bogert 1940). He never published on the extensive
lizard collections, but did draw Eoveridge’s attention to
a specimen that he thought might be a new species, and
for which a superb drawing had been prepared (fig. 1 in
Eoveridge 1944). Eoveridge confirmed this assessment

and described the species in Bogert’s honour. He conside¬
red it closely related to a South African species, Oedura
karroica Hewitt, 1925, but did not consider the few Af¬
rican representatives of Oedura to be congeneric with
Australian Oedura Gray, 1842, which had been based on
the Australian species Oedura marmorata Gray, 1842. He
therefore placed all African representatives of Oedura in a
new genus, Afroedura, with his new subspecies, Afroedu¬
ra karroica bogerti as the genotype.

Taxonomic status of Afroedura bogerti. Onderstall
(1984) investigated relationships hQtwQQn Afroedura spe¬
cies, and on morphological grounds recognized three spe¬
cies groups. He examined material collected by WDH in
1971 and 1974, and based on its possession of two pairs
of scansors per digit and a verticillate tail placed it in his
Aransvaalicd’ group, along with A. transvaalica (Hewitt,
1925) and A. loveridgei Broadley, 1963. His 'africana'
group, which included A. karroica, was characterized by
having three pairs of scansors per digit and a verticillate
tail, and he therefore elevated A. bogerti to a full species
(Onderstall 1984). Based on material collected in 2009
from Tambor in the Iona National Park (see below), sig¬
nificant genetic divergence of A. bogerti from all other
Afroedura (Jacobsen et al. 2014; Makhubo et al. 2015)
confirmed its specific status. However, there remains con¬
fusion over its phylogenetic relationships. Jacobsen et al.
(2014) and Makhubo et al. (2015) found that A. bogerti
was part of the A. transvaalica group, although they dif¬
fered in the latter group’s relationships to other species
groups. This association remains of zoogeographic inter¬
est as the range of A. bogerti is separated by nearly 2000
km from other members of the A. transvaalica group
(sensu Jacobsen et al. 2014). However, among Angolan
geckos it is easily recognized by its dorso-ventrally flat¬
tened body, smooth homogenous dorsal scalation, pos¬
sessing 1-2 pairs of scansors under the fourth toe, and the
verticillate tail.

Type locality of Afroedura karroica bogerti. In his de¬
scription of Afroedura k. bogerti, Eoveridge (1944) noted
that the type specimen (AMNH 47841) was an adult male
from Namba (Mombolo), Cuanza Sul Province, Angola,
collected by Harry and Allan Chapman, between Sep¬
tember and November 1925. Although the locality was
not defined in more detail by Eoveridge, Bogert (1940)
had previously given general geographical co-ordinates
for Mombolo (12°10’S, 14°50’E), but did not mention
Namba. Crawford-Cabral and Mesquitela (1989) mapped
the vertebrate collections recorded from Angola but over¬
looked Eoveridge’s (1944) two gecko descriptions. They
did record Bogert’s (1940) Mombolo (as ‘Mombola’) us¬
ing the details given in his paper, and also listed Namba
(Missao da Namba, 11°55’ S, 14°5rE), approximately
27 km north of Bogert’s Mombolo locality. It should be
noted that the geographical co-ordinates listed for both
these localities are relatively vague and provide only de¬
grees and minutes.

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159

j.riiXT!:^ ':rfTTTr:T!'rTTTTTT*^^’~ ^ . , , A ,

W' X

lit i

Titulo de Concessao i.

POR

Possmio a ‘■‘tmor lic c/a/z/cs ^

i*rofPss() i\v coiicossrio uPfOOjQ/d /fl

(IG ,. Hoar/c/a, ,. -

m%k.c7a,f,vra Jg 1930,

3'icpit p p’rdir a qiie fe rcfe.rr rls/f iituh' com c il /
po fdha n°7iii/)JP dp f.cmpaiiimmtc n" / 9 / . sccfac - ,

|jr cad^Mtc s dfjirito no Tom bo Geral da pra-

Figure 1. A; (left) Photograph of the original “Titulo de Concessao” (28 January 1930) confirming William Chapman’s ownership
of the farm that was purchased by the Kath-Brock family. B: (right) the farm map from the “Titulo de Concessao” showing ‘ Alengo
Sandula’ at middle of lower boundary.

There is no detailed history or route for the VAE, but a
brief summary of the expedition is given in the Mammals
of Angola (Hill and Carter 1941, p: 3). It records (salient
comments abstracted):

Messrs. Herbert Lang and Rudyerd Boulton, collectors,
went to Angola in April, 1925, and remained there for
about three months. Landing at Lobito, near Catumbela,
a few animals were secured here. The expedition went
to Hanha Estate (not the Hanha usually given on maps),
an oil palm plantation near the coast, some thirty-two
kilometers north of Lobito. The party then went south by
way of Huambo where they were joined by Messrs. A.

S. Vernay, Alan and Charles Chapman . At the

end of August the expedition united at Capelongo and

returned by way of Caconda to Huambo . At Huambo

the party again divided . Boulton and Charles Chap¬

man went to Namba in the Mombolo region.

The geographical locations of sites detailed in Hill
and Carter (1941) are again relatively vague: i.e. Chi-
pepe, near Cassongue (12°S, 15°E); Monte Victoria Ver¬
dun (12° OS’S, 15°E); and Namba (Mombolo) (11°35 S,
14°25’ E).

Although Eoveridge (1944) recorded that the type
specimen of A. k. bogerti was collected during the VAE,

he specifically states that it was ''collected by Harry and
Allan Chapman, between September and November,
19251' This was after the American members of the VAE
had departed. This discrepancy is probably explained by
a comment in Hill and Carter (1941, p: 5) where they note

that their mammal material included “. fifty mammals

... purchased from Mr. C. P. Chapman, collected at Chi-
pepe, Namba, and Monte Victoria Verdun!) and it is thus
possible that Eoveridge’s type specimen was obtained in
the same way.

Many of these locations are discussed in the recently
published ‘Reminiscences’ of William Chapman, the fa¬
ther of Charles, Harry and Alan Chapman (Stassen 2010).
The latter two sons (note corrected spelling of Alan, not
Allan) are the collectors of the type specimen of A. k.
bogerti (Eoveridge 1944). William Chapman was the son
of the famous South African explorer James Chapman
(Chapman 1868), and one of the original ‘Trek Boers’,
who moved away from British rule in the Cape region,
and eventually settled (1881-1928) in southern Angola.

Chapman notes "Ernst Meyer had selected a farm in
the Mombolo country at the base of a mountain range
calledNambd' (Stassen 2010, p: 295). He later comments
"The next day I crossed the Etala stream [a tributary of
the Cuchem] with my wagon and went up to the small
plain below the koppie on which I subsequently built my

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160

Branch, W.R. et al.: Loveridge’s Angolan geckos

Figure 2. The ruins of farm Monte Verde, surrounded by eucalyptus trees (middle distance), overlay those of William Chapman’s
farm Monte Victoria-Verdun. Viewed from an intrusive rock outcrop on the lower northern slopes of Sandula Hill.

house’’’ (Stassen 2010, p: 297). He called it Monte Vic¬
toria-Verdun (Stassen 2010, p: 25 notes it was originally
called Sandula, but see below).

It was noted (Stassen 2010, p: 13) that William Chapman:

. liked the company of scientific explorers and quite a

number of them were invited to stay for some time on
his farm. As a result the type specimens of quite a few
species offauna and flora were recorded at Sandula,
Namba or Chipepe, the farms of the Chapman clan
near Mombolo.

A thorough examination of official detailed cartograph¬
ic material supported by the historical accounts, allowed
us to identify the possible location of Chapman’s farm on
topographic maps as “Fazenda Monte Verde”, located on
the northeastern slopes of the Lupangue mountains, close
to the headwaters of the Etala stream, which drains be¬
tween rock outcrops from the mountain. We were able to
conhrm this following a site visit (5-6 November 2016),
and from inspection of the original “Titulo de Concessao”,
dated 28 January 1930 (Fig. lA), that conhrms the farm’s
ownership by William Chapman. The farm was purchased
by the Kath-Brock family, who renamed it as Monte
Verde. The original farm map attached to the title deed
reveals that the “koppie” (hill) noted by Chapman was
originally called Sandula (Fig. IB). The brick farm build¬
ings ofthe Brock family (12°10'09”S, 15°0F42”E, 1798m
a.s.l.) were built on, and incorporate some of, the original
Chapman house, but both are now derelict, whilst Sandula
Hill (12°1F04”S, 15°0F41”E, 2242m a.s.l) is locally now
called Monte Verde. This prominence is capped in granite
outcrops, with intrusive rock outcrops on its lower slopes
and is close to the farm site. These outcrops form suitable
habitat for flat geckos (Fig. 2).

Stassen (2010, p25) notes ""Mombolo is a small vil¬
lage on the Benguela highlands in the Cuanza Sul district
and is also called Omambolo, Nakamombolo or Maka-
mombolo'”. Although two small quimbos (villages) to the
southwest of Chapman's farm have been identified in the
cartographic material referenced as Mombolo, we con¬
sider that the name is more correctly associated with the
general region to the south of Missdo da Namba, as is
shown in the Carta de Angola at the scale of 1/100 000,
where the area immediately to the south of Missao da
Namba is named Mombolo. This is an extensive grassy
area named as the Anhara do Mombolo, and at the south¬
ern edge of which lies the present town of Maka-Mom-
bolo (12°1F54”S, 14°52'06”E, 1760m asl) mentioned
by Stassen (2010, p25). Eocal people refer to extensive
flat natural grasslands as ‘mombolos’, areas suitable for
planting staple crops. Missao da Namba is a Seventh-day
Adventist church established by James Delmes Baker,
who settled in the area in November 1928 (Anon, 2017).

The Eynes-Vincent bird expedition (1930-31) was a
specialist trip for Cisticola species in Central and West
Africa (Eynes and Sclater 1933, 1934). On 1 March 1931
the expedition visited “Chipepe (Mombolo loc. 5900ft)”,
identified in the official topographic maps as Fazenda
Quipepe (11°59'30”S, 14°56'10”E), having driven 140
miles from Huambo, via Bailundo. The expedition then
spent 2-8 March 1931 at “Namba (nr. Chipepe) 5700 ft.
to 6700ft.”, where they were assisted by “Herr Koster”
(probably Paul Friedrich Heinrich Koster who married
William Chapman’s daughter Sarah, and who remained
in the Mombolo region after the ‘Trek Boers’ moved to
Namibia in 1928; Stassen 2010).

Although our studies and site visits give greater detail
to the probable origin of the type specimen of A. k. bo-
gerti, the exact location of its capture remains unknown.

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161

12®E 16®E

Figure 3. Geographical distribution of Afroedura bogerti. Insert (left) shows the polygon that encompasses the area from which the
type specimen was collected. The problematic Namibian specimen is included.

and cannot be determined with greater accuracy based on
existing knowledge. We conclude that the vague type lo¬
cality, i.e. “Namba (Mombolo)” refers to a general area
that probably corresponds to a polygon that can be de¬
limited by the points (detailed above) of William Chap¬
man’s farm (Monte Victoria-Verdun, later Monte Verde),
Chipepe/Quipepe, the farm of one of his sons, Missao da
Namba, and Maka-Mombolo (Fig 3.). This is also adja¬
cent to Mombolo (Missao da Namba, AO018, 11°55’S,
14°51 ’E), an Important Bird Area for the conservation of
a number of Angolan birds (Birdlife 2016).

New distribution records for Afroedura bogerti. Fol¬
lowing its discovery in 1925 the next specimen of this spe¬
cies was collected by Dr C. Koch on a Transvaal Museum
Expedition to southwest Angola in September 1956. Col¬
lected near Caraculo (15°01'36.7”S, 12°39'07.57”E), this
specimen (TM 24545) was not mentioned by FitzSimons
(1959) in his description of new reptiles (e.g. Pachydac-
tylus caracuUcus and Prosymna visseri) collected during

Koch’s expedition. It did, however, direct subsequent
searches when one of us (WDH) visited Angola (1971
and 1974) to specifically search for geckos of the genera
Pachydactylus, Rhoptropus and Afroedura. These sur¬
veys obtained significant new A. bogerti material from
various localities, including: TM 40263-68, 40279-95
(23 specimens), Caraculo, Namibe Province, 27 March
1971; TM 40508-20 (13 specimens), Tambor, Namibe
Province, Angola (16°04'00.1"S, 12°26'59.9"E), 1 April
1971; TM 40536-37 (two specimens) Furnas (? - plot¬
ted as nearest rock outcrops to centre of quarter-degree
square (QDS) 1612Ab in original field notes), Namibe
Province (1612Ab, 16°23'30.0"S, 12°08'30.0"E), 1 April
1971; TM 41132^4 (13 specimens), turn off to Morro
do Chapeu Armado, Namibe Province (14°31'42.8"S,
12°30'06.8''E), 18 April 1971; TM 41211-16 (six spec¬
imens), Eucira road, 5 km south of Catara River, Na¬
mibe Province (13°36'15.5'’S, 12°38'44.0"E), 19 April
1971; TM 45366-68 (3 specimens), 10 km west of So-
que, Huambo Province (12°21'45.2"S, 15°01'42.5"E), 10

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Branch, W.R. et al.: Loveridge’s Angolan geckos

Figure 4. Regional variation in colouration and habitus of Afroedura bogerti from Angola A Omauha Lodge, Namibe Province
B 52 km N Caraculo, Namibe Province C Praia do Meva, Benguela Province (P Vaz Pinto). D Candumbo Rocks, Huambo Province
(L Verburgt). All photos by WR Branch, except where noted.

May 1974; TM 45374, 1 km south Luimbale, Huambo
Province (12°15'13.3"S, 15°19'00.8"E), 10 May 1974;
TM 45381-98 (18 specimens), Candumbo Rocks, 16
km west of Vila Nova, Huambo Province (12°44'09.6"S,
15°58'27.8"E), 11 May 1974; TM 46587-90 (four
specimens), 3 km west of Bocoio, Benguela Province
(12°28'58.0"S, 14°06'24.8"E), 28 May 1974; TM 46631-
34 (four specimens), Numba (= Namba), on track from
Atome to Cassongue (vicinity of Missao da Namba),
Cuanza Sul Province (11°55'01.9"S, 14°5r39.1"E), 29
May 1974.

Following a hiatus in field surveys to Angola during the
protracted civil war (1975-2002), no additional material
was added until international collaborative biodiversity
surveys began in 2009. During the first of these (Huntley
2009) additional material was collected: PEM R17936-37
(two specimens), Omauha Eodge, 15 km south of Tambor,
Namibe Province (16°12'02.2”S, 12°24'06.6”E, 341m),
18 January 2009; PEM R18041^2 (two specimens),
CAS 248780-81 (two specimens donated by PEM), 0.5
km south of Tambor, Namibe Province (16°04'26.9”S,
12°25'59.8”E, 352m), 21 January 2009. Subsequent field
work in the ProNamib region north of Namibe (2012,
2015) and in the Huambo region (2016) resulted in addi¬
tional material from new localities: PEM R21595, Granite
outcrops in sandy veld, 50 km E Namibe on main tar road
to Eeba, Namibe Province (15°00'56.1”S, 12°33T8.1”E,
516m a.s.L), 8 December 2012; PEM R21596, small gran¬
ite outcrops in succulent veld, 52 km N on tar road on road
to Eucira from junction with Eubango-Namibe road, Na¬
mibe Province (14°39'29.0”S, 12°3r37.8”E, 586m a.s.L);

AG 137-41 (to be accessioned into PEM collection), 5
specimens, 1 km east of Farm Mucongo, Namibe Province
( 14047 'Or’S, 12°29'49”E, 314m a.s.L), 7 November 2015;
PEM R22488-89,2 specimens, Praia do Meva (near Santa
Maria), Benguela Province (13°23'48”S, 12°35'23”E, 10m
a.s.L), 28 December 2015; PEM R22490-91,2 specimens,
1 km west Kandumbo on road to Boas Aguas, Huambo
Province (12°44T0.1”S, 15°58'27.9”E, 1777m a.s.L), 11
March 2016.

Currently Angolan Afroedura bogerti is known from
approximately 15 localities that appear to fall into dis¬
junct populations occurring above and below the Great
Escarpment, and in diverse habitats and on different ge¬
ological substrates. Colouration and scalation varies be¬
tween the known populations of A. bogerti (Fig. 4) and
preliminary morphological and genetic analysis corrobo¬
rates the existence of cryptic diversity within the species
(Branch et al. 2017). Molecular sequences forH. bogerti
incorporated into recent phylogenies of the genus were
based on tissues collected from lowland populations
within the Angolan Namib region (Jacobsen et al. 2014,
Tambor CAS 248780-81; Makhubo et al. 2015, Omau¬
ha Eodge, PEM R17936-37). A fiat gecko, referred to as
Afroedura cf. bogerti, was discovered in a rock crevice
on the summit of the Otjihipa Mountains, northern Opu-
wo District, Namibia (approx. 17°18T8”S, 12°36'35”E,
1170m) in 1992 (Branch 1998; Griffin 2003). However,
no voucher material is available in the State Museum,
Windhoek (A.M. Bauer, pers. comm. May 2016), and the
taxonomic status of the Namibian population cannot be
assessed until further material becomes available.

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163

12‘>E

14°E

16°E

12®S

14°S

16®S

Legend

• Pachydactylus scutatus

• Pachydactylus angolensis i8®s
lI.T] Provincial Boundaries

Altitude

100 m
500 m
900 m
1300 m
1700 m

20°S

Figure 5. Distribution of Pachydactylus angolensis and Pachydactylus scutatus in Angola. Stars = type localities. For additional
Namibian localities for P. scutatus, see Bauer et al. (2002).

Angolan Thick-toed Gecko {Pachydactylus angolensis)

History. In the same paper in which he described
ura k. bogerti, Loveridge also described the small terres¬
trial gecko Pachydactylus scutatus angolensis Loveridge,
1944. Loveridge’s (1944) description was based on three
specimens. The holotype (AMNH 47874) was “an adult
male from Hanha, Benguela Province, Angola, collected
by Arthur Vernay, Herbert Lang and Rudyerd Boulton,
May 17, 1925”. One of the two paratypes was also col¬
lected at the type locality but on 13 May 1925, and the
other collected earlier “from Lobito Bay, Angola ... by
Herbert Lang, April 24, 1925”. These dates, unlike those
for A. bogerti, indicate that the geckos were actually col¬
lected during the VAE.

Taxonomic statns of Pachydactylus angolensis. Bauer
et al. (2002), in a review of Namibian P. scutatus Hewitt,
1927 (including the description of P. parascutatus Bauer,
Lamb and Branch, 2002), elevated P. angolensis to a full
species, noting the consistent nasal arrangement. A recent
molecular phylogeny of the genus Pachydactylus (Heinicke
et al. 2017) confirms the specific status of P. angolensis, but
reveals its sister relationship to P. cariculicus not P. scuta¬
tus. With the elevation of P. angolensis to specific status, P.
scutatus was considered to be restricted to Namibia north of
the Brandberg. However, WDH (unpubl.) had already col¬
lected the first Angolan P. scutatus from Iona National Park
(TM 40751), and others from Espinheira (TM 40615-18),
when he visited the region in April 1971. Recent material
from the latter locality has also been reported by Cerlaco et

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Branch, W.R. et al.: Loveridge’s Angolan geckos

Figure 6. Regional variation in colouration of Pachydactylus angolensis from Angola. A P. angolensis - inland form (Serra da Tchi-
vira: photo P Vaz Pinto) B P. angolensis - coastal form (Chimalavera Regional Natural Park: photo WR Branch).

al. (2016). The TM geckos from Iona and Espinheira have
the characteristic narrow and dark-edged white nape band
illustrated in Boone and Barts (2006) which is not evident
in P. angolensis or mentioned in its description (Loveridge
1944). Thick-toed geckos {Pachydactylus) are poorly repre¬
sented in Angola, with only seven currently recognized spe¬
cies recorded; P. cariculicus, P. scutatus, P. angolensis, P
punctatus, P oreophilus, P rangei and P. vanzyli. This con¬
trasts dramatically with Pachydactylus diversity in Namibia
(38 species) and South Africa (30 species). Pachydactylus
angolensis can be distinguished from most Angolan Pachy¬
dactylus (e.g. P. cariculicus, P punctatus, P rangei and P.
vanzyli) by its keeled dorsal scalation, from P. oreophilus
by its smaller size, and from P. scutatus by lacking a dark-
edged white nape band and by the exclusion of the first up¬
per labial and rostral from the nostril {P. scutatus has a well
developed nape band, and both the first upper labial and
rostral enter the nostril).

Type locality of Pachydactylus scutatus angolensis.
Angolan localities referenced under the toponym “Hanha”
may cause confusion. Two main places are of concern,
and both are situated in Benguela Province: Hanha do
Norte (also Hanha Estate) and Hanha do Cubal. Bauer
et al. (2002) noted that the holotype was “.. collected at
Hanha (probably Hanha do Norte in quarter degree square
1213Bc; another locality, Hanha do Cubal, 1314Aa is also
in the same province)”. The above assumption is here ac¬
cepted, insomuch as it avoided confusion between the two
localities, and furthermore is corroborated by the fact that
Hill and Carter (1941) had earlier noted that the VAE did
not visit Hanha do Cubal, but rather the Hanha Estate oil
palm plantation. Unfortunately, although the geographic
description of Hill and Carter (1941) is basically correct,
the co-ordinates they give (13°30’ S, 14°30’ E) are incor¬
rect and refer to another Hanha toponym that lies south¬
east of the estate. It is indicated on a 1934 map of the re¬
gion, and is now known as Cambondongolo (13°2rO”S,
14°24'0”E). To avoid further confusion we recommend
that the type locality for Pachydactylus scutatus ango¬
lensis Eoveridge, 1944 be restricted to - Hanha do Norte
(12°14'42”S, 13°42'27”E), approximately 20 km north¬
east of Eobito, Benguela Province, Angola. This site is
illustrated in fig. 1 of Hill and Carter (1941).

New distribution records for Pachydactylus angolen¬
sis. Pachydactylus angolensis remains poorly-known
from Angola. Additional material (Eaurent 1964) was
collected soon after the original description, and other
specimens were collected from various localities in Na-
mibe Province by Koch during his expedition in Sep¬
tember 1956 (see above), including: Eungo (TM 24406),
Eucira (TM 24445, 24449) and Bentiaba (TM 25454-55,
25459, 25476, 25478-79). These discoveries, and others
from 24 km south of Benguela (TM 39110-11), stimu¬
lated WDH to collect more material in 1971 from Saco
do Giraul (TM 40328-29), Eucira (TM 41172), 30 km
north Dombe Grande (TM 41266), and in 1974 from
Hanha (TM 46558). More recently Cerlaco et al. (2016)
recorded a specimen from the Namibe-Eubango road,
near Mangueiras (15°2'37”S, 13°9'36”E).

Recent collections of geckos currently attributed to P.
angolensis are grouped into coastal and inland popula¬
tions (Fig. 5), with coastal populations (<300m a.s.l.) usu¬
ally associated with consolidated marine deposits, while
inland populations (>600m a.s.l.) are found in granite or
intrusive outcrops. Preliminary morphological investiga¬
tion indicates variation in dorsal colouration and habitus
(Fig. 6) between these populations that are indicative of
further cryptic diversity in Angolan geckos, and will be
investigated with integrative morphological and genetic
studies (Branch in prep.).

Acknowledgements

We thank: Brian Huntley, Joao Serodio d’Almeida, and
the Traguedo family for organising the SANBI/ISCED/
UAN 2009 Angolan Biodiversity Assessment Capacity
Building Project; and Steve Boyes and John Hilton of the
Wild Bird Trust, administers of the National Geograph¬
ic Okavango Wilderness Project (National Geographic
Society grant number EC0715-15) during which WRB,
WC, NB, WRB, WC, NB and PVP participated in the
biodiversity surveys of the headwaters of the Cuito and
Cuanavale Rivers (2015-2016). Mr Werner Kath-Brock
(Euanda) generously allowed us to inspect the original
“Titulo de Concessao” (28 January 1930) transferring
William Chapman’s farm to his grandparents.

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Zoosyst. Evol. 93 (1) 2017, 157-166

165

References

Anon (2017) Histori dos Adventista de Angola. http;//adventistadema-
lanje.blogs.sapo.pt/299.htmll [accessed 12 December 2016]

Bauer AM, Lamb T, Branch WR (2002) A revision of Pachydactylus
scutatus (Reptilia: Squamata: Gekkonidae) with the description of a
new species from northern Namibia. Proceedings of the California
Academy Sciences 53(3): 23-36.

BirdLife International (2016) Important Bird and Biodiversity Area
factsheet: Mombolo (Missao da Namba). http://www.birdlife.org
[on 23/04/2016]

Bogert CM (1940) Herpetological Results of the Vemay Angola expe¬
dition. Bulletin American Museum of Natural History 77: 1-107.

Boone J, Barts M (2006) Die Dickfingergeckos des stidlichen Afri-
kas. Teil VI: Freilandbeobachtungen und Terrarien-Nachzucht des
Rauhschuppen-Dickfingergeckos Pachydactylus scutatus HEWITT,
1927. Sauria Berlin 28(2): 45-51.

Branch WR (1998) Field Guide to the Snakes and other Reptiles of
Southern Africa. Ralph Curtis Publishing, Cape Town, 368 pp.

Branch WR (2016) Preface Amphibian and Reptile Conservation Spe¬
cial Angola-Africa issue. Amphibian and Reptile Conservation.
10(2): 1-3.

Branch WR, Conradie W (2013) Geographical Distribution: Naja (Bou-
lengerina) annulata annulata Bucholtz & Peters, 1876 Banded Water
Cobra. African Herp News 59: 51-54.

Branch WR, McCartney CJ (1992) A report on a small collection of
reptiles from southern Angola. Journal of the Herpetological Asso¬
ciation of Africa 41: 1-3.

Branch WR, Vaz Pinto P, Verburgt L, Schmitz A (2017) Cryptic Diversi¬
ty within Angolan bogerti Loveridge, 1944. Herpetologi¬

cal Association Africa 13* Conference, [poster abst.]

Brooks C (2012) Biodiversity Survey of the upper Angolan Catch¬
ment of the Cubango-Okavango River Basin. USAid, Southern
Africa, 151 pp.

Brooks C (2013) Trip Report: Aquatic Biodiversity Survey of the low¬
er Cuito and Cuando river systems in Angola. USAid, Southern
Africa, 43 pp.

Ceriaco LMP, Bauer AM, Blackburn DC, Lavres ACFC (2014) The
herpetofauna of the Capanda Dam region, Malanje, Angola. Herpe¬
tological Review 45(4):667-674.

Ceriaco LMP, de Sa SAC, Bandeira S, Valerio H, Stanley EL, Kuhn
AL, Marques MP, Vindum JV, Blackburn DC, Bauer AM (2016)
Herpetological Survey of Iona National Park and Namibe Regional
Natural Park, with a Synoptic list of the Amphibians and Reptiles of
Namibe Province, Southwestern Angola. Proceedings of the Califor¬
nia Academy Sciences 63(2): 15-61.

Chapman, J (1868) Travels in the interior of South Africa, comprising
fifteen years’ hunting and trading; with Journeys across the continent
from Natal to Walvis Bay, and visits to Lake Ngami and the Victoria
Falls. Bell and Daldy, London, 500 pp.

Conradie W, Branch WR, Measey JG, Tolley KA (2012a) A new spe¬
cies of Hyperolius Rapp, 1842 (Anura: Hyperoliidae) from the Serra
da Chela mountains, south-western Angola. Zootaxa 3269: 1-17.
https://doi.Org/10.1080/21564574.2012.676079

Conradie W, Measey JG, Branch WR, Tolley KA (2012b) Revised phy-
logeny of African sand lizards (Pedioplanis), with the description

of two new species from south-eastern Angola. African Journal of
Herpetology 61(2):91-112.

Conradie W, Bourquin S (2013) Geographical Distributions: Acontias
kgalagadi kgalagadi (Lamb, Biswas and Bauer, 2010). African Herp
News 60: 29-30. https://doi.Org/10.11646/zootaxa.3635.3.l

Conradie W, Branch WR, Tolley KA (2013) Fifty Shades of Grey: giv¬
ing colour to the poorly known Angolan Ash reed frog (Hyperolii¬
dae: Hyperolius cinereus), with the description of a new species.
Zootaxa 3635(3): 201-223.

Conradie W, Bills R, Branch WR (2016) The herpetofauna of the Cu¬
bango, Cuito and lower Cuando river catchments of south-eastern
Angola. Amphibian and Reptile Conservation Special Issue, Angola
and Africa 10(2): 6-36.

Crawford-Cabral J, Mesquite la LM (1989) Indice Toponimico de Col-
heitas Zoologicas em Angola. Instituto de Investigapao Cientifica
Tropical, Centro de Zoologia, Lisbon, 206 pp.

Ernst R, Nienguesso ABT, Lautenschlager T, Bare] MF, Schmitz A,
Holting M (2014) Relicts of a forested past: Southernmost distri¬
bution of the hairy frog genus Trichobatrachus Boulenger, 1900
(Anura: Arthroleptidae) in the Serra do Pingano region of Angola
with comments on its taxonomic status. Zootaxa 3779(2): 297-300.

FitzSimons VF (1959) Some new reptiles from southern Africa and
southern Angola. Annals of the Transvaal Museum 23: 405-409.

Griffin M (2003) Annotated Checklist and Provisional National Con¬
servation Status of Namibian Reptiles. Namibia Scientific Society,
Windhoek, 169 pp.

Heinicke, MP, Jackman, TR, Bauer AM (2017) The measure of success:
geographic isolation promotes diversification in Pachydactylus geckos.
BMC Evolutionary Biology 17(9): 1-17.

Hill ER, Carter TD (1941) The Mammals of Angola, Africa. Bulletin
American Museum of Natural History 78(1): 1-211.

Huntley B (2009) SANBI/ISCED/UAN Angolan Biodiversity Assess¬
ment and Capacity Building Project, Report on Pilot Project. South
African National Biodiversity Institute, Unpublished Report.

Huntley B, Francisco P (Eds) (2015) Avaliapao Rapida da Biodiversi-
dade da Regiao da Lagoa Carumbo. Relatorio sobre a expedi^ao. -
Rapid Biodiversity Assessment of the Carumbo Lagoon area, Lunda
Norte, Angola. Expedition Report. Republica de Angola Ministerio
do Ambiente, Luanda, 219 pp.

Jacobsen NHG, Kuhn AL, Jackman TR, Bauer AM (2014) A phy¬
logenetic analysis of the southern African gecko genus Afroedura
Loveridge (Squamata: Gekkonidae), with the description of nine
new species from Limpopo and Mpumalanga provinces of South
Africa. Zootaxa 3846(4): 451-501. https://doi.org/10.11646/zoota-
xa.3846.4.1

Laurent RF (1964) Reptiles et Amphibiens de FAngola (Troisieme
contribution). Publicapoes culturais da Companhia de Diamantes de
Angola 67: 11-165.

Loveridge A (1944) New geckos of the genera Afroedura, new genus,
and Pachydactylus from Angola. American Museum Novitates
1254:1-4.

Lynes H, Sclater WL (1933) Lynes-Vincent tour in Central and West
Africa in 1930-1931. Parti. Ibis 13(3): 694-729.

Lynes H, Sclater WL (1934) Lynes-Vincent tour in Central and West
Africa in 1930-1931. Part II. Ibis 13(4): 1-51.

Makhubo BG, Tolley KT, Bates MF (2015) Molecular phylogeny of
the Afroedura nivaria (Reptilia: Gekkonidae) species complex

zse.pensoft.net

166

Branch, W.R. et al.: Loveridge’s Angolan geckos

in South Africa provides insight on cryptic speciation. Molecular
Phylogenetics and Evolution 82: 31-42. https://doi. 0 rg/lO.lOl 6 /j.
ympev.2014.09.025

Onderstall D (1984) Descriptions of two new subspecies of Afroedura
pondolia (Hewitt) and a discussion of species groups within the ge¬
nus (Reptilia: Gekkonidae). Annals of the Transvaal Museum 33(30):
497-509.

Stanley EL, Ceriaco, LMP, Bandeira S, Valerio H, Bates ME, Branch
WR (2016) A review of Cordyliis machadoi (Squamata: Cordyli-
dae) in southwestern Angola, with the description of a new species
from the Pro-Namib desert. Zootaxa 4061(3): 201-226. https://doi.
org/10.11646/zootaxa.4061.3.1

Stassen N (2010) William Chapman Reminiscences. Protea Book
House, Pretoria, 476 pp.

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 167-187 | DOI 10.3897/zse.93.11602

4>yEnsPFr.

museum fur naturkunde

A new genus of Parastenoearididae (Copepoda, Harpaetieoida) from
the Tocantin s River basin (Goias, Brazil), and a phylogenetic
analysis of the Parastenocaridinae

Paulo H.C. Corgosinho\ Nikolaos V. Schizas^, Daniel PreviattellF, Carlos E. Falavigna da Rocha^,
Edinaldo Nelson dos Santos-Silva'^

1 Guest Researcher at the Department of General Biology, UNIMONTES, Montes Claros, Brazil

2 Department of Marine Sciences, University of Puerto Rico at Mayagiiez, Call Box 9000, Mayaguez, 00681, Puerto Rico, USA

3 Department of Zoology, Instituto de Biociencias, University ofSao Paulo, Sao Paulo, Brazil

4 Plankton Laboratory, CBIO/INPA, Av. Andre Araujo, 2936 Petrdpolis, CP 478, 69011970, Manaus-AM, Brazil

http://zoobank. org/8F621641-4E8D-4D91-825D-81734B42BCEC
Corresponding author; Paulo H. C. Corgosinho (pcorgo@gmail.com)

Received 25 December 2016
Accepted 26 February 2017
Published 10 March 2017

Academic editor;

Michael Ohl

Key Words

biodiversity

Brazilian rocky savannas

Crustacea

neotropics

new species

phylogeny

Abstract

Eirinicaris antonioi gen. et sp. n. (Parastenocaridinae) is described from the Brazilian
rocky savannas, an ecosystem under heavy anthropogenic pressure. The subfamily is
distributed worldwide, with representatives in Africa, Asia, Australia, Europe, and North
America. This is the first time a non-Remaneicaris Parastenocaridinae is described from
a Neotropical region indicating that Parastenocaridinae species were already present in
a vast geographical area, before the split of the Gondwana. The new taxon is included
within the subfamily Parastenocaridinae based on the following characters: 1) segments
5, 6, and 7 of the male antennules forming a functional unit for clasping the female; 2)
segment 7 with small process at the inner margin, forming an incipient “pocket-knife”
structure with segment 6; 3) last segment pointing medially when closed; 4) the endopod
of female leg 3 one-segmented and spiniform, without distal seta; 5) the apophysis and
terminal seta of the exopod of male leg 3 are fused; 6) the genital field is rectangular
and much broader than the height in the female; 7) the group of three lateral setae I, II,
and III of the furca and the dorsal seta are situated at the same level in the female; and
8) the basis of leg 1 has an inner seta. The new taxon can be distinguished from all other
Parastenocaridinae genera by the unique sexually dimorphic telson and furca. In the male,
the dorsal seta is inserted at the midlength of the furca and setae I, II, and III are displaced
anteroventrally. A phylogenetic analysis of the subfamily Parastenocaridinae is given
based on the description of the type species of each genus and available descriptions of
all Parastenocaridinae species. Eirinicaris gen. n. is the sister taxon of a clade formed by
Kinnecaris and Monodicaris, sharing with them the long male and female leg 5 with a
long spiniform process, and with Kinnecaris, a distal pore on the spiniform process.

Introduction

Copepods of the family Parastenoearididae Chappuis,
1940, are typical representatives of fresh groundwater
meiofauna (Corgosinho and Martinez Arbizu 2005). They
can be found in different microbiotopes such as the hy-
porheic zone of alluvial aquifers along rivers, lakes and
human-made structures such as dug or artesian wells, as

well as associated with mosses and other semi-terrestrial
environments such as phytotelmata (Menzel 1916, Chap¬
puis 1931, Joeque et al. 2013).

The taxonomy and phylogenetic relationships among
the species of Parastenoearididae are far from resolved
with many genera being potentially paraphyletic or poly-
phyletic. Most of the confusion can be attributed to Ja-
kobi (1972) who divided the family into 26 genera using

Copyright Paulo H.C. Corgosinho et al. This is an open access articie distributed under the terms of the Creative Commons Attribution License (CC BY 4.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the originai author and source are credited.

168

Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

a very unorthodox model and was strongly criticized by
Schminke 1976. Consequently, the use of Jakobi’s (1972)
generic names (i.e. Michelicaris Jakobi, 1972; Stammeri-
caris Jakobi, 1972; Minutacaris Jakobi, 1972; Nanacaris
Jakobi, 1972; Clujensicaris Jakobi, 1972; Phreaticaris
Jakobi, 1972; Pannonicaris Jakobi, 1972; Proserpinicar-
is Jakobi, 1972; Italicocaris Jakobi, 1972; Fontinalicaris
Jakobi, 1972; Entzicaris Jakobi, 1972; Lacustricaris Ja¬
kobi, \912, Nipponicaris 1972; Oshimaensicaris

Jakobi, 1972; Biwaecaris Jakobi, 1972; EnckelUcaris Ja¬
kobi, 1972; Brinckicaris Jakobi, 1972; Kinnecaris Jako¬
bi, 1972; Cafferocaris idkohi, \912, Macacocaris idkobi,
1972; Remaneicaris Jakobi, 1972; Brasilibathynellocaris
Jakobi, 1972; Pararemaneicaris Jakobi, 1972; and Sioli-
caris Jakobi, 1972) was avoided and all species were in¬
cluded in the genus Parastenocaris Kessler, 1913, until
Corgosinho and Martinez Arbizu (2005) redefined the ge¬
nus Remaneicaris, highlighting the validity of all genera
defined by Jakobi (1972). It is important to note the sem¬
inal work of Reid (1995), who redescribed Parastenoca¬
ris brevipes Kessler, 1913, and redefined Lang’s (1948)
P. brevipes-group, calling for a resolution of the taxon¬
omy within the Parastenocarididae. Recently, Schminke
(2010) shed more light on this subject and divided the
family into two monophyletic subfamilies, Parastenocari-
dinae Chappuis, 1940, and Fontinilicaridinae Schminke,
2010, both well-defined by strong synapomorphies (Ran-
ga Reddy et al. 2014).

Many genera were revised or proposed recently (viz.
Cottarelli et al. 2010, Corgosinho et al. 2008, 2010a,
2012a, b, Karanovic and Cooper 2011, Karanovic et al.
2012, Schminke 2008, 2009, 2013, Ranga Reddy et al.
2014, 2016). Most of these contributions addressed some
taxonomic uncertainties in Parastenocarididae by defining
real monophyletic groups with clear geographical distri¬
butions. With exception of the monospecific genus Itico-
caris Corgosinho, Martinez Arbizu & Previattelli, 2012,
and the genus Brasilibathynellocaris from the neotropics,
the remaining genera proposed or revalidated recently (i.e.
Stammericaris, Kinnecaris, Siolicaris, Proserpinicaris,
Remaneicaris, Monodicaris Schminke, 2009; Asiacaris
Cottarelli et al., 2010; Dussartstenocaris Karanovic &
Cooper, 2011; Horstkurtcaris Karanovic & Lee, 2012;
Cottarellicaris Schminke, 2013; Himalayacaris Ranga
Reddy, Totakura & Corgosinho, 2014; Indocaris Ranga
Reddy, Totakura & Shaik, 2016), have European, Asian,
African and Australian representatives.

The Neotropical fauna of Parastenocarididae is repre¬
sented by the genera Remaneicaris, Murunducaris Reid,
1994, Brasilibathynellocaris, Siolicaris, Iticocaris, Forfi-
catocaris idkobi, 1972, md PotamocarisT>\xssdirt, 1979.
With the exception of Remaneicaris, all the remaining
genera belong to the subfamily Fontinalicaridinae.

In order to improve our knowledge on the biodiversi¬
ty of Brazil, the National Council of Scientific Research
(CNPq) launched in 2010 a call for proposals, to assess
the biodiversity of neglected taxonomic groups in un¬
derstudied Brazilian ecosystems. Our project focused on

the microcrustaceans from the Brazilian rocky savannas.
These environments fall into the category of azonal bi-
omes (Walter 1985), which during the Pleistocene, ex¬
tended to the lowlands of what today is occupied by the
savanna ecosystems of Cerrado and Caatinga. Nowadays
they appear as insular ecosystems at the top of hills, 800
m MSL (above the sea level). This biome is under high
anthropogenic threat (Da Silva and Bates 2009) and is the
source of headwaters of important Brazilian rivers such
as Sao Francisco, Paraguay, Parana and Tocantins, con¬
necting biogeographical zones and biomes to the north,
south and east of South America.

This contribution describes one of the several new spe¬
cies and genera discovered during an intensive sampling
effort conducted in 12 rocky fields in the Brazilian inland.
A non-Remaneicaris Parastenocaridinae is described from
a Neotropical region for the first time and its phylogenetic
position within the Parastenocaridinae is discussed.

Material and methods

Specimens of an undescribed taxon were found associat¬
ed with moss in the littoral zone of the Agua Fria River,
tributary of the Sao Bartolomeu River, Tocantins hydro-
graphic basin, 1230 m MSL. The sampling station, char¬
acterized by a rocky riverbed, is located at Chapada dos
Veadeiros, Alto Paraiso de Goias, Goias State, Brazil:
14°5’30.89”S, 47°29’34.47”W(Fig. 1).

Samples of damp moss living next to the waterline
were collected on August 12, 2012. The material was
concentrated using a 50 pm mesh size net and preserved
in 4% formalin. Animals were stained with rose Bengal
and sorted with a stereomicroscope. Whole specimens
and dissected material were mounted on slides in lactic
acid for morphological inspection.

The terms ‘furca’ and ‘telson’ are used according to
Schminke (1976). Terminology and homologization
of maxillary and maxillipedal structures follow Ferrari
and Ivanenko (2008). Therefore, by the application of
serial homology, the nomenclature of Huys and Box-
shall (1991) for Mx2 (Fig. 1.5.5, p. 26) is modified as
follows: praecoxa of Mx2 is hereafter recognized as
syncoxa (praecoxa and coxa), coxa is considered as the
basis, and the basis is recognized as the first endopodal
segment with claw. Drawings were made using an Olym¬
pus BX51 microscope equipped with a drawing tube, at
a magnification of 400x and lOOOx. Abbreviations: Al
(antennule); A2 (antenna); Md (mandible); Mxl (maxillu-
la); Mx (maxilla); Mxp (maxilliped); enp (endopod); exp
(exopod); benp (baseoendopod); PI to P5 (legs 1 to 5);
ap (apomorphy); pi (plesiomorphy); Urs (urosomite). The
type material has been deposited in the invertebrate col¬
lection of the Museu de Zoologia da Universidade de Sao
Paulo - MZUSP, Sao Paulo, Brazil. Specimens of both
sexes were prepared for scanning electron microscopy
(SEM) following protocols by Felgenhauer (1987), and
Huys and Boxshall (1991).

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Zoosyst. Evol. 93 (1) 2017, 167-187

169

Figure 1. Study area. Type locality indicated with triangle. Insert shows the type locality (Agua Fria River, National Park of the
Chapada dos Veadeiros, Brazil) of Eirinicaris antonioi sp. n.

In order to determine the position of the new genus
within Parastenocarididae, the method of phylogenetic
systematics of Hennig (1966) was followed. The clado-
gram (Fig. 9) was generated using the program NONA
(Goloboff 1999) for cladistic parsimony in interface with
WINCLADA (Nixon 2002). This program uses a heu¬
ristic algorithm with unconstrained search and multiple
TBR + TBR (searches for trees using tree bisection-re¬
connection method of branch-swapping, then repeats this
process the number of times as indicated in the number
of replications box) as search strategy for the best topol¬
ogy, and a Wagner algorithm that supports character re¬
versal (allows 0 ^ n and n ^ 0 character changes) as
a “similarity” algorithm. Character states are coded as
binary (0-1) or multistate (0-n). We allowed the software
to run characters as additive (0 1 2 = 2 steps; 0

<-^2 = 2 steps). The state for each character can be seen
in the character list. The data matrix is given in Table 1.
The polarisation of characters was done a priori (zero
(0) represents the plesiomorphic condition, one (1) the
apomorphic condition, and one (1) is plesiomorphic in
comparison with two (2)) as in the ground pattern char¬
acters for Parastenocarididae (Corgosinho et al. 2007a),
Parastenocaridinae and Fontinalicaridinae (Schminke
2010). Additional decisions of character polarity were
obtained by comparing the Parastenocarididae ground
pattern with the state of character present in Psammoni-
tocrella Rouch, 1992, and other Ameiridae. The resulting
cladogram is rooted. The term “ground pattern” is used
here in the sense of ‘Grundmuster’ (Ax 1984: 156) and
refers to all plesiomorphies and autapomorphies present
in each taxon (‘StammarF sensu Ax 1984). Uninforma¬
tive characters were not mapped. Unsupported nodes in
the tree are hard collapsed. Characters are ACCTRAN
(fast) optimized.

The phylogenetic analysis is based on data from pub¬
lished literature. All the original descriptions and the de¬
scriptions of the species included in Lang’s (1948) groups
and Jakobi’s (1972) genera of Parastenocaridinae were
studied. The observation of the state of characters on out¬
groups and on the remaining species included within the
Parastenocaridinae by Schminke (2010), which are not
mentioned by Lang (1948) and Jakobi (1972), was possi¬
ble by studying the drawings and descriptions present in
a catalogue compiled by the first author.

When necessary in the text is used of the Newick (par¬
enthetical) phylogenetic notation to discuss the species re¬
lationships within and between closely related clades.

Results

Subclass COPEPODA Milne-Edwards, 1840

Order HARPACTICOIDA Sars, 1903

Family PARASTENOCARIDIDAE Chappuis, 1940

Genus Eirinicaris gen. n.

http://zoobank.org/8F621641-4E8D-4D91-825D-81734B42BCEC

Diagnosis. Al eight-segmented in male, seven-segment¬
ed in female. Male Al haplocer, eight-segmented, hap-
locer, with small process in segment seven; segments 5,
6 , and 7 forming a functional unit for clasping the female,
in grasping position, segment 7 bent inwards against seg¬
ment 6, segment 8 points in opposite direction. Allobasis
of Mx with two endites; proximal endite with one seta;
distal endite with two elements, one of them transformed
into serrated spine; proximal endopodal segment drawn
out into claw, distal endopodal segment with two setae.
Basis of PI without remarkable sexual dimorphism;
with inner and outer seta, the former longer in male; enp

zse.pensoft.net

170

Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

Table 1. Character matrix for phylogenetic reconstruction of the valid genera included by Schminke (2010) within the subfamily
Parastenocaridinae. Character states polarized a priori; polarization from 0= most plesiomorphic to 4 = most apomorphic. ?= un¬
known state of the character.

Ameiridae

1110000000

0000000000

0100000000

0000000000

00000000

Fontinalicaris

0001211111

1111111111

1111111110

0000000000

0100000000

0000000000

00000000

Remanelcaris

0001111111

1111111111

1110100001

1011100111

1010000000

0000000000

00000000

Himalayacaris

0001211111

1111111111

1111100001

0112111000

0100000000

0000000000

00000000

Indocaris

0001211111

1111111111

1110100001

1011100111

1003000000

0000000000

00000000

Parastenocaris

0001211111

1111111111

1111100011

1110000000

0103111111

1111000000

0000000000

00000010

Kinnecaris

0001211111

1111111111

1111100001

1110000111

1101111110

0000110001

1100000000

00000110

Monodicaris

0001211111

1111111111

1111100001

1110000111

1102111110

0000110001

1010000000

00000?10

Macacocaris

0001211111

1111111111

1111100001

1110000000

0102100000

0000000001

0010012000

00000002

Simpllcaris

0001211111

1111111111

1111100011

1110000000

0101100000

0000000000

0000013010

02010000

Asiacaris

0001211111

1111111111

11111000?!

1110000000

0106100000

0000000000

0000004000

10000000

Stammericaris

0001211111

1111111111

1111100011

1110000000

0102100000

0000000000

0001011000

00000001

Cottarellicaris

0001211111

1111111111

1111100011

1110000000

0102100000

0000000000

0001101000

00000002

Clujensicaris

0001211111

1111111111

1111100001

1110000000

0106100000

0000000000

0000014000

00100000

Entzicaris

0001211111

1111111111

11111000?!

1110000000

0101100000

0000000000

0000002211

00000000

Italicocarls

0001211111

1111111111

11111000?!

1110000000

0101100000

0100000000

0000002100

00000000

Michellcarls

0001211111

1111111111

1111100001

1110000000

0101100000

0000000000

00000003

Minutacaris

0001211111

1111111111

1111100011

1110000000

0101100000

0000000000

0000013000

00100000

Nanacaris

0001211111

1111111111

1111100001

1110000000

0105100000

0000000010

0000014010

00000000

Eirinicaris

0001211111

1111111111

1111100001

1110000000

0104121000

0000111110

0000000000

00000121

Eiorstkutcaris

0001211111

1111111111

1111100001

1110000000

0104100000

0000000000

0000002211

00000000

Lacustricaris

0001211111

1111111111

1111100011

1110000000

0101100000

0000000000

0000012010

01011003

not sexually dimorphic. P2 enp without marked sexual
dimorphism. Male P3 with quadratic smooth coxa; ba¬
sis short, quadratic, with row of spinules close to outer
seta, without inner ornamentation; enp modified, aes-
thetasc-like; exp unisegmented, rectangular, longer than
wide, with irregular inner margin and with medial hump,
outer margin straight, with unevenly distributed spinules,
distal margin flat, inner apophysis shorter than support¬
ing segment, blade-shaped, without distal seta or spine,
thumb slightly longer than apophysis, with broad base,
proximal expansion on both sides and leaf-shaped distal
blade. Female P3 with spiniform enp ys as long as exp-
1. Male P4 enp cylindrical, approximately half as long
as exp-1, with three distal spinules and one medial outer
spinule. Enp of female P4 spiniform, almost as long as
exp-1, distally bipinnate. Male and female P5 well devel¬
oped, a simple triangular plate reaching middle of genital
somite in male, inner margin drawn into long and point¬
ed, outwardly curved, spinous process with distal pore,
without inner ornamentation, reaching beyond the genital
field in female; armature consisting of very long outer ba¬
sal seta and two additional setae, of which proximal most
shorter. Male P6 large, tetra-lobbed fused plate covering
genital area. Female P6 represented by naked opercu¬
lar plate much broader than the height covering genital
opening. Male telson with proximal lateral pore, trans¬
verse row of small spinules along entire dorsal surface,
anterior to sensilla, and rows of spinules covering most of
preopercular lateral margin. Female telson smooth, with
proximal ventral pore and ventral tube pore near inser¬
tion of furca. Male furca irregular, with distal outer pore,
longer than width, inner and dorsal margins convex, outer

and ventral margins concave; dorsal, inner and outer mar¬
gins covered by spinules; lateral setae I, II and III, and
dorsal setae VII separated by wide gap, setae I, II, and III
displaced to antero-ventral position, seta I modified into
short spine, with broad base and acuminate tip, seta III
1/3 as long as furca, with one long peduncle and one dis¬
tal aesthetasc-like structure, 1/2 size of seta II, seta II with
broad base, a long peduncle and one distal aesthetasc-like
structure; setae IV to VII smooth, dorsal seta (VII) medi¬
ally inserted in a depression; seta IV inserted subdistally
on outer margin, approximately as long as telson without
furca, seta V distal, twice as long as seta IV, seta VI distal,
1/2 as long as seta IV; proximal bulges on inner and out¬
er margins. Female furca rectangular with distal ventral
pore, longer than wide, smooth, slightly tapering distally,
with inner flat lobe; setae smooth, lateral setae I, II, and

III, and dorsal seta VII inserted medially and more or less
opposite to each other; lateral setae reduced to one small
(seta III) and two tiny setae (setae I and II); two uncinate
processes anterior to insertion of dorsal seta VII, setae

IV, V and VI inserted distally, length and ornamentation
of setae IV, V, and VI as for the male; seta VI inserted
beneath flat lobe, small spinules close to its insertion.

Eirinicaris antonioi gen. et. sp. n.

http://zoobank.org/8F621641-4E8D-4D91-825D-81734B42BCEC
Figs 2-8

Type material. Male dissected holotype mounted onto
three slides (sample VEA17/B/R/ROF/musgo; 20 Jan
2012; MZUSP 35273). One dissected female paratype

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Figure 2. Eirinicaris antonioi sp. n. Male: A habitus, lateral view; B anal somite with caudal furca, lateral view; C anal somite with
caudal furca, dorsal view; D anal somite with caudal furca, ventral view; E mouthparts; el antennule; e2 mandible; e3 maxillulae;
e4 maxillae; e5 maxilliped. Scale bars: 1 = 50 pm (A); 2 (B, C, D) = 50 pm; 3 (E) = 20 pm.

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mounted onto one slide (sample VEA17/B/R/ROF/mus-
go; 20 Jan 2012; MZUSP 35274), one undissected fe¬
male paratype (sample VEA15/C/CP/50; 20 Dec 2012;
MZUSP 35274), and two undissected male paratypes
mounted onto a single slide (sample VEA17/B/R/ROF/
musgo; 20 January 2012; MZUSP 35274).

Type locality. National Park of the Chapada dos Vea-
deiros (North of Goias, Brazil); Agua Fria River; 1230 m
MSF; speed of water current from low to medium; tem¬
perature 20 ±5°C; pH 5 ±1. Coordinates: 14°5’30.89”S,
47°29’34.47”W.

Etymology. The generic name is in honour of the first au¬
thor’s wife, Eirini Grapsa, combining her first name with
the ancient Greek substantive for shrimp, Kapi(^ (caris).
The specific epithet “antonioi” is posthumous homage to
Antonio Alves Corgosinho Filho, father of the first author.

Description of male. Fength 320pm (variability of the
type series 314-328pm), measured from rostrum to end
of telson excluding furca. Rostrum not fused to cephalo-
thorax, with wide base and two sensilla on tip (Fig. 2A).
Cephalothorax and Urs-2-5 with dorsal integumental
window (Fig. 2A). Patterns of sensilla as depicted. Telson
with transverse row of small spinules dorsally, anterior
to sensilla, and with rows of spinules covering most of
preopercular lateral margin (Figs 2A, B, C), without or¬
namentation ventrally (Fig. 2D), posteriorly clefted, con¬
ferring a bilobate shape posteriorly (Fig. 6D), with a pore
on the ventro-lateral margin. Furca irregular, with inner
and outer bulges proximally (Figs 2B-D and 6D-F) with
distal outer pore (Fig. 6F, arrowed), about three times as
long as width, inner and dorsal margins convex, outer
and ventral margins concave; with dorsal, inner and outer
spinules; with seven setae as follows: setae I, II and III
and dorsal seta VII not aligned, separated by wide gap;
setae I, II and III displaced anteroventrally; seta I modi¬
fied into short spine, with broad base and acuminate tip;
seta II with broad base, a long peduncle and one distal
aesthetasc-like structure, twice as long as seta III, the lat¬
ter 1/3 as long as furca, with a long peduncle and one dis¬
tal aesthetasc-like structure; setae IV to VII smooth; seta
IV inserted subdistally on outer margin, about as long as
telson excluding the furca; seta V inserted distally, twice
as long as seta IV; seta VI inserted distally next to seta V,
shorter than seta IV; dorsal seta VII inserted in a depres¬
sion located in the middle of the furca.

Al (Figs 3A, B; 6A, B) eight-segmented, haplocer,
with small process in segment seven (arrowed on Figs
3A, B; 6B); segments 5, 6, and 7 forming a functional
unit for clasping the female, in grasping position, seg¬
ment 7 bent inwards against segment 6, segment 8 points
in opposite direction (Fig. 6B); segments armature as
follows: 1 (0)/2(5)/3(4)/4(l)/5(3+ (l+ae))/6(0)/7(0)/8(7+
modified seta + (2+ ae)); segment 8 with seven slender
setae, two seta fused basally to aesthetasc, and one modi¬
fied seta, the latter as in Fig. 6C.

A2 (Fig. 2el) allobasis without abexopodal armature,
with small outer spinule proximally; one-segmented exp
with one bipinnate seta; free endopodal segment bearing
seven setae/spines, outermost strongly developed.

Fabrum (not shown) triangular in lateral view.

Md as in Fig. 2e2. Coxal gnathobasis with distal teeth
and one seta; palp one-segmented, with two distal setae.

Mxl as in Fig. 2e3. Praecoxal arthrite with five ele¬
ments (one surface seta, three claw-like pinnate spines,
and one slender seta); coxal endite with one, basis with
three setae.

Mx as in Fig. 2e4. Allobasis with two endites; proxi¬
mal endite with one, distal endite with two elements, one
of them transformed into serrated spine; proximal endop¬
odal segment drawn out into claw, distal endopodal seg¬
ment with two setae.

Mxp (Fig. 2e5) subchelate; syncoxa about 1/3 the
length of basis; enp drawn into spinulose claw.

PI (Figs 3B, 7A). Unarmed coxa ornamented with
posterior row of spinules; inner seta of basis reaching tip
of enp-1, with small row of spinules near insertion of enp,
with comparatively smaller outer seta, with pore and row
of spinules beneath outer seta; enp two-segmented, enp-1
nearly as long as exp-1 and exp-2 combined, with inner
row of spinules (Fig. 7A), and two outer rows of spinules;
enp-2 with one outer spine and one long geniculate seta,
with posterior hyaline frill; exp three-segmented, exp-1
with outer spine, proximal and distal rows of spinules on
outer margin, proximal and distal to outer spine, exp-2
unarmed, with row of inner spinules close to distal corner,
exp-3 with outer row of spinules proximally, with two
outer spines and two geniculate apical setae.

P2 (Figs 3C, 7A-B) coxa ornamented with posterior
spinules; basis without outer seta, with row of spinules
on outer margin and one outer pore; enp one-segment¬
ed, reaching middle of exp-1, armed with one distal seta,
ornamented with one distal and two outer spinules; exp
three-segmented, exp-1 with long outer spine, orna¬
mented with medial row of outer spinules, with one long
spinule and smaller spinule close to outer spine (Figs 3C,
7B), with hyaline inner frill; exp-2 unarmed, with distal
row of spinules; exp-3 with one outer unipinnate spine,
one distal unipinnate spine twice as long as outer ele¬
ment, and one bipinnate apical seta nearly twice as long
as previous element, additionally with longitudinal row
of spinules on distal third, proximal to outer spine and
inner hyaline frill.

P3 as in Figs 3D, dl, d2 and 7B-C. Coxa quadratic,
with posterior row of spinules; basis short, quadratic,
with outer pore, with row of strong spinules close to exp;
enp modified as claviform aesthetasc-like seta (Figs 3D,
7B-C); exp unisegmented, rectangular, about four times
as long as wide, inner margin irregular, with one medial
inner hump, outer margin straight, with unevenly distrib¬
uted spinules, distal margin fiat, inner apophysis shorter
than exp, blade-shaped, without distal spine or seta, com¬
pletely fused to exp, thumb slightly longer than apophysis,
blade-shape, with broad base, curved inwards proximally.

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Figure 3. Eirinicaris antonioi sp. n. Male: A antennule, with process arrowed on segment seven, segment six laterally detached;
B PI, anterior; C P2, anterior; D P3, anterior; dl distal part of exopod of P3 showing the apophysis, anterior; d2 distal part of exopod
of P3 showing the apophysis, posterior; E P4, anterior; F P5, with distal pore arrowed. Scale bar = 25pm.

P4 as in Figs 3E, 7B. Coxa with posterior row of
spinules; basis with outer pore, outer seta, and row of out¬
er spinules close to exp; enp cylindrical, with accuminate
tip, approximately half the length of exp-1, with three dis¬

tal spinules and one medial outer spinule; exp 3-segment-
ed, exp-1 with long outer spine, ornamented with row of
spinules proximally and subdistally, with comparatively
smaller distal spinules, and inner hyaline frill; exp-2 un-

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Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

Figure 4. Eirinicaris antonioi sp. n. Female; A antennule; B PI, depicted with coxa, basis enp-1 and exp-1; C P2 enp; D P3, ante¬
rior; E P4 anterior; F P5, with distal pore arrowed; G genital field; H anal somite with caudal furca; I furca, lateral view. Scale bar
1 (A, F) and 2 (C, D, E, G, H, I) = 25|im.

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Zoosyst. Evol. 93 (1) 2017, 167-187

175

igure 5. SEM image of Eirinicaris antonioi sp. n. A male habitus, lateral view; B female habitus, ventral view. Scale bar A = 10pm;
= 20pm.

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Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

SIGMA-0d-2S

SiGMA-04-25

SIGMA-04-25

Time:lS:l3;5C
Date :1 Ap> 201S

Time :15:4a:46
D3te:1 Apr 2016

7ime:l6:55:46
Date :1 Apr 2016

Time:15;31:41
Date :1 Apr 2016

EHT =
WD*
Mag =

eHT =
W0 =
Mag*

EHT = 10.00 kV
WD = 25.1 mm
Mag= 7.79 KX

EHT = 10.00 kV
WD = 0.2 mm
Mag* 4.93 KX

10,00 kV
6.2 mm
49.58 K X

Signal A = IciLene

System Vacuum * 3.SSe-006 Toir

Noise Reduction * frame Avg

10.00 kV
6,2 mm

13.50 K X

Signal A* InLens

System Vacuum = 2.27e-006 Torr

Noise Reduction * Frame Avg

Signal A *SE2
System Vacuum *
Noise Reduction *

1.47e.C06rorr
Line Int. Done

Signal A* SE2
System Vacuum
Noise Reduction

= 2.84e-006Torr
“Frame Avg

10 fim

EHT*l0.CClkV
\ WD = 10.9mm

Signal A * 5E2

System Vacuum * 4.£9e-006 Torr

Time :15:07:24

SIGMA-04-25

Mag = 3.57 K X

Noise Reduction * Fiame Avg

Date :1 Apr20l6

EHT = 10.00 kV

Signal A = SE2

ZEISS I-1

WD* 4.4 mm

System Vacuum * 146e-006 Torr

Time :1S:15:20

_J SIGMA-04-25

Mag s 18,21 K X

Noise Reduction ~ Frame Avg

Date :12 Apr 2016

Figure 6 . SEM image of Eirinicaris antonioi sp. n. Male: A antennule in lateral view; B antennule segments 6 (yellow) and 7 (cor¬
al); C antennule, segment 8 showing modified seta; D telson and furca, lateral; E furca, dorsal view; F furca, ventral view, showing
modified setae I, II and III and distal pore arrowed. Scale bars A = 10pm; B = 1pm; C = 200pm; D = 2pm; E = 2pm; F = 2pm.

armed, with distal row of spinules (a long one on outer
edge; arrowed), exp-3 with row of outer spinules subdis-
tally, with one unipinnate outer spine, and one bipinnate
distal seta nearly twice as long as outer element.

P5 (Figs 3F, 7D-E) well developed reaching slight¬
ly beyond middle of second urosomite; simple triangu¬
lar plate with outer pore, distal inner margin a long and
pointed, outwardly curved, spinous process with distal
pore (arrowed on Figs 3F and 7D), without inner orna¬

mentation; armature consisting of very long outer basal
seta and two shorter elements, of which proximal one
shortest.

P6 (Fig. 7E), large tetra-lobbed fused plate covering
genital area.

Description of female. Length 310pm (variability of the
type series 310-326pm), measured from tip of rostrum to
end of telson, excluding furca. Sexual dimorphism ex-

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177

Signal A - SE2

System Vacuum = 3.54e-006 Torr
hJoise Reduction - Frame Avg

Signal A s SE2

System Vacuum = 2.07e-OD6 Torr
hJoise Reduction - Frame Avg

SIGMA-04-25

EHT = 10.00 kV Signal A = InLens

WD ® 6.2 mim System Vacuum = 1.98e-006 Torr

Mag = 16.64 K X Moise Reduction = Frame Avg

Time :T6;02:54
Dale :1 Apr 2016

WD = 6.2 inin System Vacuum = 2.92e-O06 Torr
Mag= S.55 K X Noise Reduction = Frame Avg

Time 15:28:55
Dale ;1 Apr 2016

SIGMA-04-25

EHT = 10.00 kV Signal A = SE2

WD = 6.2 mm System Vacuum = 2.12e-006 Torr

Mag= 5,03 KX Noise Reduction = Frame Avg

EHT = 10,00 KV Signal A = SE2

WD ® 13.9 mm System Vacuum = 1.10e-006 mbar

Mag= 2,60 KX Noise Reduction = Frame Avg

SIGMA-04-25

lO pm

2 pm

Figure 7. SEM image of Eirinicaris antonioi sp. n. Male; A PI showing inner seta of basis; B P3 with endopod and thumb in colour,
P4; C claviform aesthetasc representing the endopod of P3; D P5, lateral view, with distal pore arrowed; E P5 and P6. Female: F
pro- and urosomites, ventral view showing endopods of P3 and P4, and P5 and P6. Scale bars A = 10pm; B = 10pm; C = 1pm; D
= 2pm; E = 2pm; F = 102pm.

pressed in Al, PI, P3, P4, genital-double somite, number
of integumental windows, telson and furca. Cephalothorax
and Urs-2-4 with dorsal integumental windows; window on
Urs-4 extending into ventral area (Figs 5B, 8A-B). Telson
smooth, and small ventral tube pore near insertion of fur¬
ca (Fig. 8A, arrowed); anal operculum smooth and convex
(Figs 4H, 8B). Furca (Figs 4H-I, 5B, 8A-B) rectangular,
with distal ventral pore (Fig. 8A, arrowed), three times as

long as wide, smooth, slightly tapering distally, with seven
smooth setae as follows: setae I, II and III, and dorsal seta
VII inserted medially, aligned, the former three setae more
or less opposite to the latter; lateral setae reduced to one
small (seta I) and two tiny setae (seta II and III); with two
uncinate processes anterior to insertion of dorsal seta (Fig.
4H, arrowed), setae IV, V and VI inserted distally, length
and ornamentation of setae IV, V, VI, and VII as in male.

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Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

Figure 8. Eirinicaris antonioi sp. n. Female: A last urosomite, telson and furca, ventral view, proximal and distal pores arrowed;
B telson and furca, lateral view. Scale bars A = 2|im; B = lOpm.

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179

A1 seven-segmented (Figs 4A, 5B); armature as fol¬
lows: l(0)/2(4)/3(4)/4(2+ (l+ae))/5(l)/6(l)/7(7+ (2+ae)).

PI (Fig. 4B) as in male, with comparatively shorter
inner basal seta.

P2 enp (Fig. 4C), slightly dimorphic in ornamentation,
with three outer and 2 distal spinules; exp three-segment¬
ed, exp-1 without long outer spinule close to the insertion
of the outer spine.

P3 as in Figs 4D, 7F. Coxa with posterior row of
spinules; basis with outer pore and row of spinules close
to outer seta, the latter long; exp two-segmented, exp-
1 with proximal row of spinules, outer spine, row of
spinules around outer spine, and inner hyaline frill; exp-2
with subdistal row of outer spinules, with inner hyaline
frill, outer unipinnate spine and distal bipinnate element;
enp one-segmented, spiniform, with one outer spinule as
shown, ys the length of exp-1.

P4 (Figs 4E, 7F) coxa and basis as in male; exp-land
3 as in male, enp-2 without long spinule on outer edge;
enp (Fig. 4E) spiniform, about as long as exp-1, distally
bipinnate.

P5 (Figs 4F, 5B, 7F) well developed, a simple trian¬
gular plate; distal margin a long and pointed, outward¬
ly curved, spinous process with distal pore (Fig. 7F, ar¬
rowed), without inner ornamentation, reaching beyond
genital field; armature as in male.

P6 (Figs 4G, 7F) represented by naked opercular plate
much broader than height covering genital opening.

Discussion

After the revisionary work of Jakobi (1972), attempts to
resolve the taxonomy and phylogenetic systematics with¬
in the Parastenocarididae resulted in the proposition of
two subfamilies (Schminke, 2010), some new genera, and
the redefinition of some other taxa (Table 2). However,
some questions remain unanswered and the taxonomic
and phylogenetic relationships within the family are far
from complete.

Of the genera mentioned on Table 2, only Simplicaris,
Monodicaris, Asiacaris, Parastenocaris, Remaneicaris,

Kinnecaris, Stammericaris, Cottarellicaris, Himalay-
acaris and Indocaris belong to the Parastenocaridinae.
Schminke (2010) also included the following genera with¬
in this subfamily: Clujensicaris, Entzicaris, Italicocaris,
Macacocaris, Michelicaris, Minutacaris, and Nanacaris.
Karanovic et al. (2012) synonymised Lacustricaris with
Parastenocaris. However, following Schminke (2013),
such course of action was premature since the type spe¬
cies of Lacustricaris is not Proserpinicaris lacustris
(Chappuis, 1958) but Lacustricaris budapestiensis (To-
eroek, 1935). Therefore, the genus Lacustricaris must be
reinstated in the future.

The genus Eirinicaris strongly differs from all the
above Parastenocaridinae genera by its unique sexually
dimorphic telson and furca. Eirinicaris does not exhib¬
it all the diagnostic characters of Parastenocaridinae, as
proposed by Schminke (2010) and its phylogenetic posi¬
tion within this subfamily is discussed below.

List of characters and phylogenetic discussion. The
characters are listed below and the state of each character
is indicated within parentheses.

1. Inner spine on the basis of leg 1: sexually mono-
morphic (0); sexually dimorphic (1);

2. Seta on the distal endite of Mx: modified, brush-like
(1); not modified (0);

3. Seta on the Md palp: modified, brush-like (1); un¬
modified (0);

4. No. of armature elements on praecoxal arthrite of
Mxl: >5 (0); 5 (1);

5. No. of segments of male Al: 10 (0); 9(1); 8 (2);

6. No. of segments of female Al: 8 (0); 7 (1);

7. No. of segments of the A2 enp: 2 (0); 1 (1);

8. No. of armature elements on triangular A2 exp:
three spines/setae, at least 1 modified (0); 1 seta (1);

9. No. of segments on mandibular palp: 2 (0); 1 (1);

10. Accessory setae on the first enp/claw of Mx: present
(0); absent (1);

11. Syncoxal seta of Mxp: present (0); absent (1);

12. P4: sexually dimorphic (1); monomorphic (0);

13. No. of endopodal segments of PI: 3 (0); 2(1);

14. Inner seta on enp-1 of PI: present (0); absent (1);

Table 2. List of genera redefined after Jakobi (1972) followed by the respective synonyms and genera proposed after Jakobi (1972).

Genera redefined after Jakobi (1972) and

synonyms

Parastenocaris (sensu Reid 1995 and Karanovic and Lee 2012a partim.; Junior synonym:
Biwaecaris; Brinckicaris, Enckellicaris, Oshimaensicaris), Remaneicaris (Corgosinho and
Martinez Arbizu 2005), Kinnecaris (Schminke 2008; Junior synonym: Catferocaris),
Brasilibathynellocaris (Corgosinho et al. 2010a; Junior synonyms Paraforficatocaris,
Pararemanelcarls), S/oZ/ca/'/s (Corgosinho et al. 2012b), Proserpinicaris (Karanovic et al.
2012; Juinior synonyms Nipponicaris, Pannonicaris) and Sfamme/'/'ca/'/s (Schminke 2013;
Junior synonym Phreaticaris)

New genera proposed after Jakobi (1972)

Potamocarls, Murunducaris, Simplicaris Galassi and De Laurentiis, 2004, Monodicaris,
Asiacaris, Dussartstenocaris, Horstkurtcaris, Iticocarls, Cottarellicaris; Pllmalayacarls and

Indocaris.

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Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

15. No. of endopodal segments of P2: 2 (0); 1 (0);

16. Exp-2 of P2: with outer seta (0); without (1);

17. Exp-2 of P2: with inner seta (0); without (1);

18. No. of endopodal segments of P3: 2 (0); 1 (1);

19. Exp-2 of P4: with outer seta (0); without (1);

20. Exp-2 of P4: with inner seta (0); without (1);

21. No. of endopodal segments of P4: 2 (0); 1 (1);

22. Exp of male P3: not prehensile (0); prehensile (1);

23. Integumental windows: absent (0); present on Cphl
and urosomites (1);

24. Armature of the first Mx endite: 2 (0); 1 (1);

25. P5 exp and benp: separate (0); fused (1);

26. Inner seta on the basis of PI: present (0); absent (1);

27. Ornamentation of basis of the male P4 between exp
and enp: present (1); absent (0);

28. Shape of the genital operculum: broader than height
(0); higher than width (1);

29. Exp of the male P3: with a proximal hump (1),
without hump (0);

30. Eength and shape of enp of female P3: short and
rounded (0); long and spiniform (1);

31. Relative position of lateral setae I, II and III, and
dorsal furcal setae VIE aligned (1); dorsal seta pos¬
terior to lateral setae (0);

32. Penultimate segment of the male Al: with apophy¬
sis (1); without apophysis (0);

33. Armature of the apophysis of male P3: with one
distal spine (0); spine lost or reduced to a hyaline
structure (1);

34. No. of armature elements on second endite of Mx:
two setae and one spine (0); 3 (1); 2 (2);

35. P5 intercoxal sclerite: present (0); absent (1);

36. Enp of the male P4 fused to the basis: present (1);
absent (0);

37. Flat strong spine on coxa of male P4: absent (0);
present (1);

38. Medial ornamentation on the outer margin of P4
exp-3: absent (0); present (1);

39. Medial ornamentation on the outer margin of P4
exp-2: absent (0); present (1);

40. Medial ornamentation on the outer margin of P2
exp-3: absent (0); present (1);

41. Medial ornamentation on the outer margin of P2
exp-2: absent (0); present (1);

42. Enp of male P3: present (0); absent or reduced to a
seta (1);

43. Position of outer setae of P4 exp-3: distal (0); sub-
distal (1);

44. Ornamentation of the basis of the male P4: simple
row of spinules (0); with normal spinules of equal
sizes (1); sclerotized, of different sizes (2); with
strongly transformed spinules building a spinular
complex or differently build into petaloid structures
(3); lost but conserving the enp (4); loss of enp (5)
loss of ornamentation and enp (6);

45. Eength of the apophysis of the male P3: short (0);
long(l);

46. Relative position of male setae I, II and III, and dor¬
sal furcal setae VIE setae I, II, and III and seta VII
inserted at distal third of the furca, or setae I, II and
III anterior to the dorsal seta VII (0); at the same
plane on furca’s midlength (1); setae I, II and III lo¬
cated proximally in the ventral margin of the furca,
dorsal seta VII on the distal third (2);

47. Relative position of female lateral and dorsal furcal
setae: lateral and dorsal seta inserted at the distal
1/3 of the furca or setae I, II, and III are anterior to
the dorsal seta VII (0); at the same plane on furca’s
midlength (1);

48. Shape of female furca: cylindrical (0); tapering dis-
tally (1);

49. Hyaline margin of male P3: present (1); absent (0);

50. Sexual dimorphism on P5: strong, based on differ¬
ence of length (1); absent or based on differences of
ornamentation (0);

51. Width of the proximal part of the endopod of male
P4: narrow base (0); broad base (1);

52. Eength and ornamentation of the endopod of the
female P4: longer than exp-1 with ornamentation at
distal 1/3; shorter than exp-1 or as long as exp-1 (0);

53. Shape of exp-1 of the male P4: strongly concave at
the inner margin (1); not concave (0);

54. Shape of exp of the male P3: inflate, with proximal
and medial hyaline cushions (1); without this char¬
acter (0);

55. Eength of male P5: spiniform process reaching far
beyond its own urosomite (1); short (0);

56. Eength of female P5: spiniform process reaching
far beyond its own urosomite (1); short (0);

57. Furca: dimorphic (1); monomorphic;

58. Enp of male P3: transformed into an aesthetasc-like
seta (1); without this character (0);

59. Cuticle ornamentation of body somites: smooth (0);
pitted (1);

60. Position of integumental window in the last and
penultimate Urs: dorsal (0); lateral (1);

61. Size and shape of the inner process on the penul¬
timate segment of the male Al: strong and sick¬
le-shaped (1); different shape (0);

62. Ventral ornamentation of male Urs 3: two groups of
spinules (1); absent (0);

63. Size of enp of the male P2: normally developed (0);
strongly reduced (1);

64. Shape of the enp of the male P4: “Y”-shaped, prox¬
imally bifurcate, with a distal flagellum or lamella

(1) ; of a different shape;

65. Shape of the apophysis of the male P3: foliaceous
and acuminate (1); different (0);

66. Eength of the thumb of the exopod of the male P3:
longer or as long as apophysis (0), shorter than
apophysis (1);

67. Shape of the enp of the male P4: foliaceous or trian¬
gular lamella (0); y-shaped enp (1); long spiniform

(2) ; short, claw-like, outwardly curved (3); lost (4);

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68. Shape of the apophysis on the male P3 exp: smooth
(0); proximally dilated, with a soft median attenua¬
tion and a thinner distal lamella at the outer margin
(1); proximally dilated, with a subtle median de¬
pression and a thinner distal lamella (2);

69. Length of furca relative to the telson: longer than
telson (1); as long or shorter than telson (0);

70. Shape of the enp of the male P4: spiniform, curved
inwards, sigmoid (1); different shape (0);

71. Enp of the male P2: present (0); absent (1);

72. P5 in both sexes: present (0); reduced (1); absent (2);

73. Shape of thumb of the exp of the male P3: a pointed
spine (0); digitiform, with rounded tip (1);

74. Outer seta of basis of P4: present (0); absent (1);

75. P5 dimorphism: with a single seta in both sexes,
elongate in male (1); with 2 or more setae (0);

76. Distal pore on the spiniform inner process of P5:
present (1); absent (0);

77. Shape of male furca: cylindrical (0); tapering distal-
ly (1); allometric in growth (2);

78. Ornamentation of the proximal outer margin of the
male P3: more than two spinules (0); two spinules
(1); less than two spinules (2); not ornamented (3);

The phylogenetic study of the family Parastenocaridi-
dae is a difficult task, which means working up Jakobi’s
(1972 a, b) legacy (Schminke 2013). The family is noto¬
rious for its ill-defined genera (Galassi and De Laurentiis
2004), and researchers must deal with a plethora of poor¬
ly detailed descriptions, a high level of convergence, and
ample distribution of plesiomorphic characters between
and within groups and genera, making generic divisions
difficult (Reid 1995, Galassi and De Laurentiis 2004,
Karanovic 2005, Schminke 2010, Corgosinho et al. 2012a,
b, Karanovic and Lee 2012a, b).

A phylogenetic hypothesis of the evolution of the sub¬
family Parastenocaridinae is herein proposed in order to
discuss the phylogenetic position of the genus Eirinicaris.
Recently, Schminke (2013) showed that meaningful con¬
clusions could be drawn from available data. Meta-analy-
sis of data collected from existing descriptions resulted in
a single most parsimonious tree, with tree length, consis¬
tency index and retention index indicating a high level of
convergence of characters within this subfamily (L=146,
CI=68, RI=72) (Fig. 9).

The monophyletic status of the Parastenocarididae,
Parastenocaridinae and Fontinalicaridinae were dis¬
cussed in previous studies (Martinez Arbizu and Moura
1994; Schminke 2010; Ranga Reddy et al. 2014). Charac¬
ters 1 -29 are compiled from the contributions mentioned
above. For polarization of these characters we recom¬
mend the studies of Martinez Arbizu and Moura (1994)
and Ranga Reddy et al. (2014). The diagnostic characters
for Parastenocaridinae and Fontinalicaridinae are pro¬
posed and discussed by Schminke (2010).

Parastenocaridinae. Schmincke (2010) proposes the
following diagnostic characters for the Parastenocaridi¬
nae, avoiding to make inferences about the polarization

of the characters: 1) the segments 5 and 7 form a func¬
tional unit for clasping the female. The segment 7 is sick¬
le-shaped in some species, with an apophysis developed
at the distal inner corner, and can fold back onto the fifth
segment during copula whereas the segment 8 points
medially; 2) female P3 enp is long and spiniform; 3) the
apophysis of male P3 is unarmed in most of the species;
4) the coxa of male P4 lacks an inner row of spinules,
but a row of spinules may be present near the insertion
of endopod or medially of the basis; 5) except for species
of Kinnecaris, Monodicaris and Macacocaris, all Paras¬
tenocaridinae share a small P5 in both sexes, not reaching
far beyond its own somite; 6) female genital field is rect¬
angular and much broader than high, and 7) the lateral
setae I, II, and III occur at the same level as, and almost
opposite to, the dorsal seta VII.

Eirinicaris can be included within the Parastenocarid¬
inae because of the following synapomorphies (Charac¬
ters 30-33):

a) Female P3 enp long, and spiniform, without distal
seta (ap);

b) the group of three lateral setae of the furca (setae
I, II and III), and the dorsal seta VII aligned (viz.
female) (ap);

c) Al is haplocer, with small process in segment 7 (this
process is sickle-shaped in genera such as Kinnecaris
and Monodicaris)', segments 5, 6, and 7 forming a
functional unit for clasping the female, in grasping
position, segment 7 bends inwards against segment
6, segment 8 points in opposite direction (ap);

d) the apophysis and terminal seta of the exp of male
P3 fused (ap);

In addition, Eirinicaris share the following symplesi-
omorphies with other Parastenocaridinae (Characters 26
and 28):

d) genital field rectangular, much broader than the
height (pi);

e) basis of PI with an inner seta (pi);

Length and shape of enp of female P3 (Character 30).
Ranga Reddy et al. (2014) considered the female P3 with
a terminal seta fused to the enp as a plesiomorphy for
the Parastenocaridinae. However, we consider this char¬
acter as an autapomorphy for the Parastenocaridinae, and
the reduced, unarmed and linguiform enp as a plesiom¬
orphy for the Fontinalicaridinae. Our decision is based
on the observation of the copepodid development of the
fontinalicaridin Proserpinicaris phyllura (Kiefer, 1938)
described by Glatzel (1991). On both male and female
copepodid IV the P3 enp is a linguiform structure, very
similar to the adult. Hence, we consider the spiniform fe¬
male P3 enp of Parastenocaridinae an autapomorphy.

Relative position of lateral and dorsal furcal setae (Char¬
acter 31). This character is the best documented for the

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1 2 3

Figure 9. Phylogeny of the Parastenocaridinae reconstructed by applying Hennigian principles and criterion of putative parsimony
based on the data matrix of Table 1. The cladogram was generated using the program NONA (Goloboff 1999) for cladistic parsi¬
mony, and in interface with WfNCLADA (Nixon 2002). For details see Material and Methods. Characters as explained in the text;
binary or multistate, polarized a priori; length of cladogram = 146. Circles represent autapomorphies, open circles represent autapo-
morphies by reversion of character state. Direction of character transformation indicated below each character.

family (Schminke 2010). There are three exceptions
only in which the dorsal seta VII and the lateral setae I,

II and III are not aligned. There is a slight gap between
the lateral setae (setae I, II and III) and dorsal seta VII in
Remaneicaris euniceae Corgosinho & Martinez Arbizu,
2005, and Parastenocaris trichelata Reid, 1995 (Schmin¬
ke 2010). The lateral setae I, II and III are inserted at the
middle of the furca, and the dorsal seta VII is inserted
distally in Himalayacaris alaknanda Ranga Reddy, To-
takura & Corgosinho, 2014. The anterior position of setae
I, II and III, and the posterior situation of the dorsal seta
VII is the condition described by Schminke (2010) for
Fontinalicaridinae. This is a plesiomorphic condition also
present in other Harpacticoida families such as Ameiridae
Boeck, 1865, Cletodidae Scott T., 1904, Canthocampti-
dae Braddy, 1880, etc. With exception of Eirinicaris gen.
n. and Macacocaris, the Parastenocaridinae condition,
with lateral setae I, II and III, and dorsal seta VII aligned,
and more or less opposite to each other, is observed in
both male and female of those species for which both
genders are described. In Eirinicaris, however, due to an
allometric growth in the male, the lateral setae I, II and

III are located proximally on the ventral margin, and the
dorsal seta VII is inserted medially inside a depression.
The normal condition for the subfamily is evident in the
female of Eirinicaris. It has been suggested that the male
and female of Macacocaris do not belong to the same
species (Schminke 2009), given the presence of a para-
stenocaridin-like furca in the male, but a fontinalicaridin

furca in the female. Although this is unusual, the sexually
dimorphic furca observed for Eirinicaris proves that such
dimorphism is possible.

Penultimate segment of the male A1 (Character 32), and
geniculation. Similarly to other Parastenocaridinae with
penultimate segment of the male Al sickle-shaped, and
with a functional clasping unit formed by segments 5, 6
and 7 (pocket-knife type, Schminke (2010)) as in Kinne-
caris and Monodicaris, the functional unit for clasping
is formed by the segments 5, 6 and 7 in Eirinicaris In
both cases the terminal segment 8 of the male Al points
medially (ap). Galassi and De Laurentiis (2004) briefly
addressed the different morphologies of the penultimate
segment of the male Al within the family Parastenocar¬
ididae. The study of the morphology of this segment in
the Parastenocaridinae reveals some diverging morphol¬
ogies. For example, in P. brevipes and many species of
the genus Parastenocaris (sensu Reid 1995), the penul¬
timate segment is strongly curved inwards, assuming a
quasi horizontal conformation, conferring to the limb an
appearance described as pocket-knife-like by Schminke
(2010) and the last segment inserts subdistally or medi¬
ally on the outer margin. Segment 7 has a medio-distal
protrusion prolonged into a long process with rounded
tip in Simplicaris (Galassi and De Laurentiis 2004: 420,
Fig. 1C). However, segment 7 is aligned with the previ¬
ous segment, and segment 8 inserts distally on segment
7, with the apophysis of the latter oriented obliquely to

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segment 8 when the A1 is in resting position. This is con¬
sidered here a modification of the sickle-shaped segment
7 as described by Schminke (2010) for the parasteno-
caridin pocket-knife male antennule. The morphology of
the penultimate male A1 segment of Simplicaris veneris
(Cottarelli and Maiolini, 1980) is similar to Parasteno-
caris brevipes. Nothing can be said about the shape and
strength of this the male antennular apophysis for the type
species of the genera Michelicaris, Italicocaris, Entzicar-
is, Horstkurtcaris, Nanacaris, Clujensicaris, Minutacaris
and Lacustricaris. The male A1 apophysis is present in
Parastenocaris, Kinnecaris, Monodicaris, Eirinicaris,
Stammericaris, and Cottarellicaris. The presence in Ma-
cacocaris is questionable and open to interpretation since
Chappuis (1952) only made reference to the presence of
a strongly prehensile male AT Following Galassi and
De Laurentiis (2004), the transformation of the penulti¬
mate segment of the male antennule may have appeared
independently within the family Parastenocarididae and
should be considered a derived state. Instead, we consider
the modifications of the 5th and 7th segment of the male
A1 as synapomorphies for the Parastenocaridinae (Ranga
Reddy et al. 2014). However, the transformation series of
the penultimate segment is difficult to establish. Hence, it
is difficult to say how many times the male Al apophy¬
sis have appeared and disappeared within the Parasteno¬
caridinae and if they evolved from absent to incipient to¬
wards a strong sickle-shape apophysis or if any other kind
of transformation is involved. To be sure, it is necessary
to recollect and/or restudy the type species of Micheli-
caris, Italicocaris, Entzicaris, Horstkurtcaris, Nanacaris,
Clujensicaris, Minutacaris and Lacustricaris, as well as
closely related species and other Parastenocaridinae spe¬
cies not included in this study, since they do not belong
and cannot be clearly included within any of the genera
currently available taxonomically.

Armature of the apophysis of male P3 (Character 33).
The apophysis is generally long and with a distal spine in
Fontinalicaridinae, and the spine is usually missing in the
Parastenocaridinae (see Schminke 2010). Some exceptions
are known. Among the Fontinalicaridinae from the Neo¬
tropical region, some species of Siolicaris exhibit a short
apophysis, and the distal spine of the apophysis is fused
or lost in all species of the genus, except for S. sandhya
(Ranga Reddy 2011). A long apophysis can be observed in
Iticocaris and in Brasilibathynellocaris (Corgosinho et al.
2010a, 2012a), but no trace of a distal spine can be ob¬
served in the adult, with the exception of a heteromorphic
male of B. salvadorensis (Noodt, 1962) and the copepodid
V of the same species (Corgosinho et al. 2010a), with a
2-segmented P3 exp with a distal spine not fused to exp-2.
Dussartstenocaris idioxenos Karanovic & Cooper, 2011,
from Australia and D. bisetosa Ranga Reddy, Totakura &
Shaik, 2016, are two examples of fontinalicaridins with¬
out the distal spine in the apophysis of the male P3 exp.
Within the Parastenocaridinae, only Himalayacaris alak-
nanda has a distal hyaline spine in the short apophysis. A

rounded hyaline cushion can be observed in some species
closely related to Parastenocaris brevipes (see Reid 1995,
Karanovic and Lee 2012a). We have no doubt that the
armed apophysis of the male P3 exp is a plesiomorphic
character, and the loss of this structure occurred several
times within the Fontinalicaridinae This is considered here
as a synapomorphy for the Parastenocaridinae, reverting to
the primitive condition only in H. alaknanda.

The following two characters are considered symplesi-
omorphies for the Parastenocaridinae.

Inner seta on the basis of PI (Character 26) The pres¬
ence/absence of an inner seta on the basis of the PI has
been exhaustively discussed by Galassi and De Laurentiis
(2004) and Schminke (2010). This character is considered
here as a plesiomorphy for the whole family, disappear¬
ing and reappearing only within the Parastenocaridinae.
The presence of a very long inner seta on the basis of PI
is an autapomorphy for Eirinicaris gen. n.

Shape of the genital operculum (Character 28). A geni¬
tal operculum which is broader than the height, appears
consistently in the females of all the species of Parasteno¬
caridinae studied so far. Interestingly, at least two types
of genital operculum are evident within the Parasteno¬
caridinae. In Eirinicaris, Simplicaris and Kinnecaris (see
Karanovic and Cooper 2011) the copulatory pore is cov¬
ered by what Galassi and De Laurentiis (2004) described
as “strongly sclerotized operculum represented by a sin¬
gle laminar plate running transversally across the geni¬
tal double-somite”. The copulatory pore is not covered
completely by such plate in Parastenocaris. Instead, two
lateral discrete plates representing the vestigial P6, form
a sclerotized plate, partially covering the genital aperture
and the median copulatory pores in Parastenocaris (see
Karanovic and Lee 2012a).

Ranga Reddy et al. (2014) proposed a division of the
Parastenocaridinae into two basic monophyletic groups:
one composed by Himalayacaris, Remaneicaris and the
Parastenocaris tirupatiensis-group (Indocaris), and a
group composed of the remaining Parastenocaridinae,
called here the crown-group. Our phylogenetic study
confirms that Ranga Reddy’s et al. (2014: 813) characters
34 (position of outer setae on third exopodal segment of
leg 4) and 35 (spinules near the insertion of the endopod
of male leg 4) support the clade formed by Himalayacaris,
Remaneicaris and Indocaris as proposed by Ranga Reddy
et al. (2014). Characters 38 to 41 appear convergently in
two monophyletic groups {Remaneicaris-Indocaris and
Kinnecaris-Monodicaris). Character 37 is an autapomor¬
phy for Himalayacaris. Character 50 is autapomorphic
for Remaneicaris. Character 62 is autapomorphic for Kin¬
necaris. For a discussion on the relationships within this
group see Ranga Reddy et al. (2014).

The crown-group is supported in the present study by
character 44 (ornamentation of the basis of the male P4)
and character 45 (length of the apophysis of the male P3).
These are discussed below.

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Ornamentation of the basis of the male P4 (Character 44).
A row of spinules on the basis of the male P4 close to the
insertion site of the enp appears in derived groups with¬
in Remaneicaris (Corgosinho et al. 2010b; group D). It
is absent in R. ignotus (Dussart, 1983), R. meyerabichi
(Noodt, 1962), in the R. argentina-group (Corgosinho
et al. 2010b; group A), and in the R. analuizae-group
(Corgosinho et al. 2010b; group C). This character ap¬
pears as a row of slender spinules inserted in a weakly
chitinized zone in derived Remaneicaris groups; however
these spinules are often omitted in original descriptions
(Corgosinho et al. 2007). This ornamentation consists of
strong petaloid elements in Indocaris, and increase in size
from the inner to the outer margin, and is not as complex
as in Parastenocaris. This ornamentation is not present
in the ground pattern of Remaneicaris, and our phyloge¬
netic hypothesis does not support the presence of such
ornamentation in the groundpattern of the clade (Himala-
yacaris {Remaneicaris, Indocaris)). Therefore, the strong
ornamentation on the basis of the enp is considered here
a synapomorphy for the crown-group, occurring conver-
gently in Indocaris.

Within the crown-group, this character evolves into
a strong row of unequal spinules in Stammericaris, Cot-
tarellicaris and Monodicaris. These spinules are strong¬
ly sclerotized and unequal in Parastenocaris, slender in
Kinnecaris and are missing in Eirinicaris. Strong unequal
spinules are present in Kinnecaris giselae Schminke,
2008. The condition observed in species of Cottarel-
licaris, Stammericaris, and in other species such as P.
palmerae Reid, 1992, is not homologous to the condition
observed for Parastenocaris brevipes and closely relat¬
ed species. In Parastenocaris, the spinular complex in¬
volves sclerotization, heteromorphy of the spinules, and
the presence of anterior and posterior spinules on the ba¬
sis. With exception of the enlargement and sclerotization
of some spinules, nothing similar has been observed for
Cottarellicaris, Stammericaris, and P. palmerae.

Length of the apophysis of the male P3 (Character 45).
Remaneicaris, Indocaris and Himalayacaris have short
apophyses which are, in general, as long as wide. Ex¬
ceptions for this can be observed in Indocaris inopinata
Ranga Reddy, Totakura & Shaik, 2016, and in Indocaris
tirupatiensis (Ranga Reddy 2011). The shortest apophy¬
ses are found in Indocaris imbricata Ranga Reddy, To¬
takura & Shaik, 2016, and in Himalayacaris alaknanda
Ranga Reddy, Totakura & Corgosinho, 2014, and in basal
members of Remaneicaris, with some exceptions occur¬
ring in species belonging to more derived groups within
Remaneicaris such as R. membranaceae (Noodt, 1965)
andi?. oncophora (Noodt, 1965) (Noodt 1965, Corgosin¬
ho 2007). The elongated apophysis seems to be also a
derived character in Indocaris. Interestingly, I inopinata
displays an intermediate condition between I imbricata
and I tirupatiensis. Hence, it seems more parsimonious to
assume a shorter apophysis for the ground pattern of the
Parastenocaridinae. A longer apophysis is a synapomor¬

phy for the crown-group, and a convergent short apoph¬
ysis appears both within the basal Parastenocaridinae as
well as within the crown-group (viz. Cottarellicaris).

Following the above reasoning, the crown-group as
defined here, can be divided into Michelicaris and two
large monophyletic groups composed by the following
genera:

a) Group-1: Stammericaris, Cottarellicaris, Italicoca-
ris, Entzicaris, Horstkurtcaris, Macacocaris, Nana-
caris, Asiacaris, Clujensicaris, Simplicaris, Lacus-
tricaris, and Minutacaris;

b) Group-2: Parastenocaris, Kinnecaris, Monodicar¬
is, and Eirinicaris.

Group-1. The monophyly of group-1 is supported on
the ground of a complex series of transformations of the
male P4 enp (Character 67).

Four main monophyletic subgroups were identified
within group-1: {Stammericaris, Cottarellicaris)', {Itali-
cocaris, {Entzicaris, Horstkurtcaris))', Macacocaris; and
{{Clujensicaris, {Asiacaris, Nanacaris)), {Minutacaris,
{Simplicaris, Lacustricaris))).

Schminke (2013) redefined the genus Stammericaris
and proposed Cottarellicaris to encompass similar spe¬
cies belonging to obviously distinct subgroups. Although
Schminke correctly described and discussed in detail the
diagnostic characters he proposed to each genus, he was
reluctant to explicitly discuss the synapomorphies for
both genera. However, he clearly defined the complex P4
enp as a character common to Stammericaris and Cot¬
tarellicaris. The presence of a seta or lamella inserted
distally on the male P4 enp with a proximal bifurcation
(what we call here “Y”-shaped enp) (Character 64) and
the presence of at most two spinules on the proximal out¬
er margin of the male P3 (Character 78) are considered
here as synapomorphies for Stammecaris and Cottarelli¬
caris. The “Y”-shaped enp is not exclusive for Cottarelli¬
caris and Stammericaris, but can be also found in Paras¬
tenocaris palmerae. However, Karanovic and Lee (2012)
attributed this species to Parastenocaris on the basis of
the presence of hyaline processes on the inner margin of
the basis of the male P4. We have discussed above the
condition of this ornamentation within this group and we
agree with Schminke (2012), not supporting the inclusion
of P. palmerae in the genus Parastenocaris. Some of the
characters proposed by Karanovic and Lee (2012a) are
symplesiomorphies, allowing the inclusion of unrelated
species within the genus Parastenocaris. As correctly
mentioned by Schminke (2013), Reid (1995) conceded
that the structure of the endopod P4 male complex and
the long and spinulate endopod P4 female could be tak¬
en as an indication that P. palmerae is part of the bre-
vipes-gxowg), but she argued that the short female geni¬
tal field, the P3 male and the setation of the caudal rami
speak against it. In our view, the length of the female P4
enp and the shape and setation of the furca of P. palmerae
clearly points against the inclusion of this species in Par-

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185

astenocaris. Additionally, P. palmerae should be includ¬
ed in a group of species closely related to Cottarellicaris
and Stammericaris as proposed by Schminke (2013),
based on similar morphology of the male basal ornamen¬
tation shape of the “Y-shape-like” endopod of male P4,
and similar morphology of the male P3 of Stammericaris
and P. palmerae, sharing a long apophysis and short¬
er thumb, convergently appearing as autapomorphy for
Stammericaris and as synapomorphy for a monophyletic
group composed by (Macacocaris, ((Nanacaris, (Asia-
caris, Clujensicaris)), (Minutacaris, {Simplicaris, La-
custricaris)))) (Character 66). Character 78 is discussed
by Schminke (2013), who describes a maximum of one
proximal and four distal spinules for Cottarellicaris, and
two proximal and eight distal spinules for Stammericaris.

Italicocaris, Entzicaris and Horstkurtcaris share a P3
apophysis with a “recorted” outer margin (Character 68,
shape of the apophysis on the male P3 exp), proximal-
ly dilated, with a median depression and a thinner distal
lamella. It is important to stress that Karanovic and Lee’s
(2012b) diagnosis to the genus Horstkurtcaris is not sup¬
ported by a single synapomorphy. Some characters such
as “Male antennula seven-segmented, prehensile, with
geniculation between third and fourth and fifth and sixth
segments” are the result of inaccurate descriptions, since
the male A1 is never seven-segmented in Parastenocari-
didae (Corgosinho et al. 2007). Additionally, the genicu¬
lation always occurs between 4th and 5th segment, and
between 6th and 7th segments. Therefore, the use of the
generic name Horstkurtcaris should be restricted to H.
nolli (Kiefer, 1930) and H. nolli alpina (Kiefer, 1960)
only, pending a revision and phylogenetic study of the
Parastenocaridinae at the species level. The similarities
between Entzicaris and Horstkurtcaris are considerable.
Both H. nolli and Entzicaris entzii (Toeroek, 1935) share
the morphology of the male P3, with an enpsigmoid in
shape, curved to the inner margin (Character 70 in this
study); the male P4 of E. entzi is different to that of H.
nolli in the presence of a single spinule on the basis close
to the insertion of the endopod. The female limbs are
slightly different in ornamentation and length of the en¬
dopod, and both species possess a long furca with all the
elements inserted distally. A remarkable difference can be
observed in the male P5, being shorter, with the setae in¬
serted distally, and with a feeble inner spiniform process
in H. nolli. Chappuis (1940) showed a larger P5 of H. no¬
lli with a conspicuous inner spiniform process, similar to
what was described for E. entzii. These astounding simi¬
larities suggest that H. nolli and E. entzii are geographical
variants of the same widely distributed species.

The third is composed solely by the genera Macaco-
caris; the fourth subgroup is composed by Clujensicaris,
Asiacaris, Nanacaris, Simplicaris, Minutacaris', and La-
custricaris. In most of these species the male P3 exp is
slender, slightly curved towards the inner margin, the
apophysis is elongate, blade-shaped, with a rounded tip,
without distal seta; the thumb ranges from smaller than
the apophysis (Character 66; 0^1) as in Simplicaris,

Minutacaris, Nanacaris, and Clujensicaris), to larger
than the apophysis (Character 66; 1^0) as in Asiacaris.
The monophyly of the group composed of Nanacaris,
Asiacaris, Clujensicaris, Minutacaris, Simplicaris and
Lacustricaris is supported by the presence of a short
spiniform enp of the male P4 (Character 67), which is
lost in Nannacaris, Asiacaris and Clujensicaris. This
group also diplays a trend towards the reduction or loss
of the armature of the basis of the male P4 as in Asiacaris
and Clujensicaris (Character 44). This character appears
convergently in Himalayacaris alaknanda. However, the
male P4 enp is not completely lost in H. alaknanda, ap¬
pearing as an inner uncinate bud on the basis.

The phylogenetic position of Macacocaris is difficult
to decipher. Macacocaris shares many characters with
other genera, such as the short enp of the male P4 (Char¬
acter 63) as in Monodicaris, the pitted cuticle (Character
61) as in Kinnecaris and Monodicaris, strong and une¬
qual ornamentation of the inner basis of the male P4 as
in Monodicaris, Par astenocaris, Stammericaris and Cot¬
tarellicaris, and the dimorphic P5 (shorter in the male,
with the elements arranged distally as in Par astenocaris).
Additionally, the males of the genus Macacocaris males
possess a strongly transformed Al, which Chappuis
(1952) describes as “fortement prehensiles”, probably
similar to what can be observed for Kinnecaris and Mo¬
nodicaris. Pending a full morphological and molecular
study of this genus, and the redescription of Macacocaris
macaco (Chappuis, 1952), its phylogenetic position is as
inferred in the cladogram (Fig. 9).

Group-2. This group is composed of the genera Par as¬
tenocaris, Kinnecaris, Monodicaris, and Eirinicaris.

Schminke (2009) recognized the similarities and close
relationship of Kinnecaris with Monodicaris. The recog¬
nition of the closer relationship between Kinnecaris and
Par astenocaris can be traced back to Lang (1948), who
pointed to the closer relationship between the P. brevi-
pes-gxon^ and the P. muscicola-gronp, the latter com¬
posed at that time of Kinnecaris cajfer (Chappuis, 1936)
andi^. muscicola {Chdi^^ms, 1936).

“The Brevipes-gxow^ must be closely related to the
Muscicola-gxovy). The enp of P4 is built in the same
way in both groups, however, the Brevipes-gxQW^,
which is the most derived group of both, have kept the
basal tooth or finger-like processes.” (free translation
from Lang 1948, p. 1219).

Par astenocaris, Kinnecaris and Monodicaris share
the tapering furca in the male and female in which the
lateral setae I, II and III, and the dorsal seta VII are situ¬
ated in the middle of the rami, setae I, II and III opposite
to seta VII (Characters 46 an 47, for the male and female,
respectively). The tapering furca and the position of se¬
tae I, II, and III aligned opposite to seta VII is observed
in the female of Eirinicaris (Character 48), changing
position of setae I, II, and III, their relative position to

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186

Corgosinho, RH.C. et al.: A new new genus of Parastenocarididae (Copepoda: Harpacticoida) from Brazil

seta VII (with a large gap between them), the shape and
ornamentation of the furca in the male as the result of the
extreme dimorphism.

Eirinicaris is closely related to Kinnecaris and Mo-
nodicaris. These three genera share the long spiniform
process on the male and female P5, reaching beyond the
middle of the second (genital) urosomite (Characters 55
and 56 for the male and female, respectively), and proxi¬
mal insertion of the lateral setae on the female. An inter¬
esting character, which was previously described for Kin¬
necaris by Karanovic and Cooper (2011), is the presence
of a pore at the distal rim of the inner acute spiniform
process of the P5 (Character 76). This pore is also pres¬
ent in Eirinicaris, but was not described for Monodicaris.
The recent observations of an undescribed species of a
new genus from Brazil (Corgosinho and Previattelli, pers.
obs.) revealed the presence of this pore on the male P5.
This is an indicative that this pore is widely distributed
within the family, making possible that it could have been
overlooked in Monodicaris.

On the morphology of Eirinicaris gen. n. Eirin¬
icaris gen. n. is an intriguing genus with some unique
characters. The basis of the male PI possesses a very
long inner seta, a character never reported for this fam¬
ily before. The telson and furca are very ornate in the
males of this species, and the furca exhibits an extreme
level of dimorphism with setae I, II and III situated
proximally on the ventral side of the furca. Spinular or¬
namentation on the telson and furca is not uncommon
within the family. The presence of spinular ornamen¬
tation on the telson is present in species closely relat¬
ed to the parastenocaridin R. analuizae Corgosinho &
Martinez Arbizu, 2005 and R. tridactyla Corgosinho,
Martinez Arbizu and Santos-Silva, 2007. Other species
within this subfamily such as P. spinicauda Wells, 1964,
P. spinosa Wells, 1964, P. trisaetosa Chappuis, 1954,
also possess spinular ornamentation on the telson. With¬
in the Fontinalicaridinae, Parastenocaris nigerianus
Chappuis, 1959 and some species of Forficatocaris ex¬
hibit spinular ornamentation of the telson. Concerning
the furca, normally the modification occurs in females
(Schminke 1976). Such high levels of ornamentation on
the telson and furca have never been described for the
family. Similar levels of ornamentation can be observed
only in freshwater Canthocamptidae Brady, 1880.

Equally impressive is the level of modification of the
posterior seta of the last segment of the Al, the endopod
of the P3 and the furcal setae I, II, and III in the males.
The last segment of the male Al possesses an addition¬
al modified aesthetasc-like seta ventrally. Additionally,
the enp of the male P3, and the furcal setae II and III
are transformed into aesthetasc-like structures. Within
the Copepoda the aesthetascs are generally restricted to
the Al. Aesthetascs are also present in the mouthparts of
some Paranannopidae Por, 1986 (Gee and Huys 1991).
To our knowledge, this is the first species of Copepoda
with aesthetascs-like setae on the furca and leg 3 of male.

Distribution and ecology. Prior to this study, Remanei-
caris was the only representative of Parastenocaridinae in
the Neotropical zone. The discovery of Eirinicaris in Bra¬
zil extends the geographical distribution of other mono-
phyletic groups of Parastenocaridinae to South America,
hence, indicating that all the main phylogenetic lineages
of Parastenocarididae were already present in a vast geo¬
graphical area, before the split of Pangea.

Aknowledgements

The authors would like to thank the National Council for
Scientific and Technological Development (CNPq) and the
Sao Paulo Research Foundation (FAPESP) for financing
the project “Biodiversity of Microcrustaceans in Brazilian
Rocky Fields” within the SCOPE of SISBIOTA (CNPq
563318/2010-4/ FAPESP 2010/52318-6). We also thank
the Chico Mendes Institute for Biodiversity Conservation
(ICMBio) and the Brazilian Institute of Environment and
Renewable Natural Resources (IBAMA), the first for al¬
lowing our studies at the National Park of the Chapada dos
Veadeiros (North of Goias, Brazil) and the second for issu¬
ing permits to collect freshwater invertebrates in National
Parks and other Brazilian territories. We are especially in
debt to the director of the National Park of the Chapada dos
Veadeiros and his staff for the field support and logistics.

References

Chappuis PA (1931) Copepoda Harpacticoida der Deutschen Limnolo-
gischen Sunda-Expedition. Archiv ftlr Hydrobiologie, Supplement-
band 8, Trop Binnengewasser 1: 512-584.

Chappuis PA (1952) Copepodes Harpacitcoides psammiques de Ma¬
dagascar. Memoires de I’lnstitut Scientifique de Madagascar 7:
145-160.

Corgosinho PHC, Martinez Arbizu P (2005) Two new interstitial species
of Remaneicaris Jakobi (Copepoda, Harpacticoida, Parastenocaridi¬
dae) from the Ribeirao do Ouro River, Brazil, with a redefinition of
the genus. Senckenbergiana Biologica 85; 147-162.

Corgosinho PHC, Martinez Arbizu P, Reid JW (2008) Revision of
the genus Murunducaris (Copepoda: Harpacticoida: Paraste¬
nocarididae), with descriptions of two new species from South
America. Journal of Crustacean Biology 28: 700-720. https;//doi.
org/10.1651/07-2907.1

Corgosinho PHC, Martinez Arbizu P, Santos-Silva EN (2010a) Revision
of Brasilibathynellocaris Jakobi, 1972 (Copepoda: Harpacticoida:
Parastenocarididae) with redefinition of the genus. Zoological Jour¬
nal of the Einnean Society 159: 527-566. https://doi.org/10.llll/
j.l096-3642.2009.00574.x

Corgosinho PHC, Martinez Arbizu P, Santos-Silva EN (2010b) Three
new interstitial species of Remaneicaris Jakobi, 1972 (Copepoda;
Harpacticoida: Parastenocarididae) from Southern and Southeastern
Brazil. Invertebrate Zoology 7(1): 1-28.

Corgosinho PHC, Martinez Arbizu P, Previatelli D (2012a) Establish¬
ment of a new genus for Parastenocaris itica (Copepoda, Harpac-

zse.pensoft.net

Zoosyst. Evol. 93 (1) 2017, 167-187

187

ticoida) from El Salvador, Central America, with discussion of the
Parastenocaris fontinalis and P. proserpina groups. Iheringia, Serie
Zoologia 102: 401-411.

Corgosinho PHC, Ranga Reddy Y, Martinez Arbizu P (2012b) Revision
of the genus Siolicaris Jakobi, 1972, with redescriptions of S. sioli
(Noodt, 1963) mdS. jakobi (Noodt, 1963) from South America, and
S. sandhya (Ranga Reddy, 2001) comb. n. from India (Copepoda,
Harpacticoida, Parastenocarididae). Zootaxa 3493: 49-71.

Cottarelli V, Bruno MC, Berera R (2010) First record of Parastenocarid¬
idae from Thailand and description of a new genus (Copepoda: Har¬
pacticoida). Journal of Crustacean Biology 30: 478-494. https://doi.
org/10.1651/09-3201.1

Da Silva JMC, Bates JM (2009) Biogeographic Patterns and Conserva¬
tion in the South American Cerrado: A Tropical Savanna Hotspot.
BioScience 53: 225-233.

Felgenhauer BE (1987) Techniques for preparing crustaceans for scan¬
ning electron microscopy. Journal of Crustacean Biology 7: 71-76.
Huys R, Boxshall GA (1991) Copepod evolution. The Ray Society,
Fondon, 468 pp. https://doi.org/10.2307/1548626
Gee JM, Huys R (1991) A review of Paranannopidae (Copepo¬
da: Harpacticoida) with claviform aesthetascs on oral append¬
ages. Journal of Natural History 25: 1135-1169. https://doi.
org/10.1080/00222939100770741

Glatzel T (1991) Neue morphologische Aspekte und die Copepodid-Stadien
Non Parastenocarisphyllnra Kiefer (Copepoda, Harpacticoida). Zoologica
Scripta 20: 375-393. https://doi.org/10.1111/j. 1463-6409.1991 .tb00302.x
Goloboff M (1999) Nona: A tree searching program. Program and doc¬
umentation. Ver.2.0. http://www.softpedia.com/get/Science-CAD/
NONA.shtml

Jakobi H (1972) Trends (Enp. P4 Mannchen) innerhalb cler Paraste-
nocarididen (Copepoda, Harpacticoida). Crustaceana 22: 127-146.
https://doi.Org/10.1163/156854072X00390
Jocque M, Fiers F, Romero M, Martens K (2013) Crustacea in Phy-
totelmata: a global overview. Journal of Crustacean Biology 33:
451-460. https://doi.Org/10.1163/1937240X-00002161
Karanovic T, Cooper SJB (2011) Third genus of parastenocaridid cope-
pods from Australia supported by molecular evidence (Copepoda,
Harpacticoida). In: Defaye D, Suarez-Morales E, Vaupel Klein JC
(Eds) Studies on Freshwater Copepoda: a Volume in Honour of Ber¬
nard Dussart. Crustaceana Monographs, Brill: 305-321. https://doi.
org/10.1163/ej.9789004181380.i-566.116
Karanovic T, Fee W (2012a) A new species of Parastenocaris from Ko¬
rea, with a redescription of the closely related P. biwae from Japan
(Copepoda: Harpacticoida: Parastenocarididae). Journal of Species
Research 1: 4-34. https://doi.Org/10.12651/JSR.2012.l.l.004
Karanovic T, Fee W (2012b) Invertebrate fauna of the world. Arthropo-
da: Crustacea: Harpacticoida: Parastenocarididae Parastenocaridid

copepods. National Institute of Biological Resources, Incheon, Ko¬
rea, Junghaengsa, Inc. 21(2): 1-232.

Karanovic T, Cho J-F, Fee W (2012) Redefinition of the parastenocari¬
did genus Proserpinicaris (Copepoda: Harpacticoida), with descrip¬
tion of three new species from Korea. Journal of Natural History 46:
25-26. https://doi.Org/10.1080/00222933.2012.681316
Fang K (1948) Monographic der Harpacticiden. Vol I and II.Hakan
Ohlssons Boktryckeri, Fund

Menzel R (1916) Uber das Auftreten der Harpacticiden gattungen Epacto-
phanes Mrazek und Parastenocaris Kessler in Surinam. Zoologischer
Anzeiger47: 145-152.

Nixon KC (2002) Winclada, v. 1.00.08. Program and documentation
available at www.cladistics.com

Ranga Reddy Y, Totakura VR, Corgosinho PHC (2014) Himalayaca-
ris alaknanda n. gen., n. sp. (Copepoda: Harpacticoida: Parasteno¬
carididae) from the hyporheic zone of a himalayan river. Northern
India. Journal of Crustacean Biology 34: 801-819. https://doi.
org/10.1163/1937240X-00002281

Ranga Reddy Y, Totakura VR, Shaik S (2016) A new genus and two
new species of Parastenocarididae (Copepoda: Harpacticoida) from
southeastern India. Journal of Natural History 50: 1315-1356.

Reid JW (1995) Redescription of Parastenocaris brevipes Kessler and
description of a new species of Parastenocaris (Copepoda: Harpac¬
ticoida: Parastenocarididae) from the U.S.A. Canadian Journal of
Zoology 73: 173-187. https://doi.org/10.1139/z95-020
Schminke HK (1976) The ubiquitous telson and the deceptive furca. Crus¬
taceana 30: 292-300. https://doi.org/10.1163/156854076X00657
Schminke HK (1976) Systematische Untersuchungen an Grundwasser-
krebsen - eine Bestandsaufnahme (mit der Beschreibung zweier neuer
Gattungen der Familie Parabathynellidae, Bathynellacea). Internation¬
al Journal of Speleology 8: 195-216. https://doi.org/10.5038/1827-
806X.8.1.18

Schminke HK (2008) First report of groundwater fauna from Papua New
Guinea: Kinnecaris Jakobi, 1972 redefined (Copepoda, Harpacti¬
coida, Parastenocarididae), and description of a new species. Crusta¬
ceana 81: 1241-1253. https://doi.org/10.1163/156854008X374568
Schminke HK (2009) Monodicaris gen. n. (Copepoda, Harpacticoida,
Parastenocarididae) from west Africa. Crustaceana 82: 367-378.
https://doi.org/10.1163/156854008X363713
Schminke HK (2010) High-level phylogenetic relationships within Paras¬
tenocarididae (Copepoda, Harpacticoida). Crustaceana 83: 343-367.
https://doi.org/10.1163/001121610X12627655658168
Schminke HK (2013) Stammericaris Jakobi, 1972 redefined and a new
genus of Parastenocarididae (Copepoda, Harpacticoida). Crustaceana
86: 704-717. https://doi.org/10.1163/15685403-00003196
Walter H (1985) Vegetation of the Earth and Ecological Systems of the
Geobiosphere. Springer-Verlag, New York, 318 pp.

zse.pensoft.net

Liebherr JK

Bryanites graeffii sp. n. (Coleoptera, Carabidae):
museum rediscovery of a relict species from Samoa

Pochai A, Kingtong S, Sukparangsi W, Khachonpisitsak S

The diversity of acorn barnacles (Cirripedia, Balanomorpha)
across Thailand’s coasts: The Andaman Sea and the Gulf of Thailand

Costa WJ EM

Redescription of Nothobranchius lucius and description of a new species
from Mafia Island, eastern Tanzania (Cyprinodontiformes, Aplocheilidae)

Albano PG, Bakker PAJ, Janssen R, Eschner A

An illustrated catalogue of Rudolf Sturany’s type specimens

in the Naturhistorisches Museum Wien, Austria (NHMW): Red Sea gastropods

Minton RL, Harris PM, North E, Tu DV

Diversity and taxonomy of Vietnamese Pollicaria (Gastropoda, Pupinidae)

Sandberger-Loua L, Muller H, Rodel M-0

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105

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135

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143

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Loveridge’s Angolan geckos, Afroedura karroica bogerti and Pachydactylus scutatus
angolensis (Sauria, Gekkonidae): new distribution records, comments
on type localities and taxonomic status

157

Corgosinho PHC, Schizas NV, Previattelli D, da Rocha CEF, dos Santos-Silva EN

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River basin (Goias, Brazil), and a phylogenetic analysis of the Parastenocaridinae

167

Zoosystematics and Evolution

93 ( 1 ) 2017

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