Table Of ContentMALACOLOGIA, 2001, 43(1-2): 237-311
DEEP-SEACRYPTOBRANCH DORID NUDIBRANCHS
(MOLLUSCA, OPISTHOBRANCHIA) FROM THE TROPICAL WEST PACIFIC,
WITH DESCRIPTIONS OFTWO NEW GENERAAND EIGHTEEN NEW SPECIES
Ángel Valdés
DepartmentofInvertebrateZoologyandGeology, CaliforniaAcademyofSciences,
Golden Gate Park, San Francisco, CA 94118, U.S.A.; [email protected]
ABSTRACT
The study of a large collection of cryptobranchi dorid nudibranchs from deep waters in New
Caledonia and the Philippines revealed the presence of Austrodoris kerguelenensis (Bergh,
1884); 18 new species belonging to the genera Cadlina, Austrodoris, Geitodoris, Discodoris,
Peltodoris, Paradoris, Diaulula, Rostanga, Sclerodoris, Baptodoris and Dendrodoris; and two
previouslyundescribedgenera, Goslineriaand Pharodohs.Theanatomyofallthesespecies, in-
cludingthedigestive, reproductive, and nervous system, arestudied in detail.
All these species areclearly distinguishablefrom othermembers oftheirgenera. Mostofthe
species have a pale, simple background coloration, and two ofthem lackeyes. Both character-
istics seem to be adaptations to living in deep waters. Other deep-water Atlantic and Pacific
species of dorid nudibranchs have similar adaptations. The two new genera are characterized
bythepresenceoflargecopulatoryspines,numerousflexiblespinesin Goslineria.andtwosolid,
bifid spines in Ptiarodohs. No othercryptobranch dorid genera previouslydescribed have simi-
larcopulatoryspines.
Some of the species here described belong to genera previously reported from cold ortem-
peratewaters, such asAustrodoris, Cadlinaand Diaulula. Mostofthespecies belongtogenera
thatarewidespreadineithercold,temperateortropicalwaters{Rostanga, Paradoris, Geitodoris
and Baptodoris), and only two belong to exclusively tropical genera (Sclerodoris and Den-
drodoris). Vicariant events and vertical dispersal could explain the processes of speciation and
theorigin ofthesedeep-waterspecies.
Keywords: Mollusca, Nudibranchia, Doridina, deep-water. PacificOcean.
INTRODUCTION Guinea, during the Challenger Expedition.
Bergh (1884) also described Archidoris aus-
In contrastto other groups of mollusks with tralisBergh, 1884, collected offthe Kerguelen
a well-docunnentecl deep-sea occurrence and Island at 173 m depth. Otherdorids studied in
numerous described deep-water species, that paperwere collected from shallow water.
very little is known about deep-sea opistho- Subsequently, Garcia et al. (1993) reported
branch mollusks, and particularlyaboutdeep- Austrodoris kerguelenensis (Bergh, 1884)
sea dorid nudibranchs. fromAntarcticdeepwaters.The genus Bathy-
To date, only three papers dealing with doris is collected from deep or cold shallow
deep Atlantic species of dorids have been waters, and it is the only genus of dorid nudi-
published. The first is Bouchet (1977), who branchs that is consistently known from the
described five new species and a new genus deep sea (Wägele, 1989; Baranets, 1993;
of cryptobranch dorids, including phyllidiids, Valdés & Bertsch, 2000).
from the northeast Atlantic. Later, Valdés & There had not been a significant collecting
Ortea (1996) described two new deep-sea effortofdeep-seaopisthobranchs in the Indo-
phyllidiids, also from the northeast Atlantic, Pacific until the French Musorstom Expedi-
and Valdés & Bouchet (1998a) described an tions. Three papers on dorid nudibranchs
abyssal new genus of Corambidae from the have been produced from the material col-
Norwegian Sea. lected intheseexpeditions: Valdés (2001) de-
The first report on deep-water Indo-Pacific scribed 12 new species of Phyllidiidae (gen-
dorids was Bergh's (1884) description of Ba- era Phyllidia and Phyllidiopsis) from deep
thydorisabyssorum Bergh, 1884, collected at waters around New Caledonia; Valdés &
4,435 m depth off New Ireland, Papua New Gosliner (in press) described four new
237
238 VALUES
species and a new genus of caryophyllidia- DESCRIPTIONS
bearing dorids from New Caledonia and the
Philippines: and Fahey & Gosliner (2000) de- Genus Cadllna Bergh, 1879
scribed three new species of the genus Hal- Type Species: Doris repanda Alder & Han-
gerdafrom these two areas and from Fiji. cock, 1842, by monotypy [= Cadlina lae-
Despite this recent proliferation of papers, ws(Linnaeus, 1767)].
there are still numerous genera and families
of dorids never reported from the deep sea. Cadlina abyssicolaValdés, new species
The present paper deals with the bulk of the (Figs. 2A, 3, 4)
collection of cryptobranch dorids collected
during the f\/lusorstom Expeditions; it consti- Material Examined
tutes the first attempt to describe in detail the
deep-water biodiversity of Indo-Pacific dorid HOLOTYPE: East of New Caledonia,
nudibranchs. Bathus 1 Expedition, stn. CP670 (20°54'S,
165°53'E), 394-397 m, 14 March 1993, 17
mm
preserved length, leg. P. Bouchet and B.
MATERIALSAND METHODS Richer de Forges (MNHN).
PARATYPES: New Caledonia, Musorstom
Thematerialexaminedwascollectedduring 4 Expedition, stn. DW222 (22°38'S,
several French scientific expeditions to the 167"37'E), 535-560 m, 29 September 1985,
southwest Pacific Ocean (Fig. 1) and the one specimen 13 mm preserved length, dis-
Philippinesbetweentheyears 1981 and 1994, sected, leg. P. Bouchet and B. Richer de
organized bythe Institutde Recherchepourle Forges (MNHN); stn. CC247 (22°09'S,
Développement(IRD,formerlyORSTOM)and 167°13'E), 435-460 m, 4 October 1985, one
the Muséum National d'Histoire Naturelle, specimen 20 mm preserved length, dis-
Paris. All specimens, including the type mate- sected, leg. P. Bouchet and B. Richer de
rial, aredeposited atthe Laboratoire de Biolo- Forges (MNHN). île des Pins, south of New
gie des Invertébrés Marins et Malacologie of Caledonia, SMIB 8 Expedition, stn. DW195
the Muséum National d'Histoire Naturelle, (22°59'S, 168°21'E), 508-514 m, 1 February
Paris (MNHN), the DepartmentofInvertebrate 1993, onespecimen 20 mm preserved length,
Zoology and Geology of the California Acad- dissected, leg. P. Bouchet and B. Richer de
emy of Sciences (CASIZ) and the Australian Forges (MNHN). South of New Caledonia,
Museum, Sydney (AM). Registration numbers Bathus 2 Expedition, stn. CP735 (23°02'S,
are not used in MNHN, and individual lotsand 166°56'E), 530-570 m, 13 May 1993, one
specimensare identified bythe uniquecombi- specimen 15 mm preserved length, leg. P.
nation of the station number and cruise Bouchet and B. Richer de Forges (MNHN).
acronym. Norfolk Ridge, New Caledonia, Bathus 3 Ex-
Descriptions of living animals are based on pedition, stn. CP831 (23°04'S, 166°56'E),
photographs or notes by collectors. All speci- 650-658 m, 30 November 1993, one speci-
mens available were dissected, and morpho- men 13 mm preserved length, leg. P.
logical examination was facilitated by making Bouchet, B. Richer de Forges and A. Waren
a dorsal incision. The internal features were (MNHN); stn. CP846 (23°03'S, 166°58'E),
examined and drawn using a dissecting mi- 500-514 m, 1 December 1993, onespecimen
croscope with a camera lucida. A portion of 14 mm preserved length, leg. P. Bouchet, B.
the mantle was critical-point dried for the Richerde Forges andA. Waren (MNHN); stn.
Scanning Electron Microscope (SEM). Spe- CP847 (23°03'S, 166"58'E), 405-411 m, 1
cial attention was paid to the morphology of December 1993, one specimen 15 mm pre-
the reproductive system, digestive system, served length, leg. P. Bouchet, B. Richer de
and central nervous system. The numbering Forges and A. Waren (MNHN). Southwest of
of the nerves in the central nervous system New Caledonia, Halipro 1 Expedition, stn.
was determined accordingtotheir relative po- CP868 (21°14'S, 165"55'E), 430-455 m, 23
sitionontheganglia.Thebuccal masswas re- March 1994, one specimen 12 mm preserved
moved and dissolved in 10% sodium hydrox- length, leg. B. Richerde Forges (MNHN); stn.
ide until the radula was isolated from the CP869 (21°14'S, 165°55'E), 450-490 m, 23
surrounding tissue. The radula was then March 1994, three specimens 11-16 mm pre-
rinsed in water, dried, and mounted forexam- served length, leg. B. Richer de Forges
ination with the SEM. (CASIZ 121095). North of New Caledonia,
DORID NUDIBRANCHS FROM THE DEEP PACIFIC OCEAN 239
CORAL Espj'ritu
Sapto - ^.
SEA
16^
jlaO
\
Récifs ^
d'Entrecasteaux Port-Vila; Ç> '3,
18^ ñ-
Cj Erromango
Récifsde
'Astrolabe
Tanria
20'
Anelghqwhat
Lifou^-\y. . : '^c
NEW Mare
22°
CALEDONIA
;|^ île;des
Pines
24'
,
'-S-
CO
162° 164° 166° 168° 170°
FIG. 1. Mapofthe NewCaledonia region, where mostofthesampleswerecollected.
Bathus 4 Expedition, stn. DW941 (19°02'S, Ventrally, the oral tentacles are short and
163°27'E), 270 nn, 8August 1994, one speci- grooved (Fig. 3F). The anterior border of the
men 14 mnn preserved length, leg. B. Métivier foot is grooved but not notched. The mantle
and B. Richerde Forges (MNHN). margin is about as wide as the foot.
Based on the field notes, the background
External Morphology colorofthe living animals is uniformlywhiteto
cream. The apices of the largertubercles are
2icAa)Tl.htTeuhbbeerocddlyoersi.ssusSmoomimseecwohovfaetrtehedelmew,viattmheodsr,iemopvslapela,r(csFoeinlg-y. ysaeralemloyewe.lcloolTowhreianstrhthehienpordpeohsroesrruevmse.daTsnhpdeecmgiialmnletnlhsea.vgelantdhse
arranged, are much larger than the others.
Thereareseveral, simpleand isolated mantle Anatomy
glandsaroundthe mantle margin. The perfoli-
ate rhinophoresarecomposedof30lamellae. The posterior end of the oral tube has two
There are seven bipinnate branchial leaves. strong retractor muscles (Fig. 3E), which are
240 VALDES
FIG.2. Preservedspecimens.A, Cadllnaabyssicola. newspecies, paratypefromMusorstom4(stn.CC247);
scale bar = 5 mm. B. Austrodoris kerguelenensis. Biocal (stn. DW33); scale bar = 2 mm. Austrodoris
caeca, newspecies, paratypefrom Halipro 1 (stn. CH876); scale bar= 5 mm. D. Pharodorisdiaphora. new
species, holotype; scalebar=2mm. E. Pharodorisphilippinensis, newspecies, holotype; scalebar=2mm.
F. Austrodorislaboutei, new species, holotype; scale bar= 2 mm. G. Geitodorispallida, new species, holo-
type: scale bar = 1 mm. H. Discodorisachroma, new species, paratype from Bathus 3 (stn. CP832); scale
bar-2 mm. I. Discodorissp.; scale bar= 10 mm.
FIG 3 Cadlinaabyssicola,newspecies,paratypefromSMIB8(stn. DW195).A. Dorsalviewoftheanatomy;
stnicevcaetliesoynbs-atresmc=a-l1escmbaalmre=bBa.1rmR=emp1.rmoDdm.u.cCteFin.tvMreaolsuytnshetreavmro;eua;sscssacylaseltebeambr;ar=sc=a1l1memmb.mar.=Ab0Db.er5teavmiilma.toifoEtn.hsAe:ntaae,mrpaiumolprlupalolraatn;idobnporbfoustcthcaeatledibcguoelnsb--;
be bursacopulathx; bg, bloodgland; bu, buccal ganglion; c, cerebral nerve; eg, cerebral ganglion; d, defer-
entduct; e, esophageal ganglion; f, femaleglands; g, genital nerve; h, hermaphroditeand digestiveglands;
hptleuhreaalrtn-erivei;ntpeisgt,inpel;eu1,ravlisgcaenrgalliolno;opp;r,mp,rorsettartaec;torr, rmhuisncolpeh;oroa,lenserovpeh;agrsu,s;renoaf,losryanlnxt;ubse,;spe,mipneadlalrenceerpvtea,clpei;,
sg, salivarygland; st, stomach; t, oraltentacle; v, vagina.
242 VALDES
attached to the body wall. The small, oval, a heartand a single blood gland situated over
muscularbuccal bulb hastwo additional mus- the central nervous system.
cles. Two long salivary glands connect to the
buccal bulb at the sides of the esophageal Etymology
junction. The buccal bulb is one-half as long
as the oral tube. The jaws consist of numer- From the Ancient Greek abyssos (deep)
ous thin, unicuspid elements about 20 (.im and the Latin cola (dweller), in reference to
long (Fig. 4D). The radular formula is 59 x the habitat of this species, used as a noun in
mm
(45.1.45) in a 20 preserved length speci- apposition.
men. The rachidian teeth have 4-5 elongate
denticles, noneofthem clearly largerthan the Remarks
others (Fig. 4A). The inner lateral teeth are
hamate, having a single cusp and a series of Cadlina abyssicola is clearly distinguish-
denticles.The innermostlateraltooth has3-4 able from other species of the genus. All the
short denticles on the inner side and 6-7 species previously described have denticu-
short, blunt denticles on the outer side. The lated mid-lateral teeth (Rudman, 1984),
following teeth have 7-10 blunt denticles only whereas C. abyssicola has smooth mid-lat-
on the outer side. The teeth increase in size eral teeth. Also, species of Cadlina, except
gradually towards the medial portion of the Cadlina dubia Edmunds, 1981, have bifid jaw
half-row. The mid-lateral teeth are hamate, rodlets (Rudman, 1984), whereas in
with a long cusp, and they lack denticles (Fig. abyssicola all of them are simple. Cadlina
4B). The outermost teeth have 10-12 small dubia, described from Ghana, differs from C.
denticles (Fig. 4C). The esophagus is long abyssicola in having much shorter radular
and connects directly to the digestive gland. teeth, all bearing strong denticles (Edmunds,
The ampulla is long and convoluted; it nar- 1981).
rows intothe gonoduct, which branches intoa Cadlina willani Miller, 1980, from New
short oviduct and the prostate (Fig. 3C). The Zealand, is the species with the closest geo-
oviduct enters the female glands near the graphic range to abyssicola. It is a white
center of the mass. The prostate is tubular species with a mid-dorsal yellow sthpe and a
and elongate (Fig. 3B); it narrows and ex- yellow band around the mantle margin. It is
pands again into the short deferent duct. The very different from C. abyssicola, which is
deferent duct opens into a common atrium white with yellow spots. Moreover, the mor-
with the vagina. The penis is unarmed. The phology of the radular teeth is very different
vagina is long and wide. At its proximal end, between these two species. The inner lateral
the vagina connects to the large, irregular teeth of abyssicola are narrow and elon-
bursa copulathx. From the distal end of the gate and have 6-7 short denticles on the
vagina, near the opening, a short duct con- outer side of the cusp, whereas those of C.
nects to the seminal receptacle and the uter- willani are shorter and have only 3 denticles
ine duct. The bursa copulathx is about ten on the outer side (Miller, 1980). Also, the mid-
times largerthan the seminal receptacle. lateral teeth of C. abyssicola are smooth,
In the central nervous system (Fig. 3D), the whereas in willani the mid-lateral teeth
cerebral and pleural gangliaappearto be par- have 7 strong denticles.
tially fused and distinct from the pedal gan- Cadlina nigrobranchiata Rudman, 1985,
glia. There are four cerebral nerves leading from southern Australia is clearly distinguish-
from each cerebral ganglion, and two pleural able from abyssicola in having a black gill
nerves lead from each pleural ganglion. The and black rhinophores (Rudman, 1985). Also,
buccal ganglia lie near the rest of the central the radular morphology of these two species
nervoussystem,joinedtothecerebral ganglia is very different. The rachidian teeth of ni-
by two long nerves. Gastroesophageal, grobranchiataare much shorterthan those of
rhinophoral, and optical ganglia are present. abyssicola. Moreover, the mid-lateral teeth
The pedal ganglia are clearly separated, with of C. abyssicola are smooth, whereas in
two nerves leading from each. The pedal and nigrobranchiatatheyhaveseveralstrongden-
parapedal commissures are enveloped to- ticles.
gether with the visceral loop along all their Schrödl (2000) reviewed the species of
length. ) Cadlina from South America and Antarctica.
The circulatory system (Fig. consists of All of them are clearly distinguishablefrom C.
DORID NUDIBRANCHS FROM THE DEEP PACIFIC OCEAN 243
FIG. 4. Cadlina abyssicola. new species, paratype from SMIB 8 (stn. DW195). A. Inner lateral teeth; scale
bar= 43jam. B. Mid-lateral teeth; scale bar= 60|.im. Outer lateral teeth; scale bar=43|.im. D. Jawele-
ments; scalebar=30|.
abyssicola in their radular morphology and affinisand magellanica, the seminal re-
anatomy. These five species - Cadlina ker- ceptacle inserts in the middle ofthevagina, in
.
guelensis Thiele, 1912; sparsa (Odhner, kerguelensis and C. sparsa it inserts near
1921); C. magellanica Odhner, 1926; affi- the bursa copulatrix, whereas in C. georgien-
nis Odhner, 1934; C. georgiensis Schrödl, sisand C. abyssicolathe insertion iscloserto
2000 - have denticulate mid-lateral teeth, the opening of the vagina. However, in C.
whereas they are smooth in C. abyssicola. In abyssicolatheseminal receptacleismoredis-
244 VALDES
tal than in . georgiensis and it is clearly Cadlina. The rachidian teeth have a number
stalked. In addition, the prostate and the am- of small denticles on each side of the central
pulla of abyssicola appear to be longer cusp that are not present in anyotherspecies
than those of C. georgiensis. previously described (Rudman. 1984)
However, sincethecolorofthelivinganimal
Cadlinasp. (Fig. 5) is unknown, and the reproductive system of
the single specimen collected is immature, I
Material Examined prefer not to name this species until new ma-
terial becomes available.
New Caledonia, Biocal Expedition, stn.
DW14 (22°47'S, 167°14'E), 440-450 m, 30 Genus AustrodorisOdhner, 1926
mm
August 1985, one specimen 5 preserved
length, leg. P. Bouchet, B. Métivier and B. Type Species: Archidoris rubescens Bergh,
Richer de Forges (MNHN). 1898, by original designation [= Aus-
trodoris l<erguelenensis (Bergh, 1884)].
External Morphology
Austrodoris kerguelenensis (Bergh, 1884)
The body is somewhat elevated, oval. The (Figs. 2B, 6, 7)
dorsum is covered with simple, conical tuber-
cles that are evenly arranged. The perfoliate Archidoris l<erguelenensis Bergh, 1884: 85-
rhinophores are composed of nine lamellae.
89, pi. 1,figs. 1-12.
TVehnetrraellya.rethfeiveorablipitnennattaeclebsranacrheiaslhorlteavaensd. Austr4o1d7o-r4i2s1g,eorfgigise.nsi1s-8G,arcnieawetsaly.n,o1n9y9m3y:
grooved. The antenor border of the foot is
herein.
simple. The mantle margin is wider than the See Wägele (1990, 1993) for a complete list
foot. of synonyms.
The color of the living animal is unknown.
The preserved specimen is uniformly white to
cream. The rhinophores and gill have the Material Examined
same color as the dorsum.
New Caledonia, Biocal Expedition, stn.
Anatomy DW33 (23°10'S, 167°10'E), 675-680 m, 29
mm
August 1985, one specimen 13 pre-
The jaws consist of numerous thin, unicus- served length, leg. P. Bouchet, B. Métivierand
pid elements about 10 (.im long (Fig. 5D). The B. Richer de Forges (MNHN). île des Pins,
prardeuslearrvefdormluelnagthis 6s8pexci(m1e9n..1.1T9h)einraach5idmiamn NDeWw193Cal(e2d5o°n5i9a',S, S1M68I°B21'8E),Ex5pe0d0i-t5imo0n8m, ms,tn.1
teeth have a large, single central cusp and February 1993, two specimens 10 pre-
5-6 blunt denticles on each side (Fig. 5A). served length, leg. P. Bouchet and B. Richer
The inner lateral teeth are wide, hamate, hav- de Forges (MNHN).
ing a single cusp and a series of denticles.
These teeth have 2-3 denticles on the inner External Morphology
side and 10-12 elongate denticles on the
outer side. The teeth increase in size gradu- The body is oval, almost rounded and
allytowardsthe medial portion ofthe half-row. somewhat elevated (Fig. 2B). The whole dor-
The mid-lateral teeth are hamate, with a long sum iscoveredwithsmall, elongatetubercles.
cuspand7-8 largedenticlesonlyontheouter In general, tuberclesarelargerinthecenterof
side (Fig. 5B).The outermostteeth have 5-11 the dorsum. Some tubercles are clearly
denticles (Fig. 5C). longer and are surrounded by areas with nu-
The reproductivesystemofthesinglespec- merous short tubercles (Fig. 6D). The
imen collected was immature, so information rhinophoral and branchial sheaths are edged
on the genital morphology is not available. by several long tubercles. The large, perfoli-
ate rhinophoresarecomposedof38lamellae.
Remarks The gill consists of six short, bipinnate
branchial leaves.
The radular morphology of this species is Ventrally, there are two short, conical oral
verydistinctfrom othermembersofthegenus tentacles (Fig. 7E). The anterior border of the
DORID NUDIBRANCHS FROM THE DEEP PACIFIC OCEAN 245
FIG. 5. Cadlinasp. specimenfrom Biocal (stn. DW14).A. Innerlat.eralteeth; scale bar= 15).im. B. Mid-.lat-
eralteeth; scalebar= 15jam. Outerlateralteeth; scalebar= 15 D.Jawelements; scalebar= 10
foot is grooved but not notched. The mantle Anatomy
margin is widerthan the foot.
Based onthefield notes, thecolorofthe liv- The posterior end of the oral tube has six
ing animals is uniformly white, with yellowish strong retractor muscles (Fig. 7C), which are
tubercles. The rhinophores and gill are pale attached to the bodywall. The oval, muscular
yellow. buccal bulb has two additional muscles. The
246 VALUES
-..-<* •'^,'^ — • ^—^
FIG. 6. Austrodoriskerguelenensis, specimen from SMIB 8 (stn. DW193).A. Innerlateral teeth; scale bar-
43|im. B. Mid-lat.eralteeth; scalebar-60|im. Outerlateralteeth; scalebar=60|.tm. D. Dorsaltubercles;
scalebar=430
buccal bulb is as long as the oral tube. The 6B). The outermost teeth are elongate and
labial armature is snnooth. The radular for- also lack denticles (Fig. 6C). The esophagus
mula is 36 X (56.0.56) in a 10 mm preserved is long and connects to the stomach.
length specimen. There are no rachidian The ampulla is long and convoluted; it nar-
teeth. The innerlateralteeth are hamate, hav- rows into the gonoduct, which branches into
ing a singlecusp, andthey lackdenticles (Fig. the short oviduct and the prostate. The
6A). The teeth increase in size gradually to- oviduct connects to the female glands near
wards the medial portion of the half-row (Fig. the centerofthe mass (Fig. 7B). The prostate
