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Research Article
Seven new “cryptic” species of Discodorididae (Mollusca, Gastropoda, Nudibranchia) from New Caledonia
expand article infoJulie Innabi‡, Carla C. Stout‡, Ángel Valdés‡
‡ California State Polytechnic University Pomona, Pomona, United States of America

Corresponding author: Ángel Valdés ( aavaldes@cpp.edu )

Academic editor: Nathalie Yonow
© 2023 Julie Innabi, Carla C. Stout, Ángel Valdés.
This is an open access article 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 original author and source are credited.
Citation: Innabi J, Stout CC, Valdés Á (2023) Seven new “cryptic” species of Discodorididae (Mollusca, Gastropoda, Nudibranchia) from New Caledonia. ZooKeys 1152: 45-95. https://doi.org/10.3897/zookeys.1152.98258
ZooBank: urn:lsid:zoobank.org:pub:D20AFC88-0963-45FE-A8B0-74D00728424F
Open Access

Abstract

The study of a well-preserved collection of discodorid nudibranchs collected in Koumac, New Caledonia, revealed the presence of seven species new to science belonging to the genera Atagema, Jorunna, Rostanga, and Sclerodoris, although some of the generic assignments are tentative as the phylogeny of Discodorididae remains unresolved. Moreover, a poorly known species of Atagema originally described from New Caledonia is re-described and the presence of Sclerodoris tuberculata in New Caledonia is confirmed with molecular data. All the species described herein are highly cryptic on their food source and in the context of the present study the term “cryptic” is used to denote such species. This paper highlights the importance of comprehensive collecting efforts to identify and document well-camouflaged taxa.

Keywords

Molecular phylogenetics, species delimitation, systematics, taxonomy

Introduction

The systematics of sea slugs has benefited enormously from the introduction of molecular data analyses, which have dramatically improved species delimitation and phylogenetic reconstruction, facilitating the description and re-description of taxa belonging to notoriously difficult taxonomic groups (e.g., Jörger et al. 2012; Churchill et al. 2014; Ekimova et al. 2015; Martín‐Hervás et al. 2021). In this context, the term “cryptic” is widely used to refer to taxa that are morphologically indistinguishable but can be identified or distinguished using molecular data (Jörger and Schrödl 2013). On the contrary, in ecological research, the term “cryptic” has long been used to denote organisms that are camouflaged on their environment or food source (Faulkner and Ghiselin 1983; Dalton and Godwin 2006; Cheney et al. 2014), and this is not uncommon in many sea slug lineages. But, while “cryptic” species of sea slugs and nudibranchs in the systematics sense have received a great deal of attention in recent years, resulting in the description and identification of numerous cryptic species (e.g., Epstein et al. 2019; Knutson and Gosliner 2022), “cryptic” sea slugs in the ecological sense have been somewhat neglected and have received significantly less attention compared to their often brightly colored, extravagantly shaped cousins.

“Cryptic” species of sea slugs in the ecological sense are difficult to collect, requiring a substantial effort by experienced collectors, or the collection and processing of substrate suspected to contain living specimens. With the exception of sacoglossans, for which substrate collection produces specimens relatively easily (Krug et al. 2016, 2018), few examples of papers describing ecologically cryptic sea slug species have been published in recent years (e.g., Pola et al. 2012; Donohoo and Gosliner 2020).

In this paper we examine a few ecologically “cryptic” species of dorid nudibranchs collected during three research expeditions to Koumac, New Caledonia. These expeditions included a multidisciplinary team of expert collectors and taxonomists, using a combination of a variety of collecting techniques and methods (direct collecting, substrate collecting, autonomous reef monitoring structures (ARMS), underwater vacuum-cleaners, brush baskets, dredging, ROVs, etc.), resulting in an exceptionally well-curated collection. Among the specimens collected were several extraordinarily cryptic species in the ecological sense that would have been difficult to detect without the collecting infrastructure of the Koumac expeditions.

All the species described or re-described herein belong to the family Discodorididae. While this group has been the subject of several monographic reviews (Valdés and Gosliner 2001; Valdés 2002; Dayrat 2010) there is no consensus on the taxonomic structure of the Discodorididae or the number of valid genera. Additionally, molecular phylogenies including substantial coverage of this group (e.g., Mahguib and Valdés 2015; Hallas et al. 2017) have failed to provide enough support to unravel the relationships among different clades. In the present study we use a newly generated molecular phylogeny, including a broad representation of Discodorididae genera, as well as morphological data to provide a framework of classification for the new species described. In some cases, this information is not sufficient to provide definitive generic placements and therefore they are left as tentative.

Materials and methods

Source of specimens

The material examined in this study was collected during three expeditions to Koumac, New Caledonia, organized by the "Muséum national d’Histoire naturelle, Paris, France (MNHN). All collected specimens were individually photographed, labeled, preserved in 95% ethanol, and deposited at the MNHN. A total of 56 specimens was examined in this study, 46 of which were successfully sequenced (Table 1).

Table 1.
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List of specimens examined in this paper, including isolate, voucher and GenBank accession numbers when available. Specimens labeled with an asterisk (*) were successfully sequenced for this study.

Species Isolate Voucher GenBank Accession Numbers
COI 16S H3
Aldisa albatrossae JM153a CASIZ 181288 KP871632 KP871679 KP871655
Asteronotus cespitosus – CASIZ 191163 MN720294 MN722441 MN720325
– CASIZ 191321 MN720296 MN722443 MN720327
Asteronotus hepaticus – – MW559976 MW559976 –
– CASIZ 191310 MN720295 MN722442 MN720326
Asteronotus markaensis – CASIZ 192316A MN720299 MN722446 MN720330
Asteronotus mimeticus – CASIZ 208221 MN720305 MN722452 MN720336
Asteronotus namuro – CASIZ 192297 MN720298 MN722445 MN720329
Asteronotus spongicolus – CASIZ 192317A MN720300 MN722447 MN720331
– CASIZ 194597 MN720301 MN722448 MN720332
Atagema spongiosa* JI09 MNHN IM-2013-86190 OQ362153 OQ379356 OQ366207
JI30 MNHN IM-2013-86189 OQ362156 – OQ366210
JI33 MNHN IM-2013-86188 OQ362154 – OQ366208
Atagema spongiosa JI02 MNHN IM-2013-86170 OQ362155 OQ379357 OQ366209
Atagema cf. osseosa – CASIZ 185142 MF958426 MF958296 –
Atagema notacristata – CASIZ 167980 KP871634 KP871681 KP871657
Atagema papillosa JI42 MNHN IM-2013-86192 OQ362138 – OQ366192
Atagema sobanovae sp. nov.* JI16 MNHN IM-2013-86211 OQ362139 – OQ366193
JI05 MNHN IM-2013-86181 OQ362141 OQ379351 OQ366195
JI06 MNHN IM-2013-86178 OQ362140 OQ379350 OQ366194
JI08 MNHN IM-2013-86187 OQ362142 OQ379352 OQ366196
JI19 MNHN IM-2013-86174 OQ362150 OQ379354 OQ366204
JI21 MNHN IM-2013-86179 OQ362145 OQ379353 OQ366199
JI23 MNHN IM-2013-86180 OQ362151 OQ379355 OQ366205
JI28 MNHN IM-2013-86175 OQ362146 – OQ366200
JI29 MNHN IM-2013-86171 OQ362148 – OQ366202
JI41 MNHN IM-2013-86173 OQ362149 – OQ366203
JI44 MNHN IM-2013-86176 OQ362147 – OQ366201
JI45 MNHN IM-2013-86177 OQ362143 – OQ366197
JI46 MNHN IM-2013-86172 OQ362144 – OQ366198
Atagema sobanovae sp. nov. – MNHN IM-2013-86229 – – –
Atagema kimberlyae sp. nov.* JI43 MNHN IM-2013-86191 OQ362152 – OQ366206
Carminodoris flammea – CASIZ 177628 MN720285 MN722433 MN720311
Diaulula greeleyi TL286 LACM 3016 KU950017 KU949947 KU950060
Diaulula nayarita TL176 LACM 153353 KU950018 KU949948 KU950061
Diaulula odonoghuei TL178 CPIC 01073 KU950036 KU949967 KU950080
TL179 CPIC 01074 KU950037 KU949968 KU950081
Diaulula sandiegensis TL025 CPIC 00911 KU950057 KU949987 KU950103
TL268 CPIC 01269 KU950058 KU949989 KU950105
Discodoris boholiensis – CASIZ 204802 MN720304 MN722451 MN720335
Discodoris cebuensis – CASIZ 185141 KP871639 KP871687 KP871663
– CASIZ 190761 MN720293 MN722440 MN720322
Discodoris coerulescens – CASIZ 182850 MF958421 MF958290 –
Doris kerguelenensis H20 – EU823146 EU823238 –
Doris pseudoargus – – AJ223256 AJ225180 –
Hexabranchus sanguineus JM70a CPIC 00336 KP871644 KP871692 KP871668
Hoplodoris desmoparypha – CASIZ 070066 MN720283 MN722431 MN720309
– CASIZ 309550 MN720308 MN722455 –
Hoplodoris rosans – CASIZ 182837 MN720288 MN722436 MN720318
– CASIZ 182921 MN720290 MN722438 MN720320
Jorunna artsdatabankia – NTNU-VM 58891 MW784174 MW784486 MW810589
– ZMBN 125946 MW784173 MW784485 MW810590
– ZMBN 127749 MW784172 MW784487 –
Jorunna daoulasi sp. nov. – MNHN IM-2013-86230 – – –
– MNHN IM-2013-86220 – – –
Jorunna daoulasi sp. nov.* JI22 MNHN IM-2013-86219 OQ362165 OQ379361 OQ366219
Jorunna hervei sp. nov. – MNHN IM-2013-86221 – – –
– MNHN IM-2013-86222 – – –
– MNHN IM-2013-86223 – – –
– MNHN IM-2013-86224 – – –
Jorunna hervei sp. nov.* JI47 MNHN IM-2013-86225 OQ362163 – OQ366217
JI48 MNHN IM-2013-86226 OQ362164 – OQ366218
Jorunna hervei sp. nov. – MNHN IM-2013-86227 – – –
– MNHN IM-2013-86228 – – –
Jorunna liviae – MNCN15.05/200187 OP948382 – –
– MNCN15.05/200188 OP948383 – –
– MNCN15.05/200189 OP948384 – –
– MNCN15.05/94693 OP948385 – –
Jorunna onubensis – ZMBN 125474 MW784171 MW784483 MW810587
Jorunna tomentosa – CASIZ 175752 MW784185 MW784508 MW810604
– CASIZ 175753 MW784202 MW784506 MW810610
– CASIZ 176820 MW784179 – MW810602
– CASIZ 193035 MW784176 MW784491 MW810607
Montereina nobilis – CASIZ 182223 HM162684 HM162593 HM162499
Paradoris liturata – CASIZ 177510 KP871648 KP871696 –
– CASIZ 182756 MW223084 MW220951 MW415015
Peltodoris atromaculata – – AF249784 AF430360 –
Platydoris sanguinea – CASIZ 177762 MF958416 MF958285 –
Rostanga byga – CASIZ 181157 MW223085 MW220952 MW415016
Rostanga calumus EED-Phy-934 – FJ917485 FJ917427 –
Rostanga elandsia – CASIZ 176110 KP871651 KP871699 KP871674
Rostanga poddubetskaiae sp. nov.* JI01 MNHN IM-2013-86199 OQ362134 OQ379347 OQ366188
JI03 MNHN IM-2013-86202 OQ362129 – OQ366183
JI07 MNHN IM-2013-86218 OQ362136 OQ379348 OQ366190
JI12 MNHN IM-2013-86203 OQ362122 OQ379345 OQ366176
JI13 MNHN IM-2013-86206 OQ362121 – OQ366175
JI15 MNHN IM-2013-86215 OQ362124 – OQ366178
JI17 MNHN IM-2013-86200 OQ362125 – OQ366179
JI18 MNHN IM-2013-86209 OQ362135 – OQ366189
JI20 MNHN IM-2013-86204 OQ362137 OQ379349 OQ366191
JI24 MNHN IM-2013-86216 OQ362127 OQ379346 OQ366181
JI25 MNHN IM-2013-86208 OQ362119 OQ379344 OQ366173
JI26 – OQ362132 – OQ366186
JI27 MNHN IM-2013-86205 OQ362130 – OQ366184
JI31 MNHN IM-2013-86212 OQ362126 – OQ366180
JI32 MNHN IM-2013-86201 OQ362133 – OQ366187
JI36 MNHN IM-2013-86213 OQ362120 – OQ366174
JI37 MNHN IM-2013-86214 OQ362123 – OQ366177
JI38 MNHN IM-2013-86217 OQ362128 – OQ366182
JI39 MNHN IM-2013-86207 OQ362131 – OQ366185
Rostanga poddubetskaiae sp. nov. JI40 MNHN IM-2013-86210 – – –
Rostanga pulchra – CASIZ 174490A MW223086 MW220953 MW415017
Sclerodoris sp. – CASIZ 182866 MN720289 MN722437 MN720319
– CASIZ 191525 MN720297 MN722444 MN720328
Sclerodoris faninozi sp. nov.* JI11 MNHN IM-2013-86198 OQ362161 OQ379359 OQ366215
Sclerodoris dutertrei sp. nov.* JI04 MNHN IM-2013-86193 OQ362157 OQ379358 OQ366211
JI14 MNHN IM-2013-86196 OQ362160 – OQ366214
JI34 MNHN IM-2013-86195 OQ362159 – OQ366213
JI35 MNHN IM-2013-86194 OQ362158 – OQ366212
Sclerodoris tuberculata – CASIZ 190788 MF958417 MF958286 MN720323
Sclerodoris tuberculata* JI10 MNHN IM-2013-86197 OQ362162 OQ379360 OQ366216
Taringa sp. – CASIZ 172039 MN720284 MN722432 MN720310
Taringa telopia – CASIZ 182933 MN720291 KP871700 KP871675
Tayuva ketos TL086 CPIC 00654 KU950019 KU949949 KU950062
Thordisa aff. albomacula – CASIZ 179590 MF958418 MF958287 MN720313
– CASIZ 181136 MN720286 MN722434 MN720314
– CASIZ 182834 MT454622 MT452888 MT454628
– CASIZ 220322 MT454620 MT452884 MT454624
Thordisa bimaculata – CASIZ 184516 MN720292 MN722439 MN720321
Thordisa nieseni – CASIZ 173057 MW223087 MW220954 MW415018

DNA extraction, amplification, and sequencing

From each specimen a small tissue sample (~ 1 mm3) was taken from the foot using sterilized forceps. DNA extraction was conducted using a Chelex protocol using a mixture of 200 µL of 10% Chelex 100 (Bio-Rad.com), blotted tissue (to remove any remaining ethanol), and 4 µL of proteinase K. The 1.7 mL microcentrifuge tubes with the mixture were placed in a water bath for 20 min at 55 °C (cell lysis and protein digestion) followed by placement in a heat block at 100 °C for 8 min (protein denaturation). Then, the microcentrifuge tubes were centrifuged to separate the Chelex beads from the supernatant containing the DNA, and 100 µL of the supernatant was aliquoted and used for DNA amplification.

The Polymerase Chain Reaction (PCR) was conducted on all samples for three genes: cytochrome c oxidase subunit one (CO1, mtDNA), ribosomal RNA 16S (16S, mtDNA), and Histone H3 (H3, nuclear), using universal primers (Folmer et al. 1994; Palumbi 1996; Colgan et al. 1998) in a Thermal Cycler T100 (Thermo Scientific, Waltham, MA). Each reaction was conducted using 38.5 µL of ultra-pure water, 5 µL of 10× PCR Dream Taq Buffer, 1.25 µL of Bovine Serum Albumin (BSA 20mg/mL), 1 µL 10 mM dNTPS, 1 µL forward primer, 1 µL reverse primer, 0.25 µL of Dream Taq, and 2 µL of DNA extraction, which resulted in each microcentrifuge tube containing a total volume of 50 µL. Reaction conditions for 16S and H3 were are follows: initial denaturation at 94 °C for 2 min, denaturation at 94 °C for 30 sec, annealing at 50 °C for 30 sec, elongation at 68 °C for 1 min, 30 cycles from denaturation to elongation and a final elongation at 68 °C for 7 min. Reaction conditions for COI were are follows: initial denaturation at 95 °C for 3 min, denaturation at 94 °C for 45 sec, annealing at 45 °C for 45 sec, elongation at 72 °C for 2 min, 35 cycles from denaturation to elongation and a final elongation at 72 °C for 10 min. Gel electrophoresis was conducted using 1% agarose tris-borate-EDTA (TBE) buffer and ethidium bromide for 15 min, including a ladder and a negative control to verify successful amplification of the PCR products of the correct length and confirm the absence of contamination. DNA purification was conducted with E.Z.N.A Cycle Pure D6492-02 kits (Omega Bio-Tek, Inc., Norcross, GA) following the manufacturer’s instructions. DNA concentration of purified samples was measured using a Nano Drop 1000 spectrophotometer (Thermo Scientific, Waltham, MA) prior to Sanger sequencing, which was outsourced to Retrogen Inc. (San Diego, CA).

Data analysis

Forward and reverse sequences were assembled, edited, and consensus sequences were extracted using the computer program Geneious v. 11.1.5 (Kearse et al. 2012). Additional sequences were downloaded from GenBank for comparison (Table 1). Sequences were aligned using the MUSCLE (Edgar 2004) plug-in in Geneious. Gaps in the 16S alignment were removed manually, and concatenation of all three genes was performed in Geneious. Bayesian and maximum likelihood phylogenetic analyses were conducted on the concatenated sequences (partitioned by gene) and on each gene fragment individually. Bayesian analysis was implemented using MrBayes v. 3.2.1 (Ronquist et al. 2012) with the GTR model, using two runs of six chains for 10 million repetitions with a sampling interval of 1,000 repetitions and burn-in of 25% removed. The maximum-likelihood analysis was conducted in RaXMLGUI v. 1.0 (Silvestro and Michalak 2012) using the bootstrap + consensus option and the GAMMAGI model with 10,000 bootstrap repetitions. Hexabranchus sanguineus (Rüppell & Leuckart, 1830) was used to root the resulting trees. Nodes in the resulting phylogenetic tree with Posterior probabilities (PP) ≥ 90% and bootstraps values (MLB) ≥ 70% were interpreted as supported.

The Automatic Barcode Gap Discovery (ABGD) software (Puillandre et al. 2012) was used to provide statistical support to determine the number of species in the sample using COI sequences of 107 specimens. Pairwise p-distance values were calculated using MEGA v. 11.0.13 (Kumar et al. 2018) using the Kimura-2 model (Kimura 1980).

Morphological examination

At least two specimens (if available) from each species recovered in the ABGD analysis were dissected to study their reproductive system (including the penis), jaw (if present), and radula. Dissections were performed by a dorsal incision from the middle of the nudibranch to the anterior end. The reproductive system was carefully removed from each specimen and drawn with a camera lucida. The penis was dissected and examined under a compound microscope. The buccal mass (including the radula and jaw) was removed from the anterior end of each animal and placed in a 10% NaOH solution to dissolve soft tissue and expose the radula and jaws. After 20 min to several hours, the radula and labial cuticle (housing the jaw) were rinsed in distilled water and mounted on a small copper plate for Scanning Electron Microscopy (SEM) examination. The samples were sputter-coated with gold and observed under a JSM- 6010PLUS/LA SEM at California Polytechnic State University, Pomona, California.

Results

The concatenated phylogenetic trees (BI and ML) recovered species of Discodorididae Bergh, 1891 + Cadlinidae Bergh, 1891 (represented by the genus Aldisa Bergh, 1878) as a monophyletic group (PP = 0.99, MLB = 70) (Fig. 1). Members of the genus Atagema Gray, 1850 are monophyletic (PP = 1, MLB = 100) and sister to the rest of Discodorididae + Cadlinidae (PP = 0.98, MLB = 96). The remaining Discodorididae (when Aldisa and Atagema are excluded) is monophyletic (PP = 1, MLB = 89) and contains a number of clades, most of which are not supported. The analyses recovered a clade containing species identified as Sclerodoris Eliot, 1904 (including the type species, S. tuberculata Eliot, 1904), as monophyletic (PP = 1, MLB = 100), which is sister to the single representative of Platydoris Bergh, 1877 (PP = 1, MLB = 92); these two groups appear to be related to another monophyletic group (PP = 1, MLB = 100), containing two species identified as members of Diaulula Bergh, 1878 [D. nayarita (Ortea & Llera, 1981) and D. greeleyi (MacFarland, 1909)], but the relationship between Platydoris, Sclerodoris, and these two species of Diaulula is not supported. Another monophyletic group includes species identified as Rostanga Bergh, 1879 (PP = 0.79, MLB = 94), with unresolved relationships to other Discodorididae clades. The genus Discodoris Bergh, 1877, including the type species D. boholiensis Bergh, 1877, is also monophyletic (PP = 1, MLB = 100) and sister to the single representative of Carminodoris Bergh, 1889 (PP = 1, MLB = 99), and these two groups appear to be related to some species identified as Thordisa Bergh, 1877, which also form a monophyletic group (PP = 1, MLB = 100). Although not supported in the ML analysis, Discodoris, Carminodoris, and Thordisa appear to be related to the monophyletic genus Jorunna Bergh, 1876 (PP = 1, MLB = 96), including the type species J. tomentosa (Cuvier, 1804). Another genus recovered as monophyletic is Asteronotus Ehrenberg, 1831 (PP = 1, MLB = 91), including the type species A. cespitosus (van Hasselt, 1824), which is sister (PP = 1, MLB = 94) to another monophyletic group including species identified as Hoplodoris Bergh, 1880 (PP = 1, MLB = 99), and together sister (PP = 1, MLB = 75) to another group of species identified as Thordisa (PP = 1, MLB = 99). Other traditional genus-level groups appear to be related but these relationships are not supported; these include Paradoris liturata (Bergh, 1905), the type species of Peltodoris Bergh, 1880 (P. atromaculata Bergh, 1880), Discodoris coerulescens Bergh, 1888, and specimens currently identified as Tayuva lilacina (Gould, 1852). Finally, the genus Diaulula including the type species D. sandiegensis (Cooper, 1863) is monophyletic (PP = 1, MLB = 100) and sister to Montereina nobilis MacFarland, 1905. Single gene fragment phylogenetic analyses provided similar results in general but with lower resolution (Suppl. materials 1–3).

Figure 1. 

Graphic representation of the molecular analyses results A histogram represents the distance plot for the ABGD analysis using the COI gene showing pairwise p-distances (Kimura 2 model) among candidate species B Bayesian consensus tree of the concatenated 16S, COI and H3 gene fragments. Posterior probabilities from the Bayesian analysis are listed above each branch; bootstrap values from maximum likelihood analysis are listed below each branch.

The ABGD analysis recovered 52 distinct species in the sample, which matches the structure recovered in the phylogenetic analysis (Table 2). The species recovered include all the taxa described below in the systematics section and species currently recognized as valid in the literature. The only exceptions are Diaulula sandiegensis and Diaulula odonohuei (Steinberg, 1963), which ABGD failed to recover as distinct, and specimens identified as Discodoris cebuensis Bergh, 1877, which ABGD recovered as two distinct species.

Table 2.
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Candidate species (groups) recovered in the ABDG analysis of COI sequence fragments. Initial Partition with prior maximal distance P = 2.15e-02; barcode gap distance = 0.088; distance simple distance minimum slope = 1.00.

Group Species Voucher # (Isolate #)
1 Aldisa albatrossae CASIZ 181288 (JM153a)
2 Asteronotus cespitosus CASIZ 191321, CASIZ 191163
3 Asteronotus hepaticus n/a, CASIZ 191310
4 Asteronotus markaensis CASIZ 192316A
5 Asteronotus mimeticus CASIZ 208221
6 Asteronotus namuro CASIZ 192297
7 Asteronotus spongicolus CASIZ 192317A, CASIZ 194597
8 Atagema cf. osseosa CASIZ 185142
9 Atagema notacristata CASIZ 167980
10 Atagema kimberlyae sp. nov. MNHN IM-2013-86191 (JI43)
11 Atagema papillosa MNHN IM-2013-86192 (JI42)
12 Atagema sobanovae sp. nov. MNHN IM-2013-86211 (JI16), MNHN IM-2013-86178 (JI06), MNHN IM-2013-86181 (JI05), MNHN IM-2013-86187 (JI08), MNHN IM-2013-86177 (JI45), MNHN IM-2013-86172 (JI46), MNHN IM-2013-86179 (JI21), MNHN IM-2013-86175 (JI28), MNHN IM-2013-86176 (JI44), MNHN IM-2013-86171 (JI29), MNHN IM-2013-86173 (JI41), MNHN IM-2013-86174 (JI19), MNHN IM-2013-86180 (JI23)
13 Atagema spongiosa MNHN IM-2013-86190 (JI09), MNHN IM-2013-86188 (JI33), MNHN IM-2013-86170 (JI02), MNHN IM-2013-86189 (JI30)
14 Carminodoris flammea CASIZ 177628
15 Diaulula greeleyi LACM 3016 (TL286)
16 Diaulula nayarita LACM 153353 (TL176)
17 Diaulula sandiegensis/odonoghuei CPIC 00911 (TL025), CPIC 01269 (TL268), CPIC 01073 (TL178), CPIC 01074 (TL179)
18 Discodoris boholiensis CASIZ 204802
19 Discodoris cebuensis CASIZ 185141
20 Discodoris cebuensis CASIZ 190761
21 Discodoris coerulescens CASIZ 182850
22 Doris kerguelenensis (H20)
23 Doris pseudoargus n/a
24 Hexabranchus sanguineus CPIC 00336 (JM70a)
25 Hoplodoris desmoparypha CASIZ 070066, CASIZ 309550
26 Hoplodoris rosans CASIZ 182837, CASIZ 182921
27 Jorunna artsdatabankia NTNU-VM 58891, ZMBN 125946, ZMBN 127749
28 Jorunna daoulasi sp. nov. MNHN IM-2013-86219 (JI22)
29 Jorunna hervei sp. nov. MNHN IM-2013-86225 (JI47), MNHN IM-2013-86226 (JI48)
30 Jorunna liviae MNCN15.05/200187, MNCN15.05/200188, MNCN15.05/200189, MNCN15.05/94693
31 Jorunna onubensis ZMBN 125474
32 Jorunna tomentosa CASIZ 175752, CASIZ 175753, CASIZ 176820, CASIZ 193035
33 Paradoris liturata CASIZ 177510, CASIZ 182756
34 Peltodoris atromaculata n/a
35 Montereina nobilis CASIZ 182223
36 Platydoris sanguinea CASIZ 177762
37 Rostanga byga CASIZ 181157
38 Rostanga calumus EED-Phy-934
39 Rostanga elandsia CASIZ 176110
40 Rostanga poddubetskaiae sp. nov. MNHN IM-2013-86208 (JI25), MNHN IM-2013-86213 (JI36), MNHN IM-2013-86206 (JI13), MNHN IM-2013-86203 (JI12), MNHN IM-2013-86214 (JI37), MNHN IM-2013-86215 (JI15), MNHN IM-2013-86200 (JI17), MNHN IM-2013-86212 (JI31), MNHN IM-2013-86216 (JI24), MNHN IM-2013-86209 (JI18), MNHN IM-2013-86218 (JI07), JI20 (MNHN IM-2013-86204), MNHN IM-2013-86217 (JI38), MNHN IM-2013-86202 (JI03), MNHN IM-2013-86205 (JI27), MNHN IM-2013-86207 (JI39), MNHN IM-2013-86201 (JI32), MNHN IM-2013-86199 (JI01)
41 Rostanga pulchra CASIZ 174490A
42 Sclerodoris dutertrei sp. nov. MNHN IM-2013-86193 (JI04), MNHN IM-2013-861924 (JI35), MNHN IM-2013-86195 (JI34), MNHN IM-2013-86196 (JI14)
43 Sclerodoris sp. CASIZ 182866
44 Sclerodoris sp. CASIZ 191525
45 Sclerodoris faninozi sp. nov. MNHN IM-2013-86198 (JI11)
46 Sclerodoris tuberculata CASIZ 190788, MNHN IM-2013-86197 (JI10)
47 Taringa sp. CASIZ 172039
48 Taringa telopia CASIZ 182933
49 Tayuva ketos n/a, CPIC 00654 (TL086)
50 Thordisa aff. albomacula CASIZ 181136, CASIZ 220322
51 Thordisa albomacula CASIZ 179590, CASIZ 182834
52 Thordisa bimaculata CASIZ 184516
53 Thordisa nieseni CASIZ 173057

There are consistent interspecific morphological differences among representative specimens in the clades recovered in the phylogenetic analyses, which also correspond to the species from the species delimitation analyses. These differences included aspects of internal morphology such as radular morphology and reproductive system differences that are discussed in the Systematics section below.

Systematics

Family Discodorididae Bergh, 1891

Atagema Gray, 1850

Atagema Gray 1842–50 [1850]: 104. Type species: Doris carinata Quoy & Gaimard, 1832 [= Atagema carinata (Quoy & Gaimard, 1832)], by monotypy.

Trippa Bergh 1877: 63. Type species: Trippa ornata Bergh, 1877 [= Atagema ornata Ehrenberg, 1831], by original designation.

Phlegmodoris Bergh 1878: 593. Type species: Phlegmodoris mephitica Bergh, 1878 [= Atagema spongiosa (Kelaart, 1858)], by subsequent designation by Valdés and Gosliner (2001).

Petelodoris Bergh, 1881: 227–228. Type species: Petelodoris triphylla Bergh, 1881 [?= Atagema ornata (Ehrenberg, 1831)], by monotypy.

Glossodoridiformia O’Donoghue, 1927: 87–89. Type species Glossodoridiformia alba O’Donoghue, 1927 [= Atagema alba O’Donoghue, 1927], by original designation.

Remarks

For an in-depth discussion of the characteristics of the genus Atagema and its synonyms see Valdés and Gosliner (2001).

Atagema spongiosa (Kelaart, 1858)

Figs 2A, B, 3A, 4A–C

Doris spongiosa Kelaart, 1858: 97–98. Type locality: Inner Harbor, Trincomalie, Ceylon [= Trincomalee, Sri Lanka].

Doris areolata Alder & Hancock, 1864: 119, pl. 30, figs 1–3 [non Doris areolata Stuwitz, 1835]. Type locality: Waltair, Madras Presidency [= Visakhapatnam, Andhra Pradesh], India.

Phlegmodoris mephitica Bergh, 1878: 594–597, pl. 66, figs 8–20. Type locality: Lapinig Island, Ubay, Philippines.

Trippa (Phlegmodoris) paagoumenei Risbec, 1928: 87–90, text fig. 15, pl. B, fig. 3, pl. 3, fig. 1. Type locality: Paagoumene, New Caledonia.

Material examined

Pointe Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.6'E), 0 m depth [Koumac 2.1 stn. KM100, rocky shore, rubble, sand, mud, seagrasses], 12 Sep 2018, 1 specimen 49 mm long (MNHN IM-2013-86170, isolate JI02). Koumac, New Caledonia (20°34.7'S, 164°16.5'E), 2–4 m depth [Koumac 2.1 stn. KR231, rocky bottom turning to mud, sponges, Halimeda], 25 Sep 2018, 1 specimen 27 mm long, dissected (MNHN IM-2013-86190, isolate JI09). Pointe Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.6'E), 0 m depth [Koumac 2.2 stn. KM100, rocky shore, rubble, sand, mud, seagrasses], 1 Mar 2019, 1 specimen 29 mm long (MNHN IM-2013-86188, isolate JI33). Koumac, New Caledonia (20°35.1'S, 164°16.3'E), 7–8 m depth [Koumac 2.2 stn. KR231], 1 Mar 2019, 1 specimen 6 mm long (MNHN IM-2013-86189, isolate JI30).

Description

Body oval, flattened, covered with large, rounded tubercles decreasing in size towards the mantle margin (Fig. 2A, B). A central, longitudinal ridge runs between the rhinophores and gill. A series of depressions on each side of the central ridge, generally decreasing in size towards the mantle margin. Entire dorsal surface, except for the depressions, covered with caryophyllidia. Branchial sheath composed of three large lobes; gill composed of five tripinnate branchial leaves, arranged horizontally in the living animal. Rhinophoral sheaths elevated; rhinophores long, lamellated, with 24 lamellae. Juvenile specimens with less marked dorsal tubercles (Fig. 2B). Body color opaque greyish brown in adult specimens, except for the depressions, which are dark brown to black (Fig. 2A); juveniles translucent gray (Fig. 2B). Rhinophores and branchial leaves are the same color as the dorsum.

Figure 2. 

Photographs of live animals of the genus Atagema Gray, 1850 A, B Atagema spongiosa (Kelaart, 1858), MNHN IM-2013-86188 on black background (A), MNHN IM-2013-86189 in situ (B) C, D Atagema kimberlyae sp. nov., MNHN IM-2013-86191 on black background (C), MNHN IM-2013-86191 in situ (D) E Atagema papillosa (Risbec, 1928), MNHN IM-2013-86192 on black background.

Reproductive system (Fig. 3A) with a long, narrow, simple ampulla that connects with the female gland complex and an elongated, convoluted prostate, with several folds. Prostate ~ 3× as long as the ampulla. The prostate narrows slightly before expanding into the long, simple, wide deferent duct. Deferent duct several times as wide as the prostate, but shorter in length. The penis is unarmed. The vagina is long and wide, as wide as the deferent duct, and connects directly to the small, oval bursa copulatrix. The small elongate seminal receptacle also connects to the bursa copulatrix next to the vaginal connection and the short uterine duct that enters the female gland complex. The bursa copulatrix is ~ 2× as large as the seminal receptacle.

Figure 3. 

Drawings of the reproductive systems of specimens of the genus Atagema Gray, 1850 A Atagema spongiosa (Kelaart, 1858), MNHN IM-2013-86190 B, C Atagema kimberlyae sp. nov., MNHN IM-2013-86191, general view (B), detail of the bursa copulatrix and seminal receptable (C) D, E Atagema papillosa (Risbec, 1928), MNHN IM-2013-86192, general view (D), detail of the bursa copulatrix and seminal receptable (E). Abbreviations: am, ampulla; bc, bursa copulatrix; dd, deferent duct; fg, female gland complex; pr, prostate; sr, seminal receptacle; vg, vagina.

Radular formula 18 × 35.0.35 in a 27-mm long specimen (MNHN IM-2013-86190). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a small cusp and lacking denticles (Fig. 4A, B). Innermost teeth very small in comparison to mid-laterals (Fig. 4A). The teeth increase in size suddenly towards the medial portion of the half-row (Fig. 4A). Outermost teeth small, decreasing in size gradually, and hamate (Fig. 4C). No jaw was observed, labial cuticle smooth.

Figure 4. 

SEM of the radula of specimens of the genus Atagema Gray, 1850 A–C Atagema spongiosa (Kelaart, 1858), MNHN IM-2013-86190, innermost teeth (A), mid-lateral teeth (B), outer lateral teeth (C) D–F Atagema kimberlyae sp. nov., MNHN IM-2013-86191, innermost teeth (D), mid-lateral teeth (E), outer lateral teeth (F) G–I Atagema papillosa (Risbec, 1928), MNHN IM-2013-86192, innermost teeth (G), mid-lateral teeth (H), outer lateral teeth (I).

Biology

Geographic range including the Indian and Western Pacific oceans (see synonymy and remarks). In New Caledonia it is found under rocks during the day in shallow water, from 0–8 m depth. The specimens examined were obtained by direct collection during low tide and/or SCUBA diving; they were highly cryptic on rocks covered with sponges and other encrusting organisms.

Remarks

Doris spongiosa Kelaart, 1858 was originally described from Sri Lanka and re-described by Valdés and Gosliner (2001), who transferred it to the genus Atagema, and recognized two synonyms, Doris areolata Alder & Hancock, 1864 and Phlegmodoris mephitica Bergh, 1878. This species is common across the tropical Indo-Pacific region and is well characterized and illustrated in modern literature (Wells and Bryce 1993; Yonow 2008; Hervé 2010; Gosliner et al. 2018; Nakano 2018). The specimens here examined from New Caledonia match the original description as well as the common usage of the name in the references above (see Hervé 2010).

Trippa (Phlegmodoris) paagoumenei Risbec, 1928 was originally described based on a single specimen collected in Paagoumene, northern New Caledonia, but it was later reported from Nouméa, southern New Caledonia (Risbec 1930, 1953). Risbec (1928) described T. paagoumenei as having a rather tough notum, dark violet in color, except towards the edges of the foot and the mantle, where it has a yellowish tint, and completely covered with purplish green, irregular tubercles. One of the specimens from Nouméa was unusual as it was covered by a bright green deposit of metallic appearance (Risbec 1953). Rudman (2002) considered T. paagoumenei a member of the genus Atagema and a synonym of A. spongiosa, and we concur with this opinion.

Atagema spongiosa is clearly distinct from other species of Atagema recognized as valid in the modern literature, such as Atagema ornata (Ehrenberg, 1831) [= Atagema intecta Kelaart, 1858] and Atagema carinata (Quoy & Gaimard, 1832), illustrated and/or redescribed in Willan and Coleman (1984), Valdés and Gosliner (2001), and Rudman (2005), as well as Atagema echinata (Pease, 1860), illustrated by Tibiriçá et al. (2017) and Gosliner et al. (2018). None of these species possesses the characteristic dorsal pattern of tubercles, depressions with a central ridge present in A. spongiosa. Atagema boucheti Valdés & Gosliner, 2001, described based in a preserved specimen from New Caledonia deep water (405–411 m depth), is characterized by having the dorsum covered by large, irregularly scattered tubercles, not aligned to form ridges. Although the live color of this species is unknown, the external morphology is clearly different from other species of Atagema including Atagema spongiosa (see Valdés and Gosliner 2001).

Atagema papillosa (Risbec, 1928)

Figs 2E, 3D, E, 4G–I

Phlegmodoris papillosa Risbec, 1928: 90–91, pl. 8, fig. 2. Type locality: Nouméa, New Caledonia [not indicated in the original description], see Risbec (1953).

?Trippa albata Burn, 1962a: 101–102, text fig. 5. Type locality: Sunderland Bay, Phillip Island, Victoria, Australia.

?Atagema sp. 11: Gosliner et al. 2018: 116.

Material examined

Koumac, New Caledonia (20°35.6'S, 164°16.2'E), 4–6 m depth [Koumac 2.3 stn. KD510, coral debris and coarse sand], 30 Oct 2019, 1 specimen 11 mm long, dissected (MNHN IM-2013-86192, isolate JI42).

Description

Body oval, flattened, covered with a complex network of small ridges with two levels of organization (Fig. 2E). The largest ridges cover the entire body, leaving some depressions in between. Smaller ridges occur in the depressions dividing them into smaller fragments. Entire dorsal surface, except for the depressions, covered with caryophyllidia. Branchial sheath composed of three large lobes; gill composed of five tripinnate branchial leaves, arranged horizontally in the living animal. Rhinophoral sheaths elevated; rhinophores long, lamellated, with 16 lamellae. Body color opaque grey with scattered yellow spots; depressions with gray ridges dividing dark grey to black fragments. Gill leaves are the same color as the dorsum. Rhinophores greyish to yellowish cream.

Reproductive system (Fig. 3D, E) with a large, folded ampulla that connects with the female gland complex and an elongate prostate. The prostate is much longer and ~ 2× as narrow as the ampulla. The prostate narrows substantially into a long, folded tube before expanding into the short, curved, wide deferent duct. The deferent duct is ~ 2× as narrow as the prostate. The penis is unarmed. The vagina is long and narrow, slightly narrower than the deferent duct, and connects directly to the oval bursa copulatrix. The elongate seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the short uterine duct, which enters the female gland complex. The bursa copulatrix is several times as large as the seminal receptacle (Fig. 3E).

Radular formula 13 × 19.0.19 in a 11-mm long specimen (MNHN IM-2013-86192). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a small cusp and lacking denticles (Fig. 4G–I). Innermost teeth very small in comparison to mid-laterals (Fig. 4G), elongate, with an inconspicuous secondary cusp mid-length. The teeth increase in size suddenly towards the medial portion of the half-row (Fig. 4G). Outermost teeth small, decreasing in size gradually, and hamate (Fig. 4I). No jaw was observed, labial cuticle smooth.

Biology

Possibly a New Caledonia endemic, rare, 4–6 m depth. The single specimen was collected by dredging on coral debris and coarse sand bottoms.

Remarks

Phlegmodoris papillosa Risbec, 1928 was originally described based on a single specimen collected in Nouméa, New Caledonia, with a short description and an illustration of the live animal. Risbec (1928) described the species as having the notum covered with large papillae and bearing spots with the appearance of black ocelli standing out against a yellowish background. Risbec (1928) also mentioned that the elongated, perfoliate rhinophores of P. papillosa are retractile in funnel-shaped sheaths with a well-marked ocelliform spotted papilla; and the gill is retractile in a cavity with a star-shaped orifice. The specimens here examined closely resemble the original description of P. papillosa with the exception that the notum is grey, not yellowish.

Atagema albata (Burn, 1962a) is a similar species, originally described as Trippa albata, based on three specimens collected in Victoria, Australia. The specimens were described as pure white, sometimes with cream pigment, and characterized by having a soft, broad, flat body, with the mantle covered with low caryophyllidia, all similar in size, and with a mid-dorsal crest, extending from between the rhinophores to the branchial cavity. Burn (1962a) also described the branchial cavity as having an irregular outline and the rhinophores as perfoliate, with small, raised sheaths. Burn (1962a) compared T. albata with the New South Wales species T. intecta Kelaart, 1859 (= Goniodoris erinaceus Angas, 1864), which according to Burn (1962a) is usually much larger than A. albata and is of an ashy-brown color. With the available information is it not possible to confirm if A. albata and A. papillosa are the same species, and sequence data from A. albata would be needed to confirm this potential synonymy.

Finally, the specimen from the Philippines illustrated by Gosliner et al. (2018) as Atagema sp. 13 presents a similar external appearance and could be the same species. Examination of specimens is needed to confirm this possibility.

Atagema kimberlyae sp. nov.

https://zoobank.org/FFE42C3A-F0E3-486D-9376-DC999DE7F241
Figs 2C, D, 3B, C, 4D–F

Atagema sp. 2: Hervé 2010: 190.

Type material

Holotype : Koumac, New Caledonia (20°35.5'S, 164°16.4'E), 5 m depth [Koumac 2.1 stn. KR223, patch of sponges, small bits of sedimented coral, coarse sand and mud with algae], 19 Sep 2018, 20 mm long, dissected (MNHN IM-2013-86191, isolate JI43).

Description

Body oval, flattened, covered with small, irregular tubercles and short ridges decreasing in size towards the mantle margin (Fig. 2C, D). A central, longitudinal area devoid of tubercles or ridges runs between the rhinophores and gill. A series of depressions on each side of the central ridge, generally decreasing in size towards the mantle margin. Entire dorsal surface, except for the depressions, covered with caryophyllidia. Branchial sheath composed of three large lobes; gill composed of five tripinnate branchial leaves, arranged horizontally in the living animal. Rhinophoral sheaths elevated; rhinophores long, lamellated, with 20 lamellae. Body color opaque greyish brown, with pale brown pigment mainly on top of the tubercles and ridges and scattered opaque white pigment; depressions dark brown to black (Fig. 2C). Rhinophores and branchial leaves are the same color as the dorsum.

Reproductive system (Fig. 3B, C) with a short, wide, simple ampulla that connects with the female gland complex and a convoluted prostate. The prostate has several folds and is approximately as wide as the ampulla. The prostate narrows slightly into a curved duct before expanding into the long, ovoid, wide deferent duct. At its widest point, the deferent duct is slightly wider than the prostate. The penis is unarmed. The vagina is long and narrow and connects directly to the spherical bursa copulatrix. The vagina is approximately as wide as the deferent duct. The small elongate seminal receptacle also connects to the bursa copulatrix near the vaginal connection and the short uterine duct that enters the female gland complex. The bursa copulatrix is several times larger than the seminal receptacle (Fig. 3C).

Radular formula 15 × 20.0.20 in a 20-mm long specimen (MNHN IM-2013-86191). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a small cusp and lacking denticles (Fig. 4D–F). Innermost teeth very small in comparison to mid-laterals (Fig. 4D), elongate, with an inconspicuous secondary cusp mid-length. The teeth increase in size suddenly towards the medial portion of the half-row (Fig. 4E). Outermost teeth small, decreasing in size gradually, and hamate (Fig. 4F). No jaw was observed, labial cuticle smooth.

Biology

Possibly a New Caledonia endemic, rare, 5 m depth. The single specimen was obtained while SCUBA diving by direct collection on an unidentified sponge on which it was highly cryptic.

Etymology

This species is named after Kimberly García Mendez, who participated in two of the Koumac expeditions, collecting a number of specimens and helping enormously with the processing and photographing of samples.

Remarks

Atagema kimberlyae sp. nov. is assigned to the genus Atagema for two reasons, 1) the molecular phylogenetic analysis places the specimens sequenced in a clade containing A. spongiosa, a well stablished member of this genus (see above); 2) the morphological characteristics of this new species are consistent with the diagnosis of the genus provided by Valdés and Gosliner (2001), including a flexible body with series of tubercles all covered with caryophyllidia and depressions, the anterior border of the branchial sheath composed of three lobes and the gill leaves arranged horizontally; furthermore the prostate is tubular, with a single portion, the penis and vagina are unarmed, the labial cuticle smooth, and all radular teeth are hamate and smooth.

Atagema kimberlyae sp. nov. is morphologically similar to Atagema spongiosa (described above), particularly to the juvenile specimens, but is genetically distinct. Also, it lacks the distinctive dorsal ridge of A. spongiosa and presents a number of anatomical differences, including a comparatively much shorter and wider ampulla, a wider prostate, a rounded bursa copulatrix instead of oval, and comparatively larger innermost lateral teeth. A review of the literature reveals that no other described Indo-Pacific species of Atagema are morphologically similar to A. kimberlyae sp. nov., hence it is described as new.

The geographic range of Atagema kimberlyae sp. nov. is close to that of Atagema molesta (Miller, 1989 as Trippa molesta), introduced based on a single specimen collected from Te Hāwere-a-Maki (Goat Island), New Zealand. Miller (1989) described and illustrated the holotype, which differs from A. kimberlyae sp. nov. in several regards, including the more complex dorsal pattern of tubercles and ridges present in A. molesta, giving the animal a spikier appearance, and the reproductive system, which has a much larger deferent duct and a shorter prostate in A. kimberlyae sp. nov. While the radular morphology of the two species is similar, the radular formula is not, 23 × 32.0.32 in a 12-mm specimen of A. molesta versus 15 × 20.0.20 in a 20-mm long specimen of A. kimberlyae sp. nov.

Based on the species delimitation analysis presented here, A. kimberlyae sp. nov. is closely related but genetically distinct from specimens identified as Atagema cf. osseosa and Atagema notacristata whose sequences are deposited in GenBank.

Atagema sobanovae sp. nov.

https://zoobank.org/C296974E-92C6-4F7C-8E4A-ABF61D48F896
Figs 5, 6, 7

?Atagema sp. 9: Gosliner et al. 2018: 116.

Type material

Holotype : Koumac, New Caledonia (20°35.6'S, 164°16.3'E), 3 m depth [Koumac 2.1 stn. KR230], 28 Sep 2018, 22 mm long (MNHN IM-2013-86211, isolate JI16).

Other material examined

Cap Deverd, Koumac, New Caledonia (20°46.2'S, 164°22.6'E), 5 m [Koumac 2.1 stn. KR213], 12 Sep 2018, 1 specimen 13 mm long (MNHN IM-2013-86178, isolate JI06). Koumac, New Caledonia (20°39.6'S, 164°16.2'E), 6 m depth [Koumac 2.1 stn. KR229], 27 Sep 2018, 1 specimen 8 mm long (MNHN IM-2013-86175, isolate JI28). Koumac, New Caledonia (20°35.6'S, 164°16.3'E), 3 m depth [Koumac 2.1 stn. KR230], 28 Sep 2018, 1 specimen 17 mm long, dissected (MNHN IM-2013-86180, isolate JI23); 1 specimen 18 mm long, dissected (MNHN IM-2013-86179, isolate JI21). Koumac, New Caledonia (20°35.1'S, 164°16.3'E), 7 m depth [Koumac 2.1 stn. KR409, muddy bottom with solitary soft and hard corals and hydroids], 28 Sep 2018, 1 specimen 8 mm long (MNHN IM-2013-86229). Koumac, New Caledonia (20°35.1'S, 164°16.3'E), 3 m [Koumac 2.2 stn. KR231], 1 Mar 2019, 1 specimen 9 mm long (MNHN IM-2013-86176, isolate JI44). Koumac, New Caledonia (20°37.3'S, 164°18'E), 6 m depth [Koumac 2.3 stn. KD522, grey sand with Caulerpa and Halimeda], 2 Nov 2019, 1 specimen 10 mm long (MNHN IM-2013-86174, isolate JI19). Koumac, New Caledonia (20°34.3'S, 164°13.5'E), 1–10 m depth [Koumac 2.3 stn. KR907, sanded slab with gorgonians, scattered seagrass, and Caulerpa; channel drop-off with gorgonians], 7 Nov 2019, 1 specimen 7 mm long (MNHN IM-2013-86173, isolate JI41). Koumac, New Caledonia (20°34.4'S, 164°13.8'E), 8 m depth [Koumac 2.3 stn. KR913], 14 Nov 2019, 1 specimen 11 mm long (MNHN IM-2013-86171, isolate JI29); 1 specimen 10 mm long (MNHN IM-2013-86172, isolate JI46). Koumac, New Caledonia (20°35.1'S, 164°16.3'E), 7 m depth [Koumac 2.3 stn. KR1019, “fond de vase” with Caulerpa and sponges], 4 Nov 2019, 1 specimen 28 mm long (MNHN IM-2013-86181, isolate JI05); 1 specimen 22 mm long, dissected (MNHN IM-2013-86187, isolate JI08); 1 specimen 9 mm long (MNHN IM-2013-86177, isolate JI45).

Description

Body oval, elevated, completely covered with a dense, complex network of delicate ridges (Fig. 5). Large caryophyllidia present at the points where ridges meet. A series of small depressions free of ridges and caryophyllidia present on each side of the mantle. A single, elevate dorsal hump present on the center of the dorsum, not visible in juvenile specimens (Fig. 5E). Branchial sheath composed of three lobes; gill composed of five tripinnate branchial leaves, arranged horizontally in the living animal. Rhinophoral sheaths elevated; rhinophores long, lamellated, with 8–10 lamellae. Body color opaque creamy grey, depressions a bit darker. Rhinophores and branchial leaves are the same color as the dorsum.

Figure 5. 

Photographs of live animals of Atagema sobanovae sp. nov. A, B MNHN IM-2013-86180, on black background (A), in situ (B) C, D holotype (MNHN IM-2013-86211), on black background (A), in situ (B) E MNHN IM-2013-86229 juvenile specimen on black background.

Reproductive system (Fig. 6) with a short, convoluted ampulla that connects with the female gland complex and an elongated prostate. The prostate is as long as the ampulla and it narrows slightly into an elongate duct before expanding into the short, simple, deferent duct. The penis is unarmed. The vagina is short and wide, approximately as wide as the deferent duct, and connects directly to the oval bursa copulatrix. The oval seminal receptacle also connects to the bursa copulatrix next to the vaginal opening and the short uterine duct that enters the female gland complex. The bursa copulatrix is slightly larger than the seminal receptable.

Figure 6. 

Drawing of the reproductive system of Atagema sobanovae sp. nov., MNHN IM-2013-86180. Abbreviations: am, ampulla; bc, bursa copulatrix; dd, deferent duct; fg, female gland complex; pr, prostate; sr, seminal receptacle; vg, vagina.

Radular formula 22 × 35.0.35 in an 18-mm long specimen (MNHN IM-2013-86179) and 17 × 34.0.34 in a 22-mm long specimen (MNHN IM-2013-86187). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a small cusp and lacking denticles (Fig. 7A, B). Innermost teeth very small in comparison to mid-laterals (Fig. 7A). The teeth increase in size gradually towards the medial portion of the half-row (Fig. 7A). Outermost teeth small, decreasing in size gradually, and hamate (Fig. 7C). No jaw was observed, labial cuticle smooth.

Figure 7. 

SEM of the radula of specimens of Atagema sobanovae sp. nov., MNHN IM-2013-86179, innermost teeth (A), mid-lateral teeth (B), outer lateral teeth (C).

Biology

This species could be widespread in the Western Pacific (see remarks). Found in shallow water (1–10 m depth). The specimens were exclusively collected on an unidentified species of grey sponge inhabiting the surface of scallops; the nudibranchs were highly cryptic on the sponge and often found buried in the sponge tissue. Few specimens were obtained by direct collection while SCUBA diving but more of them were found in the lab while searching for crustaceans associated with the sponges.

Etymology

This species is named after Anna Šobáňová, crustacean expert who originally discovered this species in the field while looking for crustaceans living in sponges.

Remarks

Atagema sobanovae sp. nov. is assigned to the genus because of its position in the molecular phylogenetic trees, in a clade containing other species of Atagema such as A. spongiosa and A. cf. osseosa. Also, the morphological characteristics of this new species are consistent with the diagnosis of the genus by Valdés and Gosliner (2001). Atagema sobanovae sp. nov. has a flexible body with series of dorsal ridges and a central conspicuous tubercle, all covered with caryophyllidia, the anterior border of the branchial sheath is composed of three lobes and the gill is arranged horizontally; the prostate is tubular, with a single portion, the penis and vagina are unarmed; the labial cuticle smooth and all radular teeth are hamate and smooth.

A review of the literature shows that no other described species of Atagema possesses the external characteristics of A. sobanovae sp. nov. The only other tropical Indo-Pacific species with a uniform color is Atagema carinata (Quoy & Gaimard, 1832), which was described from the coast of Thames, New Zealand, as yellowish white with a dorsal longitudinal ridge between the rhinophores and the gill. The illustration provided by Quoy and Gaimard (1832–1833: pl. 16, figs 10–14) represents an animal with a distinct dorsal ridge very different from the complex dorsal pattern of A. sobanovae sp. nov. with depressions, ridges, and a central tubercle. The specimens of A. carinata described and illustrated by Rudman (2005) are consistent with the original description.

A specimen from the Philippines illustrated by Gosliner et al. (2018) as Atagema sp. 9 could belong to A. sobanovae sp. nov. but this needs anatomical and molecular confirmation.

Jorunna Bergh, 1876

Kentrodoris Bergh, 1876: 413. Type species: Kentrodoris rubescens Bergh, 1876 [= Jorunna rubescens Bergh, 1876], by subsequent designation by Ev. Marcus (1976).

Jorunna Bergh, 1876: 414. Type species: Doris johnstoni Alder & Hancock, 1845 [= Jorunna tomentosa (Cuvier, 1804)], by monotypy.

Audura Bergh, 1878: 567–568. Type species: Audura maima Bergh, 1878 [= Jorunna maima (Bergh, 1878)], by monotypy.

Centrodoris P. Fischer 1880–1887 [1883]: 522 (unjustified emendation for Kentrodoris Bergh, 1876).

Awuka Er. Marcus, 1955: 155–156. Type species Awuka spazzola Er. Marcus, 1955 [= Jorunna spazzola (Er. Marcus, 1955)], by original designation.

Remarks

For an in-depth discussion of the characteristics of the genus Jorunna and its synonyms see Camacho-García and Gosliner (2008).

Jorunna daoulasi sp. nov.

https://zoobank.org/0D41E0FA-826A-4761-BB7B-B71CE0B2E97E
Figs 8A–C, 9A, 10A, B

?Jorunna sp. 10: Gosliner et al. 2018: 122.

?Rostanga sp. 4: Nakano 2018: 263.

Type material

Holotype : In front of the harbor, Koumac, New Caledonia (20°35.3'S, 164°16.4'E), 6 m depth [Koumac 2.1 stn. KR220], 17 Nov 2018, 12 mm long, (MNHN IM-2013-86230).

Other material examined

In front of the harbor, Koumac, New Caledonia (20°35.3'S, 164°16.4'E), 6 m depth [Koumac 2.1 stn. KR220], 17 Nov 2018, 1 specimen 24 mm long, dissected (MNHN IM-2013-86220). Koumac, New Caledonia (20°35.2'S, 164°16.3'E), 6 m depth [Koumac 2.3 stn. KR886], 21 Nov 2019, 1 specimen 27 mm long, dissected (MNHN IM-2013-86219, isolate JI22).

Description

Body oval, narrow, elongate, completely covered with numerous caryophyllidia (Fig. 8A–C). Branchial and rhinophoral sheaths low, simple, circular; gill composed of nine short, tripinnate branchial leaves, imbricated, arranged upright, with the apices close to each other in the living animal. Rhinophores short, lamellated, with eight or nine lamellae. Body color grey, with a complex network of white lines of different thicknesses; in some specimens some of the lines are very thick and contain darker areas (Fig. 8A), whereas in others thicker lines form the main network and thinner lines form a secondary network (Fig. 8) and in others all lines are approximately the same thickness (Fig. 8B). Rhinophores and branchial leaves are the same color as the dorsum but the rhinophoral lamellae and in some cases the gill lamellae are white.

Figure 8. 

Photographs of live animals of the genus Jorunna Bergh, 1876 A–C Jorunna daoulasi sp. nov., MNHN IM-2013-86219 on black background (A), MNHN IM-2013-86220 in situ (B), Holotype (MNHN IM-2013-86230) in situ (C) D–F Jorunna hervei sp. nov., MNHN IM-2013-86228 on black background (D), MNHN IM-2013-86224 and Holotype MNHN IM-2013-86225 in situ with egg mass (E), MNHN IM-2013-86226 in situ with egg mass (F).

Reproductive system (Fig. 9A) with a long, narrow, curved ampulla that connects with the female gland complex and an elongate prostate. The prostate is as wide as the ampulla but narrows substantially before expanding into the short, curved, narrow deferent duct. The deferent duct is much narrower than the prostate. The penis is unarmed. The vagina is very elongate and wide distally, several times wider than the deferent duct, narrowing considerably proximally and connecting directly to the irregular bursa copulatrix. The oval seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the short uterine duct that enters the female gland complex. The bursa copulatrix is ~ 3× as large as the seminal receptable. A large accessory gland connects to a narrow and convoluted duct that opens into the genital atrium, where a curved, sharp stylet is located.

Figure 9. 

Drawings of the reproductive systems of specimens of the genus Jorunna Bergh, 1876 A Jorunna daoulasi sp. nov., MNHN IM-2013-86219 B Jorunna hervei sp. nov., MNHN IM-2013-86226. Abbreviations: ag, accessory gland; am, ampulla; bc, bursa copulatrix; dd, deferent duct; fg, female gland complex; pr, prostate; sr, seminal receptacle; st, stylet; vg, vagina.

Radular formula 24 × n.0.n in a 26-mm long specimen (MNHN IM-2013-86220) and 25 × n.0.n in a 27-mm long specimen (MNHN IM-2013-86219). Rachidian teeth absent. Innermost lateral teeth wide, having a short cusp with four or five irregular denticles (Fig. 10A). Mid-lateral teeth hamate, lacking denticles (Fig. 10A). The teeth increase in size gradually towards the distal portion of the half-row (Fig. 10B). Outermost teeth very elongate, longer than mid-lateral teeth, with several elongate apical denticles (Fig. 10B). No jaws ware observed.

Figure 10. 

SEM of the radula of specimens of the genus Jorunna Bergh, 1876 A, B Jorunna daoulasi sp. nov., MNHN IM-2013-86220, innermost teeth (A), outer lateral teeth (B) C–E Jorunna hervei sp. nov., MNHN IM-2013-86224, innermost teeth (C), mid-lateral teeth (D), outer lateral teeth (E).

Biology

Range includes New Caledonia and possibly Papua New Guinea and Japan (see Remarks section below); uncommon, found at ~ 6 m depth on an unidentified grey sponge on which it is highly cryptic. All the specimens were found directly on the sponges while SCUBA diving.

Etymology

This species is named after Alain Daoulas, outstanding collector and naturalist, who participated in two of the Koumac expeditions, collecting a number of important specimens.

Remarks

Jorunna daoulasi sp. nov. is placed in the genus Jorunna because it fits morphologically within the diagnoses of the genus provided by Valdés and Gosliner (2001) and Camacho-García and Gosliner (2008). Specifically, J. daoulasi sp. nov. has a soft mantle covered with long caryophyllidia, the radular teeth are hamate, and the reproductive system has an accessory gland and a copulatory stylet. Finally, in the molecular phylogenetic analyses, J. daoulasi sp. nov. is a member of a well-supported clade containing other members of Jorunna.

Camacho-García and Gosliner (2008) provided a comprehensive revision and illustrations of the valid species of the genus Jorunna, including all the Indo-Pacific taxa described to date. None of the species included in Camacho-García and Gosliner’s (2008) monograph have a similar color pattern and morphology to J. daoulasi sp. nov. Since then, several additional new species have been described from the Atlantic Ocean (Edmunds 2011; Alvim and Pimenta 2013; Ortea et al. 2014; Ortea and Moro 2016; Neuhaus et al. 2021) and the Indian Ocean (Tibiriçá et al. 2023), but they are also morphologically and/or genetically different from J. daoulasi sp. nov. The most similar species to J. daoulasi sp. nov. in external morphology are Jorunna sp. 10 from Papua New Guinea illustrated by Gosliner et al. (2018) and Rostanga sp. 4 from Japan illustrated by Nakano (2018), which have a very similar body shape and color and could represent the same species.

Jorunna hervei sp. nov.

https://zoobank.org/DAD18B3C-3AFA-428E-909E-71309CE1ACB3
Figs 8D–F, 9B, 10C–E

Type material

Holotype : Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.5'E), 7 m depth [Koumac 2.1 stn. KR868, rock, sponges, algae including Halimeda], 26 Sep 2018, 1 specimen 24 mm long (MNHN IM-2013-86225, isolate JI47)

Other material examined

Koumac, New Caledonia (20°35.6'S, 164°16.3'E), 3 m depth [Koumac 2.1 stn. KR230], 28 Sep 2018, 1 specimen 11 mm long (MNHN IM-2013-86221). Koumac, New Caledonia (20°35.1'S, 164°16.3'E), 3 m depth [Koumac 2.1 stn. KR231], 29 Sep 2018, 1 specimen 21 mm long, dissected (MNHN IM-2013-86222). Koumac, New Caledonia (20°35.1'S, 164°16.2'E), 8 m depth [Koumac 2.1 stn. KR410, sponge bottom], 29 Sep 2018, 1 specimen 14 mm long (MNHN IM-2013-86223). Pandop Point Reef, Koumac, New Caledonia (20°35.2'S, 164°16.3'E), 6 m depth [Koumac 2.1 stn. KR859, sandy-muddy bottom with sponges, Caulerpa], 17 Sep 2018, 1 specimen 25 mm long, dissected (MNHN IM-2013-86226, isolate JI48); 1 specimen 14 mm long (MNHN IM-2013-86227). Pointe de Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.5'E), 7 m depth [Koumac 2.1 stn. KR868, rock, sponges, algae including Halimeda], 26 Sep 2018, 1 specimen 22 mm long (MNHN IM-2013-86224). Koumac, New Caledonia (20°32.9'S, 164°16.8'E), 5 m depth [Koumac 2.3 stn. KR917], 19 Nov 2019, 1 specimen 16 mm long (MNHN IM-2013-86228).

Description

Body oval, flattened, completely covered with numerous caryophyllidia (Fig. 8D–F). Branchial and rhinophoral sheaths low, simple, circular; gill composed of nine short, tripinnate branchial leaves, slightly imbricated, arranged fully upright in the living animal. Rhinophores short, lamellated with elongate apices, seven or eight lamellae. Body color variable from pale brown to grey, with numerous irregular dark patches, surrounded by white pigment (Fig. 8E). Rhinophores and branchial leaves are the same color as the dorsum.

Reproductive system (Fig. 9B) with an elongate, curved ampulla that connects with the female gland complex and an elongate prostate with a single fold. The prostate is as wide as the ampulla but narrows substantially into a long tube before expanding slightly into the short, curved, narrow deferent duct. The penis is unarmed. The vagina is narrow, as wide as the deferent duct, and very elongate, connecting directly to the oval bursa copulatrix. The oval seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the long uterine duct that enters the female gland complex. The bursa copulatrix is many times larger than the seminal receptacle. A large accessory gland connects to a wide duct that opens into the genital atrium, where a sharp, curved stylet is located.

Radular formula 24 × n.0.n, in a 21-mm long specimen (MNHN IM-2013-86222), 28 × n.0.n in a 22-mm long specimen (MNHN IM-2013-86224), and 30 × n.0.n in a 25-mm long specimen (MNHN IM-2013-86226). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a long cusp and lacking denticles (Fig. 10C–E). Innermost teeth smaller than mid-laterals (Fig. 10C). The teeth increase in size gradually towards the medial portion of the half-row (Fig. 10D). Outermost teeth very elongate, longer than mid-lateral teeth, increasing in size gradually, and hamate (Fig. 10E). No jaws were observed.

Biology

The pale brown egg mass is a highly coiled ribbon with ca. seven tightly packed whorls with a wavy upper edge (Fig. 8E). Eggs are ~ 105 µm in diameter. The geographic range includes New Caledonia and could be an endemic species; uncommon, found at 3–8 m depth on an unidentified brownish grey sponge on which is highly cryptic. All the specimens were collected directly from the sponges while SCUBA diving.

Etymology

This species is named after Jean-François Hervé, pioneer in the study of the sea slugs of New Caledonia and excellent collector; he participated in two of the Koumac expeditions, finding numerous specimens.

Remarks

As in the case of Jorunna daoulasi sp. nov., Jorunna hervei sp. nov. is placed in the genus Jorunna because it fits morphologically within the diagnoses of the genus provided by Valdés and Gosliner (2001) and Camacho-García and Gosliner (2008). Jorunna hervei sp. nov. has a soft mantle covered with long caryophyllidia, the radular teeth are hamate, and the reproductive system has an accessory gland and a copulatory stylet, all of which are characteristics of Jorunna. Furthermore, in the molecular phylogenetic analyses, Jorunna hervei sp. nov. is sister to J. daoulasi sp. nov. as well as a member of a well-supported clade containing other members of Jorunna.

Jorunna hervei sp. nov. differs from Jorunna daoulasi sp. nov. in several regards. Externally, J. hervei sp. nov. is less elongate than J. daoulasi sp. nov. and lacks the network of white pigment; instead it has numerous irregular dark patches, in some specimens surrounded by white pigment. The reproductive system of J. hervei sp. nov. is similar to that of J. daoulasi sp. nov., but the accessory gland is comparatively smaller, the bursa copulatrix is much larger in comparison to the seminal receptable, and the deferent duct is shorter in comparison to the vagina. The main anatomical difference between these two species is the radular morphology, while Jorunna hervei sp. nov. has inner and mid-lateral teeth hamate, having a long cusp and lacking denticles, in J. daoulasi sp. nov. the innermost lateral teeth are wide, having a short cusp with four or five irregular denticles. Finally, the ABGD analysis recovered J. hervei sp. nov. and J. daoulasi sp. nov. as distinct species.

Jorunna liviae Tibiriçá, Strömvoll & Cervera, 2023 recently described from Mozambique (Tibiriçá et al. 2023) is sister to J. hervei sp. nov. and is morphologically similar but differs in several important respects. First of all, the species delimitation analysis recovered J. hervei sp. nov. and Jorunna liviae as different species. Additionally, the body of J. liviae appears to be narrower and more elongate than that of J. hervei sp. nov. More importantly, the outermost radular teeth of J. liviae contain multiple elongate denticles, which are absent in all specimens examined of J. hervei sp. nov. Also, the prostate of J. liviae is flattened, whereas the prostate of J. hervei sp. nov. is tubular an elongate, and the accessory gland appears to be comparatively much larger in J. liviae than in J. hervei sp. nov. although is it variable in size (Tibiriçá et al. 2023). Finally, the eggs of J. liviae are white, whereas they are pale brown in J. hervei sp. nov. It is clear that these two species are similar but distinct.

A review of the literature does not reveal any other species morphologically similar to J. hervei sp. nov. Rostanga sp. 7 in Gosliner et al. (2018) has some superficial resemblance but there are some obvious differences, including the background color, grey in J. hervei, pink in Rostanga sp. 7, and the egg mass, having one or two loosely packed whorls with ochre, large eggs in Rostanga sp. 7, versus seven tightly packed whorls with pale brown eggs in J. hervei.

Rostanga Bergh, 1879

Rostanga Bergh, 1879: 353–354. Type species: Doris coccinea Forbes in Alder & Hancock, 1848 [= Rostanga rubra (Risso, 1818)], by original designation.

Boreodoris Odhner, 1939: 31–33. Type species: Boreodoris setidens Odhner, 1939 [= Rostanga setidens (Odhner, 1939)], by monotypy.

Rhabdochila P. Fischer, 1880–1887 [1883]: 521. Type species Doris coccinea Forbes in Alder & Hancock, 1848 [= Rostanga rubra (Risso, 1818)], by subsequent designation by Iredale and O’Donoghue (1923).

Remarks

For an in-depth discussion of the characteristics of the genus Rostanga and its synonyms see Rudman and Avern (1989) and Valdés and Gosliner (2001).

Rostanga poddubetskaiae sp. nov.

https://zoobank.org/EF949405-58D8-4D48-AD09-1CB3CE3993F5
Figs 11, 12, 13

Type material

Holotype : Anse de Koumac, Koumac, New Caledonia (20°34'S, 164°16'E), 4 m depth [Koumac 2.1 stn. KR206], 5 Sep 2018, 1 specimen 23 mm long (MNHN IM-2013-86199, isolate JI01).

Other material examined

Anse de Koumac, Koumac, New Caledonia (20°34'S, 164°16'E), 4 m depth [Koumac 2.1 stn. KR206], 5 Sep 2018, 1 specimen 25 mm long (MNHN IM-2013-86200, isolate JI17); 1 specimen 12 mm long (MNHN IM-2013-86201, isolate JI32); 1 specimen 26 mm long, dissected (MNHN IM-2013-86202, isolate JI03); 1 specimen 19 mm long, dissected (MNHN IM-2013-86203, isolate JI12); 1 specimen 16 mm long, dissected (MNHN IM-2013-86204, isolate JI20). Cap Deverd, Koumac, New Caledonia (20°46.2'S, 164°22.6'E), 5 m depth [Koumac 2.1 stn. KR213], 29 Sep 2018, 1 specimen 26 mm long, dissected (MNHN IM-2013-86205, isolate JI27); 1 specimen 28 mm long, dissected (MNHN IM-2013-86206, isolate JI13). Anse de Koumac, Koumac, New Caledonia (20°34.6'S, 164°16.1'E), 5 m depth [Koumac 2.1 stn. KR219], 17 Sep 2018, 1 specimen 12 mm long (MNHN IM-2013-86207, isolate JI39); 1 specimen 23 mm long, dissected (MNHN IM-2013-86208, isolate JI25); 1 specimen 26 mm long (MNHN IM-2013-86209, isolate JI18); 1 specimen 17 mm long (MNHN IM-2013-86210, isolate JI40). Koumac, New Caledonia (20°35.6'S, 164°16.3'E), 3 m depth [Koumac 2.2 stn. KR230], 2 Mar 2019, 1 specimen 20 mm long (MNHN IM-2013-86213, isolate JI36); 2 Mar 2019, 1 specimen 21 mm long (MNHN IM-2013-86214, isolate JI37); 3 Mar 2019, 1 specimen 20 mm long (MNHN IM-2013-86212, isolate JI31). Pointe de Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.5'E), 7 m depth [Koumac 2.1 stn. KR868], 26 Sep 2018, 1 specimen 26 mm long (MNHN IM-2013-86215, isolate JI15); 1 specimen 24 mm long (MNHN IM-2013-86216, isolate JI24); 1 specimen 14 mm long (MNHN IM-2013-86217, isolate JI38). Koumac, New Caledonia (20°33.7'S, 164°13.1'E), 12 m depth [Koumac 2.3 stn. KR206], 3 Nov 2019, 1 specimen 19 mm long (MNHN IM-2013-86218, isolate JI07).

Description

Body oval, elongate, completely covered with numerous caryophyllidia (Fig. 11). Branchial and rhinophoral sheaths low, simple, circular; gill composed of seven wide, tripinnate branchial leaves, extended laterally, lying on the dorsum in the living animal. A low, irregular, inconspicuous ridge runs between the rhinophores and the gill, not clearly visible in all specimens. Rhinophores very elongate, almost conical, lamellated, with 15 or 16 lamellae. Body color pinkish to orange, with irregular darker patches all over the dorsum. Rhinophores reddish; branchial leaves the same color as the dorsum.

Figure 11. 

Photographs of live animals of Rostanga poddubetskaiae sp. nov. A holotype MNHN IM-2013-86199 on black background B holotype (MNHN IM-2013-86199) and MNHN IM-2013-86217 in situ with egg masses C MNHN IM-2013-86205 in situ D MNHN IM-2013-86216 and MNHN IM-2013-86217 in situ E MNHN IM-2013-86209 on black background.

Reproductive system (Fig. 12) with a long, narrow, curved ampulla that connects with the female gland complex and an irregular, elongate prostate. The prostate is wider than the ampulla, but it narrows substantially into a long, folded tube, before expanding into the short, wide deferent duct. The penis is unarmed. The vagina is elongate, several times narrower than the deferent duct, connecting directly to the large, oval bursa copulatrix. The smaller, elongate seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the short uterine duct that enters the female gland complex. The bursa copulatrix is several times larger than the seminal receptacle.

Figure 12. 

Drawing of the reproductive system of Rostanga poddubetskaiae sp. nov., MNHN IM-2013-86202. Abbreviations: am, ampulla; bc, bursa copulatrix; dd, deferent duct; fg, female gland complex; pr, prostate; sr, seminal receptacle; vg, vagina.

Radular formula 28 × 73.0.73 in a 23-mm long specimen (MNHN IM-2013-86208), 36 × 80.0.80 in a 26-mm long specimen (MNHN IM-2013-86205), and 37 × 81.0.81 in a 26-mm long (MNHN IM-2013-86209). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a small cusp and lacking denticles (Fig. 13A, B). Innermost teeth very small in comparison to mid-laterals (Fig. 13A). The teeth increase in size gradually towards the medial portion of the half-row (Fig. 13B). Outermost teeth small, decreasing in size gradually, and hamate (Fig. 13C), outermost one with 13–20 irregular denticles. No jaw was observed, labial cuticle smooth.

Figure 13. 

SEM of the radula of specimens of Rostanga poddubetskaiae sp. nov., MNHN IM-2013-86205 A innermost teeth B mid-lateral teeth C outer lateral teeth.

Biology

All the specimens were found on an unidentified species of sponge while SCUBA diving. The presence of these highly cryptic nudibranchs was initially determined in the field by observing the egg masses on the sponges. In most cases, to separate the nudibranchs, the sponges were brought to the lab and examined under a microscope.

Etymology

This species is named after Marina Poddubetskaia, indefatigable collector and diver, who first discovered the animals here described during the two of the Koumac expeditions.

Remarks

Rostanga poddubetskaiae sp. nov. is provisionally assigned to the genus Rostanga based on the results of the molecular phylogenetic analyses, which place this species solidly nested within a clade containing other species identified as members of Rostanga. However, there are some notable differences between Rostanga poddubetskaiae sp. nov. and the diagnoses of the genus Rostanga provided by Rudman and Avern (1989) and Valdés and Gosliner (2001), such as the absence of jaws and elongate outermost radular teeth, and the presence of short caryophyllidia; moreover, the arrangement of the branchial leaves flattened against the dorsum and the presence of a dorsal ridge are unusual for a species of Rostanga. Additional resolution in the phylogeny of dorid nudibranchs and a larger sample are needed before this species can be placed in a genus with confidence.

Rostanga poddubetskaiae sp. nov. appears to be sister to Rostanga elandsia Garovoy, Valdés & Gosliner, 2001 from South Africa, but additional species need to be included in the analysis to confirm those relationships. Morphologically, R. poddubetskaiae sp. nov. exhibits a number of differences from other members of this genus, including the presence of a dorsal ridge, elongate rhinophores, a gill flattened against the body, and smooth, hamate inner and mid radular teeth, and short, pectinate outermost lateral teeth. The Indo-Pacific species of Rostanga have been reviewed in papers by Rudman and Avern (1989), Baba (1991), and Garovoy et al. (2001), and none of them have external and internal characteristics present in R. poddubetskaiae sp. nov. The only exception is Rostanga crawfordi (Burn, 1969), described as Rostanga australis Rudman & Avern, 1989, which appears to have a dorsal ridge in some specimens (see Rudman and Avern 1989; Coleman 2008) and a similar external coloration to R. poddubetskaiae sp. nov., but the radular teeth are very different: specifically, the outer teeth are elongate with numerous denticles on the tip.

Sclerodoris Eliot, 1904

Sclerodoris Eliot, 1904: 361. Type species: Sclerodoris tuberculata Eliot, 1904, by subsequent designation by Valdés and Gosliner (2001).

?Gravieria Vayssière, 1912: 29–30. Type species: Gravieria rugosa Vayssière, 1912, by monotypy.

Tumbia Burn, 1962b: 161–163. Type species: Asteronotus (Tumbia) trenberthi Burn, 1962b [= Sclerodoris trenberthi (Burn, 1962b)], by monotypy.

Remarks

For an in-depth discussion of the characteristics of the genus Sclerodoris and its synonyms see Valdés and Gosliner (2001).

Sclerodoris tuberculata Eliot, 1904

Figs 14A, 15A–C, 16A–C

?Doris castanea Kelaart, 1858: 110. Type locality: Sober Island, Tricomalie [= Trincomalee] harbor, Ceylon [= Sri Lanka].

Sclerodoris tuberculata Eliot, 1904: 381–382. Type locality: Prison Island [= Changuu], Zanzibar harbor, Tanzania.

Sclerodoris minor Eliot, 1904: 381. Type locality: Chuaka [= Chwaka], Zanzibar, Tanzania.

Sclerodoris rubra Eliot, 1904: 382–383. Type locality: reef off the east coast of Zanzibar, Tanzania.

Halgerda rubra Bergh, 1905: 126–127, pl. 4 fig. 2, pl. 15 figs 34–36. Type locality: Bandas [= Banda Islands], Indonesia, 36 m depth.

Material examined

Pointe de Pandop, Koumac, New Caledonia (20°34.9'S, 164°16.5'E), 7 m depth [Koumac 2.1 stn. KR868], 26 Sep 2018, 1 specimen 44 mm long, dissected (MNHN IM-2013-86197, isolate JI10).

Description

Body oval, flattened, with an irregular, coriaceous texture (Fig. 14A). Branchial and rhinophoral sheaths somewhat elevated, simple, circular. Gill composed of eight short, tripinnate branchial leaves, arranged upright. Rhinophores short, lamellated, with 18 lamellae. Visceral hump clearly elevated over the rest of the mantle, with several lateral protuberances and a conspicuous depression mid-length. Dorsum completely covered with small caryophyllidia. Body color red, with several large, irregularly opaque white patches, mainly on the mantle margin and some white pigment irregularly scattered all over. Rhinophores and branchial leaves are the same color as the dorsum.

Figure 14. 

Photographs of live animals of the genus Sclerodoris Eliot, 1904 A Sclerodoris tuberculata Eliot, 1904, MNHN IM-2013-86197 on black background B–D “Sclerodoris” dutertrei sp. nov., Holotype (MNHN IM-2013-86193) on black background (B), MNHN IM-2013-86195 on black background (C), MNHN IM-2013-86194 on black background (D) E Sclerodoris faninozi sp. nov., Holotype (MNHN IM-2013-86198) on black background.

Reproductive system (Fig. 15A, B) with a long, wide, convoluted ampulla with several folds, which connects with the female gland complex and the oval, flattened prostate. The prostate narrows substantially into a long, straight duct, before expanding into the short, wide deferent duct. The penis is armed with triangular spines, varying in size (Fig. 15C) with thickened bases and sharp cusps. The vagina is elongate, narrow, as wide as the deferent duct, connecting directly to the large, oval bursa copulatrix. The elongate seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the short uterine duct that enters the female gland complex (Fig. 15B). The bursa copulatrix is ~ 4× as large as the seminal receptable. An accessory gland connects to the genial atrium where the deferent duct and the vagina meet. The accessory gland is granular in texture and approximately as large as the seminal receptable.

Figure 15. 

Drawing of the reproductive system of specimens of the genus Sclerodoris Eliot, 1904 A–C Sclerodoris tuberculata Eliot, 1904, MNHN IM-2013-86197, general view (A), detail of the bursa copulatrix and seminal receptable (B), penial spines (C) D–F Sclerodoris faninozi sp. nov., Holotype (MNHN IM-2013-86198), general view (D), detail of the bursa copulatrix and seminal receptable (E), penial spines (F) G “Sclerodoris” dutertrei sp. nov., MNHN IM-2013-86193. Abbreviations: ag, accessory gland; am, ampulla; bc, bursa copulatrix; dd, deferent duct; fg, female gland complex; pr, prostate; sr, seminal receptacle; vg, vagina.

Radular formula 38 × 49.0.49 in a 44-mm long specimen (MNHN IM-2013-86197). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having an elongate cusp and lacking denticles (Fig. 16A, B). Innermost teeth very small in comparison to mid-laterals (Fig. 16A). The teeth increase in size gradually towards the medial portion of the half-row. Outermost teeth small, decreasing in size gradually, composed of a short, blunt cusp with numerous small denticles (Fig. 13C). No jaw was observed, labial cuticle smooth.

Figure 16. 

SEM of the radula of specimens of the genus Sclerodoris Eliot, 1904 A–C Sclerodoris tuberculata Eliot, 1904, MNHN IM-2013-86197, innermost teeth (A), mid-lateral teeth (B), outer lateral teeth (C) D–F “Sclerodoris” dutertrei sp. nov., MNHN IM-2013-86195, innermost teeth (D), mid-lateral teeth (E), outer lateral teeth (F) G–I Sclerodoris faninozi sp. nov., Holotype (MNHN IM-2013-86198), innermost teeth (G), mid-lateral teeth (H), outer lateral teeth (I).

Biology

Rare, found under rocks at 7 m depth. Widespread in the Indo-Pacific region. The single specimen was found under a rock while SCUBA diving where it was highly cryptic.

Remarks

Eliot (1904) described Sclerodoris tuberculata based on one specimen collected in Zanzibar as follows: “Dark brown with sandy spots, exactly like a sponge splashed with sand. Underside clear bright brownish red. Branchial pocket crenulate. The middle part of back covered with conical warts, which form an irregular keel; smaller warts on mantle-edge. Rhinophores red; branchiae eight, voluminous; axes red, tips white. Animal alters shape, sometimes rather high, sometimes quite flat like Platydoris. Consistency quite hard and rather rough. Two depressions with deep black markings as in some species of Trippa.” In the same paper Eliot (1904) introduced two additional species also resembling sponges, Sclerodoris minor Eliot, 1904, and Sclerodoris rubra Eliot, 1904, both synonyms of S. tuberculata. Sclerodoris tuberculata is considered a widespread species in the Indo-Pacific region and is well documented in the literature (Valdés and Gosliner 2001; Yonow 2008; Gosliner et al. 2018; Nakano 2018). The material here examined is consistent with the original description of S. tuberculata and subsequent records; however, a record of this species from New Caledonia (Hervé 2010) is probably the closely related species Sclerodoris rubicunda (Baba, 1949).

Eliot (1906) suggested that Doris castanea Kelaart, 1858 was possibly the same species as Sclerodoris tuberculata Eliot, 1904, but indicated the identity of the latter could not be established with certainty based on the type material. Eliot (1906: pl. 42, figs 6, 7) reproduced the original drawing by Kelaart, which clearly resembles a dark specimen of S. tuberculata. Later, Eliot (1908) regarded Sclerodoris rubra Eliot, 1904 as a senior synonym of Halgerda rubra Bergh, 1905.

Allan (1947) reported S. tuberculata from New South Wales, Australia, under the genus name Peronodoris Bergh, 1904 and commented on Eliot’s (1906) proposed synonymy between this species and D. castanea. Allan (1947) indicated that “although the colour sketch of the upper surface of Kelaart’s specimen resembles that of our specimen to a very slight degree,” the undersurface is exactly like the color sketch of the New South Wales material of S. tuberculata. Allan (1947) concluded that whether S. tuberculata was eventually to become a synonym of D. castanea remained to be seen, as fresh material from the two type localities needs to be examined before this can be determined.

Rudman (1978) endorsed Eliot’s (1908) decision to synonymize Halgerda rubra Bergh, 1905 with Sclerodoris rubra Eliot, 1904. At the same time Rudman (1978) regarded Sclerodoris rubra Eliot, 1904 and Sclerodoris minor Eliot, 1904 as synonyms of Sclerodoris tuberculata Eliot, 1904, and based on the Principle of First Reviser (ICZN 1999: Article 24), Rudman (1978) established S. tuberculata as the valid name for this species. Rudman (1978) also commented that the original description of D. castanea by Kelaart (1858) was most inadequate and therefore best to ignore it. In this paper we follow Rudman’s (1978) conclusion and regard Sclerodoris tuberculata Eliot, 1904 as the valid name for this species with the synonymies established above. We also leave the question of the identity of D. castanea as unresolved.

Hervé (2010) reported Sclerodoris tuberculata from New Caledonia but based on the photographs published (Hervé 2010: 214), it seems that these records correspond to Sclerodoris rubicunda (Baba, 1949). The present study is the first confirmed record of Sclerodoris tuberculata from New Caledonia.

Sclerodoris faninozi sp. nov.

https://zoobank.org/619B72BC-611E-4E53-ABAA-0D8D67284448
Figs 14E, 15D–F, 16G–I

Type material

Holotype : Koumac, New Caledonia (20°33.7'S, 164°11.2'E), 0 m depth [Koumac 2.3 stn. KB518, blocks of dead coral on the margin of the fringing reef flat of the lagoon island], 20 Nov 2019, 25 mm long, dissected (MNHN IM-2013-86198, isolate JI11).

Description

Body oval, flattened, with an irregular, coriaceous texture (Fig. 14E). Branchial and rhinophoral sheaths somewhat elevated, simple, irregular. Gill composed of five short, tripinnate branchial leaves, arranged upright. Rhinophores short, lamellated, with 15 lamellae. Visceral hump elevated over the rest of the mantle. Dorsum completely covered with small caryophyllidia, a longitudinal ridge, and several large, rounded tubercles. Body color yellowish brown, with scattered opaque white pigment, and areas or dark brown and dark gray. Branchial leaves and rhinophores dark brown.

Reproductive system (Fig. 15D, E) with a long, wide, convoluted ampulla with several folds, which connects with the female gland complex and the elongate, convoluted prostate. The prostate is as wide as the ampulla, but narrows substantially into a very long duct, before expanding into the long, narrow deferent duct. The penis is armed with rounded spines having a short, sharp cusp (Fig. 15F). The vagina is elongate, narrow, as wide as the deferent duct, connecting directly to the large, spherical bursa copulatrix. The elongate seminal receptacle also connects to the bursa copulatrix and the uterine duct that enters the female gland complex. The bursa copulatrix is ~ 3× wider than the seminar receptable, but similar in volume (Fig. 15D). No accessory gland was observed.

Radular formula 32 × 68.0.68 in a 25-mm long specimen (MNHN IM-2013-86198). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having an elongate cusp (sometimes bifurcate) and lacking denticles (Fig. 16G–I). Innermost teeth very small in comparison to mid-laterals (Fig. 16G). The teeth increase in size gradually towards the medial portion of the half-row. Outermost teeth small, decreasing in size gradually, elongate, with a short cusp and numerous denticles (Fig. 13I). No jaw was observed, labial cuticle smooth.

Biology

Rare, found intertidally under rocks, possibly a New Caledonia endemic. The single specimen was obtained by brushing blocks of dead coral on the margin of a fringing reef flat.

Etymology

This species is named after Sébastien Faninoz whose efforts were critical for the organization of the Koumac expeditions.

Remarks

In the phylogenetic analyses conducted herein, Sclerodoris faninozi sp. nov. is sister to Sclerodoris tuberculata, the type species of Sclerodoris, forming a well-supported clade; for this reason, S. faninozi sp. nov. is placed in the genus Sclerodoris. Moreover, most of the anatomical characteristics of S. faninozi sp. nov. match the diagnosis of the genus Sclerodoris provided by Valdés and Gosliner (2001). Specifically, S. faninozi sp. nov. has a flattened, coriaceous dorsum covered with caryophyllidia, the rhinophoral sheaths are somewhat elevated; the penis is armed with hooks and the vagina is unarmed; the labial cuticle and radular teeth are smooth, hamate with the outermost lateral teeth multi-denticulate. The only exception is the accessory gland, which is a diagnostic trait for Sclerodoris, but was not observed in S. faninozi sp. nov. Although the absence of an accessory gland in S. faninozi sp. nov. could have been result of damage to the specimen, it appears that the presence of this organ is variable in Sclerodoris.

Sclerodoris faninozi sp. nov. is externally similar to Sclerodoris coriacea Eliot, 1904 introduced based on a specimen collected near Chwaka (as Chuaka), on the east coast of Zanzibar, Tanzania. Eliot (1904) described S. coriacea as yellowish brown in color with the dorsal surface covered with a “distinctly raised but somewhat irregular reticulate pattern.” Rudman (1978) redescribed S. coriacea also based on specimens from Zanzibar, and a color photograph of a live animal was illustrated by Gosliner et al. (2018). The specimen of S. faninozi sp. nov. here examined is similar to all these descriptions with the exception of the presence of a dorsal ridge, absent in S. coriacea. The radular morphology of S. faninozi sp. nov. is also similar to that of S. coriacea as described by Rudman (1978) but the innermost teeth of S. faninozi sp. nov. have a bifurcated cusp, whereas they are simple in S. coriacea (Rudman 1978: fig. 13).

“ Sclerodoris dutertrei ”, sp. nov.

https://zoobank.org/504AD504-89AE-48D4-9840-4800830CC0AC
Figs 14B–D, 15G, 16D–F

Type material

Holotype : Anse de Koumac, New Caledonia (20°34.2'S, 164°16.5'E), 0 m depth [Koumac 2.1 stn. KR213], 11 Sep 2018, 31 mm long (MNHN IM-2013-86193, isolate JI04).

Material examined

Récif Sud de Pandop, Koumac, New Caledonia (20°35.4'S, 164°16.5'E), 0 m depth [Koumac 2.1 stn. KR322, reef flat with rocks, living and dead corals], 27 Sep 2018, 1 specimen 23 mm long (MNHN IM-2013-86196, isolate JI14). Koumac, New Caledonia (20°35.6'S, 164°16.3'E), 3 m depth [Koumac 2.2 stn. KR230], 2 Mar 2019, 1 specimen 12 mm long (MNHN IM-2013-86194, isolate JI35); 1 specimen 20 mm long, dissected (MNHN IM-2013-86195, isolate JI34).

Description

Body oval, flattened, with an irregular, coriaceous texture (Fig. 14B–D). Branchial and rhinophoral sheaths somewhat elevated, simple, irregular. Gill composed of five short, tripinnate branchial leaves, arranged upright. Rhinophores short, lamellated, with 12–14 lamellae. Visceral hump elevated over the rest of the mantle. Dorsum completely covered with small caryophyllidia and a complex network of ridges and scattered large, rounded tubercles. Body color variable, yellow to pale brown with scattered opaque white pigment and some specimens with rounded black spots. Branchial leaves are the same color as the dorsum; rhinophores brown proximally, with white apices.

Reproductive system (Fig. 15G) with a long, wide, convoluted ampulla with several folds, which connects with the female gland complex and the oval, flattened prostate. The prostate narrows substantially into a long, convoluted duct, before expanding into the short, wide deferent duct. The penis is unarmed. The vagina is elongate, much narrower than the deferent duct, connecting directly to the large, oval bursa copulatrix. The elongate seminal receptacle also connects to the bursa copulatrix next to the vaginal connection, and the short uterine duct that enters the female gland complex. The seminal receptable possesses a spherical tip and it is similar in volume to the bursa copulatrix. An accessory gland connects to the genial atrium where the deferent duct and the vagina meet. The accessory gland is granular in texture and approximately as large as the bursa copulatrix.

Radular formula 37 × 54.0.54 in a 20-mm long specimen (MNHN IM-2013-86195). Rachidian teeth absent. Inner and mid-lateral teeth hamate, having a short cusp and lacking denticles (Fig. 16D, E). Innermost teeth very small in comparison to mid-laterals (Fig. 16D). The teeth increase in size gradually towards the medial portion of the half-row. Outermost teeth small, decreasing in size gradually, elongate, with a short cusp and lacking differentiated denticles (Fig. 16F). No jaw was observed, labial cuticle smooth.

Biology

Found under rocks at 0–3 m depth. All the specimens were obtained by direct collection while SCUBA diving. The specimens were very cryptic on rocks with sponges and other encrusting organisms.

Etymology

This species is named after Valentine Dutertre whose hard work, dedication, and skill were critical for the collection of numerous important sea slug species during the Koumac expeditions.

Remarks

The phylogenetic analysis places “Sclerodoris” dutertrei sp. nov. in a well-supported clade containing two other species identified as members of Sclerodoris. These two species were sequenced and submitted to GenBank but never formally studied, thus their morphological characteristics remain undescribed. This clade is not closely related to the clade containing the rest of the species of Sclerodoris, including the type species, Sclerodoris tuberculata. Therefore, “S.” dutertrei sp. nov. cannot be definitely included in the genus Sclerodoris and the generic placement of this species is regarded as tentative until a well resolved phylogeny of the Discodorididae permits a more accurate taxonomic placement. “Sclerodoris” dutertrei sp. nov. is tentatively placed in Sclerodoris (as indicated by the quotation marks) because anatomically this species is for the most part consistent with the diagnosis for Sclerodoris provided by Valdés and Gosliner (2001), including a flattened, coriaceous dorsum covered with caryophyllidia, rhinophoral sheaths somewhat elevated; a lobate accessory gland, without stylet; labial cuticle and radular teeth smooth, hamate with the outermost lateral teeth multidenticulate. The only exception is the penis, which appears to be unarmed in “S.” dutertrei sp. nov., but the presence of penial spines is a characteristic of Sclerodoris sensu stricto (see Valdés and Gosliner 2001).

“Sclerodoris” dutertrei sp. nov. is distinct from other species previously assigned to Sclerodoris: no other species described to date possesses a yellow to pale brown dorsum with scattered opaque white pigment (sometimes with rounded black spots), completely covered with small caryophyllidia and a complex network of ridges and scattered large, rounded tubercles. As mentioned above, Sclerodoris tuberculata is red with several large, irregularly shaped, opaque white patches and a conspicuous depression mid-length on the dorsum, not present in “Sclerodoris” dutertrei sp. nov.; Sclerodoris faninozi sp. nov. is yellowish brown, with scattered opaque white pigment, and areas of dark brown and dark gray but also has a longitudinal ridge, and several large, rounded tubercles, also absent in “Sclerodoris” dutertrei sp. nov. Other Indo-Pacific species described also present external characteristics that distinguish them from “Sclerodoris” dutertrei sp. nov. For example, Sclerodoris apiculata (Alder & Hancock, 1864) is characterized by having a network of ridges radiating from elevated conical centers, each with an elongated filament (see Alder and Hancock 1864; Hervé 2010; Gosliner et al. 2018; Nakano 2018). Sclerodoris coriacea has the dorsum completely covered with large, elongate tubercles joined by conspicuous ridges (see Rudman 1978; Gosliner et al. 2018), very different from those in “Sclerodoris” dutertrei sp. nov. Sclerodoris japonica (Eliot, 1913), originally described as a member of the genus Halgerda (see Eliot 1913) is characterized by having a yellowish grey dorsum covered with small ridges, and numerous, large roundish areas of a darker grey, varying in intensity, which correspond to dorsal depressions or pits. Sclerodoris rubicunda is a red species with two large patches of white and purple pigment and a series of conspicuous dorsal ridges (Baba 1949; Gosliner et al. 2018; Nakano 2018). Sclerodoris trenberthi (Burn, 1962b) and Sclerodoris tarka Burn, 1969 both described from Victoria, Australia are also distinct from “Sclerodoris” dutertrei sp. nov. Sclerodoris trenberthi has a characteristic longitudinal dorsal structure composed of “irregularly sized and spaced low hard pustules surmounting a low ridge” running from the rhinophores to the gill (Burn 1962b), which is absent from “Sclerodoris” dutertrei sp. nov. Sclerodoris tarka is a dusky yellow to yellowish orange species with a pattern of conspicuous dorsal ridges (Burn, 1969) and an indistinct medial ridge, also absent in “Sclerodoris” dutertrei sp. nov. Finally, Sclerodoris virgulata Valdés, 2001 is the only species of Sclerodoris with a white dorsum lacking dorsal ridges or depressions (Valdés 2001), also very different from “Sclerodoris” dutertrei sp. nov.

Discussion

The phylogeny presented here is largely consistent with previous morphological studies and the classification of the Discodorididae proposed by Valdés and Gosliner (2001) and Valdés (2002) with some exceptions. For example, the genus Atagema is sister to the rest of Discodorididae + Cadlinidae, but due to the poor representation of Cadlinidae in this study, these results should be taken cautiously. There is also a discrepancy with the molecular analysis by Hallas et al. (2017), who found Atagema + Aphelodoris as sister to remaining members of Discodorididae, but Aldisa + Cadlina forming a distinct clade, as also recovered by Johnson (2010) and Johnson and Gosliner (2012). On the contrary, in the present analyses Aldisa is nested within the Discodorididae. The more limited taxon sampling in the present study could explain this discrepancy, but the goal of the present analysis is only to place the new species here described in a phylogenetic context, not to provide a reliable reconstruction of the phylogeny of Discodorididae, which may only be achieved with next generation sequence data. There are some other differences between the present analyses and previous classification attempts of species included herein. For example, Discodoris coerulescens was regarded by Dayrat (2010) as a member of a metaphyletic group branching from near the basal node of Discodorididae he named “Montereina,” but the present analyses appear to suggest a close relationship with the genus Tayuva Er. Marcus and Ev. Marcus, 1967. Tayuva was considered a synonym of Discodoris by Valdés (2002) and T. lilacina, originally described as Doris lilacina Gould, 1852, is regarded as a member Discodoris by some authors (e.g., Gosliner et al. 2018); however, other authors following Dayrat (2010) placed this species in Tayuva, a distinct genus with a single pantropical species (e.g., Ballesteros et al. 2016; Yonow 2017). The results of the present analysis appear to confirm that Tayuva is distinct from Discodoris as suggested by Dayrat (2010), but it is unclear how many species are present in this pantropical complex. Finally, the genus Montereina MacFarland, 1905 was synonymized with Peltodoris by Valdés (2002), but the results of the present analyses suggest that these two groups are distinct as suggested by Dayrat (2010).

Based on the phylogenetic analyses here presented, it appears that the genus Sclerodoris is paraphyletic. The new species “Sclerodoris” dutertrei sp. nov. was recovered in a well-supported clade containing two other species identified as members of Sclerodoris, but not in the clade including Sclerodoris tuberculata Eliot, 1904, which is the type species of Sclerodoris. Thus, the description of a new genus name for the clade including “Sclerodoris” dutertrei sp. nov. is an option. However, due to the limited sample size in our molecular phylogenies and the lack of support for several clades, we prefer to postpone any decisions regarding this group until a more reliable phylogeny of the Discodorididae is available, as there could be available genus-level names for this group. Therefore, the generic placement of “Sclerodoris” dutertrei sp. nov. is regarded as tentative, indicated by the quotation marks.

Bouchet et al. (2007) argued that “it can safely be affirmed that, as a result of the recent sampling programs, both in shallow and in deep-water, no other South Pacific island group has been so intensively surveyed as New Caledonia.” However, recent field work during the Koumac expeditions seems to have revealed additional diversity missed during early work, suggesting that documenting the New Caledonia molluscan diversity is still a work in progress. As Bouchet et al. (2007) indicated, the question of how many mollusk species are present in New Caledonia remains unanswered and this is particularly true for sea slugs. This paper is a small contribution towards the goal of describing the sea slug diversity of New Caledonia as field work continues to produce previously unseen taxa.

It is unclear how many of the species here described are endemic to New Caledonia. Payri et al. (2019) suggested that probably < 15% of the New Caledonia marine mollusks are endemic, although they also indicated that “several scientists have already demonstrated connections between the marine life of New Caledonia, the Great Barrier reef, and the center of maximum diversity of the Coral Triangle.” Based on photographs published in field guides or other publications, it is likely that Atagema papillosa (Risbec, 1928), Atagema sobanovae sp. nov., and Jorunna daoulasi sp. nov. are widespread in the Western Pacific, but we have been unable to find photographs of Atagema kimberlyae sp. nov., Jorunna hervei sp. nov., Rostanga poddubetskaiae sp. nov., Sclerodoris faninozi sp. nov., and “Sclerodoris” dutertrei sp. nov. in other publications outside New Caledonia. But due to the very cryptic nature of these species, it could very well be that they have been overlooked. While the small size of the eggs of J. hervei sp. nov. suggests planktotrophic development and therefore a potentially large geographic range, the recent description of a very similar species from the Indian Ocean, J. liviae, may indicate there is a species complex of species with similar external morphologies present in different ocean basins. Much more work on these neglected dorid nudibranchs is needed to have a better understanding of their taxonomy, diversity, and evolution.

The specimens here examined where collected using different techniques, including dredging, direct collecting (intertidally and SCUBA diving), and substrate collecting. Due to the highly cryptic coloration and morphology of some of the species, their presence was detected initially by the observation of egg masses on the sponges. In the particular case of A. sobanovae sp. nov., most of the specimens were collected by dissecting the sponges in the laboratory as the nudibranchs were buried in the tissue, and almost invisible. The diversity of collecting techniques and specialized methods used during the Koumac expeditions were critical in the discovery of the species here examined. This paper provides a rare example of the description and re-description of ecologically cryptic sea slug species using contemporary taxonomic techniques and focusing on a narrow geographic region that, despite substantial collecting efforts (Bouchet et al. 2007), appears to remain under-sampled.

Acknowledgements

The material examined was collected during the “Our Planet Reviewed” – New Caledonia expeditions (2016–2019), a joint project of MNHN and Conservatoire d’Espaces Naturels (CEN) de Nouvelle-Calédonie, funded mainly by the Gouvernement de la Nouvelle-Calédonie, Province Nord, Agence Française de la Biodiversité (AFB), the Lounsbery Foundation, and Office des Postes et Télécommunications (OPT). The expedition operated under a permit issued by Direction du Développement Economique et de l’Environnement (DDEE) of Province Nord. We are especially grateful to Philippe Bouchet for the invitation to participate in the expedition and to Sébastien Faninoz, Virginie Héros, Philippe Maestrati, Pierre Lozuet, Alain Daoulas, Jean-François Hervé, Yves Thévenet, and many others for their help and support. We also thank Jenelle Innabi, Tatiana Vargas, and Jade de Souza for their assistance with the molecular work.

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Supplementary materials

Supplementary material 1 

Individual analysis of COI gene fragments

Julie Innabi, Carla C. Stout, Ángel Valdés

Data type: figure (jpg file)

Explanation note: Posterior probabilities are shown above the branches and bootstrap values from the maximum-likelihood analysis values shown below branches.

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 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.
Download file (143.02 kb)
Supplementary material 2 

Individual analysis of 16S gene fragments

Julie Innabi, Carla C. Stout, Ángel Valdés

Data type: figure (jpg file)

Explanation note: Posterior probabilities are shown above the branches and bootstrap values from the maximum-likelihood analysis values shown below branches.

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 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.
Download file (122.25 kb)
Supplementary material 3 

Individual analysis of Histone H3 gene fragments

Julie Innabi, Carla C. Stout, Ángel Valdés

Data type: figure (jpg file)

Explanation note: Posterior probabilities are shown above the branches and bootstrap values from the maximum-likelihood analysis values shown below branches.

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 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.
Download file (125.02 kb)
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