Dendronotus nordenskioeldi, User, 2021

User, GBIF. Org, 2021, A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): a multilevel organismal diversity approach, Contributions to Zoology 90 (1), pp. 93-153 : 104-112

Dendronotus nordenskioeldi sp. nov.

Figs 1–3 , 5–7

ZooBank: http:// urn:lsid:zoobank.org:act:9FB63088-BF8A-4990-B292-7E26DEA0FDCF

Etymology. In honour of Baron Nils Adolf Erik Nordenskiöld, outstanding Arctic explorer, geologist, and mineralogist. The Laptev Sea had been originally named “Nordenskiöld Sea”, after this Arctic explorer.

Type locality. Laptev Sea.

Type material. Holotype. ZMMU Op-665. Arctic region , Laptev Sea, sta. 100, 69 m depth, collector Olga Zimina.

Description. Body relatively narrow, preserved holotype 19 mm length (fig. 5). Five to six main branched appendages on oral veil. Five appendages on rhinophoral stalks; 12–14 rhinophoral lamellae. Lateral papilla on rhinophoral sheath present. Five pairs of dorsolateral appendages. Circa 20 lip papillae. Dorsolateral appendages with relatively short primary stalk, moderately branched secondary branches and tertiary branches (fig. 5A, B). Basal colour is semitranslucent white. No additional pigment. Dorsal processes of jaws inclined posteriorly at approximately 53° to the longitudinal axis of the jaw body and 0.42 of its length (fig. 5D). Masticatory border of jaw with fine denticles (fig. 5E). Radular formula: 43 × 3–11.1.11–3. Central (rachidian) tooth bears very weak denticulation that are difficult to separate into individual denticles (up to 20 and more variously varied denticles at least) (fig. 5F, G). Denticles without deep furrows.Lateral teeth elongate, slightly curved, bearing up to seven denticles (+ 2–3 reduced denticles may present) (fig. 4F–H). Ampulla thickened, kidney-shaped. Prostate discoidal, consisting of up to 20 alveolar glands. Distal part of vas deferens moderate in length, transitioning to long, thick, curved copulatory organ. Bursa copulatrix large, distinctly elongated, with seminal receptaculum placed distally.

Distribution. So far known only from the Laptev Sea.

Remarks. Externally, Dendronotus nordenskioeldi sp. nov. resembles white forms of D. lacteus but differs by the absence of a distinct reticulation and peculiar ribs on the central teeth, which is a common characteristic of D. lacteus (Korshunova et al., 2017a) . According to the molecular differences, a minimal Synopsis of the previously described valid intergroup distance for the COI gene (7.9%) taxa of the family Dendronotidae is found between D. nordenskioeldi sp. nov and D. europaeus . The mean intergroup Genus Dendronotus Alder & Hancock, 1845 distances between D. nordenskioeldi sp. nov. Type species. Dendronotus frondosus and D. rufus , D. lacteus , and D. kamchaticus are (Ascanius, 1774)

8.3%, 8.3%, and 8.8% respectively. A maximal intergroup distance (15.0%) is found between Diagnosis.Dorsolateralappendageswithdistinct

D. nordenskioeldi sp. nov and D. patricki tertiary branches. Oral veil with branched (Appendix, table A2). appendages Downloaded. Jaws commonly from Brill.com with 12 set/12of /2023 tightly04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

packed ridge-like semi-discoid structures and species, an extended diagnosis is provided also with denticles. Radula with at least more when possible. The fine-scale diagnostics of than eight lateral teeth in adult specimens. the genus Dendronotus is a complex task since Central teeth with cusp integrated within lateral variation patterns of habitus and anatomical denticles (or within teeth body if denticles characters overlap in various species. By a absent), the central cusp is not protruding. careful listing it is possible to step-by-step Denticle-bear part of central teeth separated fulfill the task and present a mutilelevel from lateral sides by usually distinct shoulder, organismal diversity, though not in a strictly thus central teeth with squarish base and defined form, as was targeted previously triangular top.Prostate with evident, conspicous (e.g., Odhner, 1936; Robilliard, 1970), but in alveolar glands, commonly represent by a a complex form that is best suited to the discoid structure (varies from a flattened disk evolutionary mosaic in character evolution. to a compressed spherical structure), or very There are also still uncertanties regarding rarely non-discoid, linear (in this case alveolar some particular characters as well as previous glands also present). Copulative organ basically overinterpretations. First of all, previously conical, with various ratios of length and width the pattern of branching in the dorsolateral and degrees of apical tapering. appendages was claimed to be of considerable taxonomic importance (Ekimova et al., Natural history. Representaives of the genus 2015: Fig. 8 ). In this respect, it is necessary to Dendronotus inhabit a broad bathymetric state, that while some trends exist in a few range, from intertidal to depths over 3000 m, species, importance of these characters were and a variety of substrates (including stony considerably overestimated partly due to the and soft benthic environments). A majority use of preserved specimens in the analysis. of the Dendronotus species feed on hydroids This can be illustrated by the D. kamchaticus (Robilliard, 1970; Thompson & Brown, 1984; case, when according to Ekimova et al. (2015: Martynov & Korshunova, 2011). There as a few Fig. 8D ), D. kamchaticus has bulbous short notable exceptions, such as D. iris Cooper, 1863 branches that differ considerably from those from the northeastern Pacific,which is an active in any other Dendronotus species. This resulted predator of ceriantharian cnidarians (Wobber, from the use of preserved specimens with 1970; Shaw, 1991), whereas for the wide-bodied considerably contracted branches, whereas species D. robustus Verrill, 1870 , D. velifer G.O. the living adult specimens of D. kamchaticus Sars, 1878 and D. bathyvela Martynov et al. , have elongated branches of dorsolateral 2020a less specific prey spectrum (including appendages, which are not fundamentally polychaetes and hydroids) has been recorded different from the type species of the genus, (Roginskaya, 1990, 1997). D. frondosus (Korshunova et al., 2016a) . The description of D. zakuro (similar to D. Remarks. The genus Dendronotus is restricted kamchaticus by radula morphology) is based here since some species have been moved to on recently collected specimens with both other genera. See discussions and remarks shorter “bulbous” (see Martynov et al., 2020a: under the genera Cabangus gen. nov. and Fig. 3A ) and elongate dorsolateral appendages Pseudobornella . (Martynov et al., 2020a: Fig.3D, E ), which is due to differences in physiological conditions. The Species composition. Diagnoses and remarks for preserved specimen of D.zakuro (see Martynov 27 included species are listed below. For each et al., 2020a Downloaded: Fig. 3C ) from demonstrates Brill.com very 12/12/2023 similar 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

“bulbous” branches, which were incorrectly the genus Pseudobornella are mentioned after depicted as specific for D. kamchaticus in its the diagnoses of the species of the genus original description (Ekimova et al., 2015: Dendronotus .

Fig. 8D ) (see details in Synopsis under D. There are also various uncertainties and kamchaticus ). Dendronotus lacteus apparently misinterpretations regarding internal charachas shorter tertiary branches, and a “curly” ters that need to be addressed before diagnoappearance of the dorsolateral appendages. ses can be provided. For example, Robilliard However, variation in D. lacteus does not only (1970) suggested to apply several coefficients concern ontogenetic stages, but also occurs of jaw proportions. However, it is easy to among different adult specimens. So, some incorrectly apply respective angle of measurelarge specimens of D. lacteus have quite long ments and receive very different results, as for elongate branches of dorsolateral appendages, example in Ekimova et al. (2015) compared similar to those in D. frondosus (Korshunova to the same species which jaws by Robilliard et al., 2017a). Most species of the genus (1970). As an example, for D. dalli in Ekimova Dendronotus possess considerably branched et al. (2015: 863) an angle of dorsal processes dorsolateral appendages with distinct tertiary to the longitudinal axis of 25° was indicated, branches (MacFarland, 1966; Robilliard, whereas in Robilliard (1970: 454) this was 60°.

1970; Korshunova et al., 2016a, b, 2017a, In the present study we re-checked jaw pro- 2019b; Martynov et al., 2020a). Unbranched portions and presented updated values for the dorsolateralappendageswererecentlyreported majority of species with sufficient available only for D. claugei from the deep-sea (Valdes et information. This character still needs further al., 2018), but due to the most basal position testing, but some characteristic patterns for of this species (fig. 1) the generic position of different species are likely to occur. Similarly, D. claugei needs to be evaluated with more the number of the prostatic alveoles once data. For another deep-sea species, D. comteti , was thought to be a character that well charthe unbranched dorsolateral appendages acterizes different species (Robilliard, 1970; were also indicated (Valdes et al., 2018: 413), Ekimova et al., 2016). However, our previous however, according to the original description (Korshunova et al. 2016a, b) and present study of D. comteti , it possesses both branched and show that this character is much more variaunbranched dorsolateral appendages (Valdes & ble, and while there are clear trends in some Bouchet, 1998: 320). Unbranched dorsolateral species, it should generally be used with care.

appendages can occur in posterior parts of some In the species diagnoses below, differences other Dendronotus species (e.g., in D.robilliardi , in shape, length and proportions of the copsee Korshunova et al., 2016a). For some species, ulative organ (penis) are indicated. While in e.g., for D. dalli in Ekimova et al. (2015: 862), some species the differences in penial morthe indication of absent tertiary branches phology are clear, in other species this can be of dorsolateral appendages is incorrect. partly due to different degrees of contraction Dendronotus dalli definitely has tertiary after preservation. This character needs furbranches (Robilliard, 1970: 453; present study, ther investigation.

fig. 7). Instead, in the genus Pseudobornella the In the present study we show that the shape general appearance of dorsolateral appendages and size of the bursa copulatrix, at least among does not show as branches, but it is ctenidium- several Dendronotus species (e.g., between like, because of very indistinct (or truly absent) D. kalikal and D. yrjargul ), are rather contertiary branches (fig. 2). More details about stant and Downloaded can be used from Brill as.a com reliable 12/12/2023 diagnostic 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/ character. However, the exact position of the Martynov et al., 2020a), in the diagnoses commonly very small receptaculum seminis below we do not provide the number because can be very difficult to determine, but despite it can be misleading, because only a part of that, it will be given further attention in the the row was counted in various species. True diagnoses below. rodlets can occur in addition, as part of the Different terms were applied for the struc- thin labial cuticle, which is separated from tures on the masticatory edge within differ- the masticatory edges. Such true rodlets have ent species of the genus Dendronotus . For been well documented for the tropical repreexample, MacFarland (1966) used “denticles” sentatives of the family Dendronotidae (Pola or “ridge-like” denticles and Robilliard (1970) & Stout, 2008), and possibly also occur in applied “denticles”, whereas Ekimova et al. many Dendronotus species, since the labial (2015) used “rodlets”. In this respect, the term cuticle with rodlets were already described for “rodlets” was used for rod-like structures that several representatives (see e.g., MacFarland, constitute the body of jaws in other nudi- 1966). However, these characters remain branch groups. In the genus Dendronotus , the largely untested by modern methods and we elements on the masticatory edges are usually do not include it in the diagnoses below. As termed as “denticles” when the bodies of jaws an additional complication, denticles and are entire. However, in the genus Dendronotus especially ridge-like structures on the mastithere is a special set of structures in addition catory edges can be easily discarded during to the denticles that appears as broad semi- preparation, and therefore in some previous disks or ridges, which can additionally be descriptions it was inappropriately indicated covered with smaller spine- or denticle-like that masticatory edges are devoid of any structures. It is likely that most species of the denticles or ridges. For example, the absence genus Dendronotus possess such structures. In of the denticles on the masticatory edges addition to the semi-disks/ridges at the masti- of D. frondosus were incorrectly mentioned catory edges, more normally looking denticles in Ekimova et al. (2015), which was further can occur. Transitive denticles on masticatory used as a putative difference between D. fronedges were also occasionally reported for juve- dosus and D. primorjensis (Ekimova et al.,

niles of D. frondosus s.l. (Colgan, 1914; Wägele 2016). However, in both species denticles on

& Willan, 2000). Therefore, in the present the masticatory edges are definitely present study we use two different terms “ridge-like (Korshunova et al., 2016a). The same is true structures” and “denticles” when character- also for other species, such as D. kamchaticus izing the masticatory edges of Dendronotus and D. kalikal . For D. kamchaticus the absence species. The few denticles seen in many cases of any structures on the mascticatory edges are likely a precursor that further transits into was indicated in the original description. For semi-disk structures on the masicatory edges D. kalikal the presence of merely “rodlets” was

(see e.g., this clearly for D. kalikal , fig. 4Q). reported in the original description (Ekimova Because the full row of denticles and/or ridges et al., 2015). However in reality denticles and is not documented for all species due to diffi- ridge-like structures are present in both of culties during preparation, the exact number these species (Korshunova et al., 2016a, 2019b;

for these structures can be uncertain. Though for D. kalikal see fig. 4Q). Therefore, when the whenever possible, we already presented the original descriptions denticles or ridge-like number of denticles/ridges, for example the structures was not indicated for species that recently described Dendronotus species (e.g., we could not Downloaded check, from we suppose Brill.com the 12/12presence /2023 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/ of at least one of these structures and indicate remarkable transformation during the develthat in the diagnoses. opment from early juvenile to adult. The cen- Though a pair of salivary glands indeed tral tooth in earlier juveniles is low and bears inserts into the pharynx on the sides of the few distinct lateral denticles. The lateral teeth oesophagus, the knowledge of these is limited in early juveniles are very few in number only to a few species (e.g., MacFarland, 1966; (1–3) or absent, showing an indistinct dentic- Valdes & Bouchet, 1998; Pola & Stout, 2008). ulation or they are almost smooth. In individ- The salivary glands are usually not figured uals approaching the adults stage, the central in the original descriptions (an exception: teeth become elongate-triangular with dis- Valdes and Bouchet, 1998) and were never tinct shoulders, lateral denticles become consistently used for taxonomic diagnostics. relatively smaller and numerous or com- We therefore do not include salivary glands pletely reduced. Meanwhile, the lateral teeth in the diagnoses of the species of the genus increase in number and the denticles become Dendronotus . more conspicuous. Since parts of juvenile The radular patterns within the genus radula may persist in some adults, this may Dendronotus still offer one of the best diag- create a considerable confusion regarding the nostic characters (Korshunova et al., 2017a). taxonomic importance of radular characters.

However in several species groups quite For instance, D. dalli usually has a smooth similar patterns of the central tooth can be central teeth without denticles in adult stage, observed. These similarities occur between whereas for adults of D. dalli also denticles on groups/clades of closely related species (for central teeth were reported, which led to the example between species that closely related incorrect synonymyzation of D. dalli with D.

to D. frondosus , e.g., D. primorjensis and D. frondosus (Odhner, 1936; MacFarland, 1966).

venustus , between D. lacteus and D. rufus , This decision was later changed in favour of between D. dalli and D. elegans ), but also the validity of D. dalli , but uncertanties over among apparently more distantly related spe- the taxonomic application of the putatively cies such as D. kamchaticus and D. zakuro , and variable radula remained (Robilliard, 1970; between D. albus and D. robilliardi (see fig. 1). Roginskaya, 1987). Such “variations” can Despite these similarities, in a majority of be overcome by a consistent application these cases fine-scale differences in morphol- of general ontogenetic principles in taxonogy of radula can be detected. At the same omy, using the attribution of a particular time, different species which are grouped in set of characters to a particular ontogenetic the same subclade (fig. 1) can demonstrate stage (Martynov et al., 2015b, 2020b). Thus, considerably different radular patterns, as for the application of a multilevel diagnostic example the clade consisting of D. jamsteci , within the genus Dendronotus (one that D. subramosus and D. albus (Robilliard, 1970; combines morphological characters of vari- Pola & Stout, 2008; Korshunova et al., 2016a; ous levels and molecular data) instead of a Martynov et al., 2020a). Furthermore, the rad- search for immediate and clearly distinctive ulae of the morphologically very different D. differences, requires a fine-scale, complex robilliardi and D. gracilis demonstrate similar approach.

patterns in the presence of a widened central tooth with numerous small lateral denticles Dendronotus albopunctatus Robilliard, 1972 without furrows (Baba, 1949; Korshunova Dendronotus albopunctatus Robilliard, 1972 :

et al. 2016a, 2019b). The radula undergoes 421–430, Downloaded Figs 1–6 ; from Behrens Brill.com, 1980 12/12: 72 /2023; Behrens 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/ and Hermosillo, 2005: 93; Lamb and Hanby, 2005: 264.

Extended diagnosis. Body wide. Four to five (plus one–two posterior) pairs of dorsolateral appendages. Six to 12 appendages of oral veil. Three to seven appendages (equal in size) of rhinophoral stalks. Lateral papilla of rhinophoral sheaths absent. Rhinophores with 9–17 lamellae. No lip papillae reported in the first description. Basal colour yellowwhite, pale pink to red-brown, with red-brown spots and tiny opaque white spots scattered over whole body, solid white line along edge of foot and oral veil. Dorsal processes of jaws inclined posteriorly at approximately 50° to the longitudinal axis of the jaw body. Masticatory processes bear distinct denticles which increase in size towards the distal end of the process. Radula with up to 41 rows of teeth. Central tooth with up to 25 denticles. Up to 14 lateral teeth with up to 12 denticles. Ampulla voluminous, folded. Bursa copulatrix large, oval. Seminal receptaculum very small and placed distally at a short distance from the vaginal opening. Prostate discoid with about 11–16 alveolar glands. The vas deferens is long, penis short, conical. Body length up to 60 mm.

Distribution. NE Pacific, Washington and Oregon, USA.

Bathymetry. Depths of 18–40 m (soft substratum).

Remarks. Externally, D. albopunctatus is somewhat similar to other species that also inhabit soft substrata, such as D. robustus and D. velifer . However, its radular characters are more similar to those of the majority of Dendronotus species.

Figures

FIGURE 1 Phylogenetic relationships of the species of the genus Dendronotus based on COI + 16S + 28S + H3 concatenated dataset inferred by Bayesian Inference (BI). Numbers represent posterior probabilities from BI and bootstrap values for Maximum Likelihood.Some branches are collapsed at species level.Dendronotus elegans from the type region (North Atlantic) are highlighted in dark purple. Abbreviations:h – holotype; p – paratype.Summary of species delimitation results from ABGD analyses for the COI dataset is shown. Downloaded from Brill.com 12/12/2023 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

FIGURE 2 Phylogenetic relationships of the species of the genera Dendronotus, Pseudobornella and Cabangus in single COI, 16S, 28S, and H3 gene trees inferred by Bayesian Inference (BI). Some branches are collapsed. Positions the Pseudobornella orientalis highlighted green; positions the Cabangus regius highlighted orange.Numbers represent posterior probabilities from BI. PHOTOGRAPHS BY A. MARTYNOV AND T. KORSHUNOVADownloaded from Brill.com 12/12/2023 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

FIGURE 3 A.Map of the Northern Hemisphere showing the distribution of D.elegans (including “D.niveus”), D.kalikal, and D.yrjargul sp. nov.The type locality of D.elegans is indicated by crossed lines. B. The haplotype networks based on cytochrome c oxidase subunit I (COI), 16S rRNA (16S), and 28S rRNA (28S) molecular data showing genetic mutations occurring within D.elegans (“D.niveus”), D. kalikal, and D.yrjargul sp. nov. specimens.Abbreviations:BeSt – Bering Strait; BS – Barents Sea; Gr – Greenland; Km – Kamchatka; KS – Kara Sea; Ku – Kuril Islands; LS – Laptev Sea; Nf – Newfoundland; NS – Norwegian Sea; WS – White Sea.Type locality of D.elegans Downloadedis marked from on Brill. the commap12/ by 12/ “x” 2023. 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

FIGURE 4 Dendronotus yrjargul sp.nov.(a–n) and D.kalikal (o–t), external and internal morphology.a–c: living holotype of D.yrjargul NTNU-VM-76306 (a) and its habitat (b, c), dorsal,ventral and lateral views with egg mass and associated hydroid Abietinaria fusca, respectively; d: Dendronotus yrjargul, habitat of living paratype NTNU-VM-76302;e: jaw of holotype; f:denticles on the masticatory edge of the holotype; g: jaws of paratype NTNU-VM-76302; h:discoid ridge-like structures on the masticatory edge of paratype NTNU-VM-76302;i: details of discoid structures on the masticatory edge of paratype NTNU-VM-76302; j: anterior part of radula of holotype; k:central teeth of radula of holotype;l:lateral teeth of radula of holotype; m:central teeth of radula of paratype NTNU-VM-76302; n: lateral teeth of radula of holotype; o: living holotype of D.kalikal; p: jaw of D.kalikal Downloaded, specimen from Brill from.com Kurile12/12/ Islands 2023; 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

FIGURE 5 Dendronotus nordenskioeldi sp. nov.ZMMU Op-665, external and internal morphology.a–b:living holotype, dorsal and lateral views respectively;c:ventral view of preserved holotype;d: jaw of holotype; e: irregular denticles on the masticatory edge of the holotype;f:posterior part of radula; g:central teeth of radula; h: lateral teeth of radula of holotype.Scale bars: d: 1mm; e: 20 µm; f:100 µm; g, h: 30 µm. PHOTOGRAPHS BY O. ZIMINA (A, B) AND T. KORSHUNOVA (C). SEM MICROGRAPHS BY A. MARTYNOV

FIGURE 6 Reproductive systems. a, Dendronotus yrjargul sp. nov.; b, D.kalikal; c, D.elegans; d, D. nordenskioeldi sp. nov. Scale bars:a–d 1mm.Abbreviations:am, ampulla; bc, bursa copulatrix; fgm, female gland mass; fo, female opening; p, penis; pr, prostate; rs, receptaculum seminis; ud, uterine duct; vd, vas deferens; vg, vaginal duct.

FIGURE 7 Representaives of the genus Dendronotus (living specimens). PHOTOGRAPHS BY T. KORSHUNOVA, A. MARTYNOV, K. FLETCHER, D. MILLER, Y. FUJIWARA, K. HASEGAWA, K. SANAMYAN, N. SANAMYAN, AND O. ZIMINA Downloaded from Brill.com 12/12/2023 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/

FIGURE 8 Dendronotus elegans. External and internal morphology.a: living specimen ZMMU Op-713 from Greenland, near East Atlantic North American coast; b: jaw, same specimen; c; posterior part of radula, general overview,same specimen; d: close up of smooth central teeth, same; e: close up of lateral teeth, same; f:living specimen ZMMU Op-714 (as “D.niveus”) from the White Sea (subarctic); g: jaw, same specimen; h:masticatory edge of the jaws,same; i: posterior part of radula, general overview,same specimen; j: close up of smooth central teeth, same; k: living specimen ZMMU Op-715 from the Laptev Sea (Arctic); l: jaw, same specimen; m: posterior part of radula, close up of smooth central teeth, same; n: lateral teeth, same.o: discoid prostate with numerous alveols (which considerably exceed the considerably underestimated number presented in the first description of D.niveus), same specimen; Scale bars: b, l, 1mm; c: 300 µm; d, h–j, m: 100 µm; g: 1000 µm; e, n: 30 µm. PHOTOGRAPHS BY O. ZIMINA (A, K) AND T. KORSHUNOVA (F). SEM MICROGRAPHS BY A. MARTYNOV Downloaded from Brill.com 12/12/2023 04:12:08PM via Open Access. This is an open access article distributed under the terms of the CC BY 4.0 License. https://creativecommons.org/licenses/by/4.0/