Biodiversity hotspot in cold waters: a review of the genus Cuthonella with descriptions of seven new species (Mollusca, Nudibranchia) Author Korshunova, Tatiana A. Author Sanamyan, Nadezhda P. Author Sanamyan, Karen E. Author Bakken, Torkild Author Lundin, Kennet Author Fletcher, Karin Author Martynov, Alexander V. text Contributions to Zoology 2021 2020-12-29 90 2 216 283 http://dx.doi.org/10.1163/18759866-bja10017 journal article 10.1163/18759866-BJA10017 1875-9866 10661858 Cuthonella soboli Martynov, 1992 ( Figs 1 , 2 , 17 , 20G , 21 ) Cuthonella soboli Martynov, 1992: 18–23 , figs 1–3; Martynov , 2006b: 290; Martynov , 2015b: 80; Martynov & Korshunova, 2011: 197–198, fig. on page 197, excluding the figure on page 198 ( C. osyoro ). Type material. Holotype . ZMMU Op-736, L = c. 30 mm (live), The Sea of Japan , Sobol Bay , intertidal, stones, 03.03.1992 . Paratype . ZMMU Op-737, L = 15 mm length (preserved), The Sea of Japan , Sobol Bay , 0.2–0.7 m depth , stones, collected by A . V . Martynov , 05.02.1992 . Other material: ZMMU Op-605, 2 spec. , L = 8 mm length (live), The Sea of Japan , Spokoinaya Bay , 3–5 m depth , brown algae, stones, collected by T . A. Korshunova and A . V . Martynov , 25.09.2014 . External morphology Body moderately wide. Foot and tail broad. Oral tentacles moderate. Rhinophores similar in size, or slightly longer than oral tentacles, smooth to slightly wrinkled.Dorsal cerata elongate, thick, arranged in continuous rows. Up to 6 pre-anal ceratal rows. Anal opening acleioproctic. Colour (live). Background colour yellowish white. Digestive gland diverticula in cerata from light brownish and sandy to tobacco- and dark-brown. Basal parts of cerata commonly darker. White spots or streaks on the ceratal external surface. Ceratal tips colourless or with dispersed white pigment. Rhinophores semi-transparent to light yellowish and orange ochre with indistinct to dispersed white pigment on the top (fig. 17A–E). Jaws. Jaws broad, yellowish in colour. Masticatory processes of jaws covered with a single row of distinct denticles (fig. 17F, G). Radula. Radula formula 28× 0.1.0 (specimen 15 mm in length), 24 × 0.1.0 (specimen 8 mm in length). Central tooth elongated with a strongly protracted, pointed non-compressed cusp (fig. 17H–K). Central tooth bears up to 10 lateral denticles. Cusp clearly delineated from the adjacent first lateral denticles. Reproductive system. Diaulic. Hermaphroditic duct leads to a moderately long, swollen ampulla. Vas deferens moderately long, without a distinct prostate. Supplementary gland long, inserts into the vas deferens a considerable distance from the elongated penial sheath. Penis conical, unarmed. Oviduct connects through the insemination duct into the female gland complex. Receptaculum seminis in a distal position, on a moderately long stalk, pear-shaped (fig. 20G). FIGURE 18 Cuthonella vasentsovichi sp. nov. A, living holotype ZMMU Op-738, Matua Island, 21 mm (preserved length), dorsal view. B, C, preserved holotype, lateral and ventral views respectively. D, jaw, paratype ZMMU Op-739, Matua Island (SEM). E, jaw, details, same. F, anterior part of the radula, paratype (SEM). G, posterior part of the radula, same. Scale bars: D, 500 µm; E, F, G, 50 µm; Photos: A, Nadezhda Sanamyan, B– G, Alexander Martynov . Ecology. Stones, rocks. Intertidal to c. 10 m depth. Veligers exhibit direct development or a shortened planktonic stage. Distribution. The northern part of the Sea of Japan , possibly also the Southern Kuril Islands and Hokkaido . Remarks. According to the molecular phylogenetic analysis, Cuthonella soboli Martynov, 1992 forms a separate clade sister to the C. osyoro clade (figs 1, 2). The minimum also repressed earlier in the tsar’s Russian COI intergroup distance of 2.89% is found Empire. between C. soboli and C. osyoro ( Table 1 ). External morphology. Body wide. Foot Externally C. soboli differs from the closely and tail broad. Oral tentacles moderate. related species C. osyoro by the absence of any Rhinophores similar in size to oral tentacles, reddish or orange spots on the cerata (fig. 17). smooth to slightly wrinkled. Dorsal papillae Morphological analysis reveals considerable numerous, elongate, thick, arranged in differences in the denticulation of the continuous rows. Up to 10 (or more) pre-anal central teeth between C. hiemalis , C. osyoro , branched and unbranched ceratal rows. Anal C. soboli , and the type species of the genus opening cleioproctic. Cuthonella , C. abyssicola s.l. (figs 4, 5, 12, 14, Colour (live). Background colour greyish. 17). Reproduction occurs in the wintertime. Digestive gland diverticula in cerata greyish The food objects of C. soboli possibly include to light greenish. Ceratal tips yellowish. athecate hydroids ( Martynov & Korshunova, Rhinophores dark yellowish, without distinct 2011). For a morphological comparison with white pigment at the top (fig. 18A). other Cuthonella species , see table 2. Jaws. Jaws moderately broad, yellowish in colour. Masticatory processes of jaws covered Cuthonella vasentsovichi sp. nov . with a single row of denticles (fig. 18D, E). ( Figs 1 , 2 , 18 , 20H , 21 ) Radula. Radula formula 40 × 0.1.0 ZooBank: http://urn:lsid:zoobank. (specimen 15 mm in length). Central tooth o r g: a c t: B 4 9 E B F 1 D - 8 E 9 F - 4 74 3 - 9 F 1 3 - elongated with a strongly protracted, pointed 860063D7FA9C non-compressed cusp (fig. 18F, G). Central Type material. Holotype . ZMMU Op-738, tooth bears up to 9 lateral denticles. Cusp L = 21 mm length (preserved), Pacific Ocean, clearly delineated from the adjacent first Middle Kuril Islands, Matua Island, Klyuv lateral denticles. Cape , 14 m , collected by N.P. Sanamyan , Reproductive system. Diaulic. Herma- 20.08.2017 . phroditic duct leads to a relatively short, Paratype . ZMMU Op-739, L = 15 mm length partially swollen, convoluted ampulla . (preserved), Pacific Ocean, Middle Kuril Vas deferens moderate in length, without Islands, Matua Island, Klyuv Cape, 14 m , a distinct prostate. Supplementary gland collected by N.P. Sanamyan, 20.08.2017 . relatively short, inserts into the vas deferens Etymology. Named in honour of Vladislav a considerable distance from the elongated Konstantinovich Vasentsovich (1898–1961). penial sheath.Penis conical,unarmed.Oviduct He was a Division Commander in the Soviet connects through the insemination duct into Far East before WWII and was repressed the female gland complex. Receptaculum during Stalin’s Great Purge, imprisoned for seminis in a distal position, on a short stalk, 15 years and freed only a few years before his oval (fig. 20H). death (Milbakh, 2003). Vladislav Vasentsovich at 14 m depth. is a relative of one of the authors of this article Distribution. Matua Island, Middle Kuril (AM). The name was also chosen because the Islands. Kuril Islands ( type locality of the new species) Remarks. The maximum intragroup belongs to the Russian Far East region and distance in C. vasentsovichi is 0.15%. The for the additional cultural intersection with minimum COI intergroup distance of 9.28% Benedykt Dybowski, who like Vladislav is found Downloaded between from C. Brill vasentsovichi .com 12/12/2023 sp04. nov:16:22. PM Vasentsovich, was of a Polish origin via Open and Access was. This sp. is nov an. open and access C. concinna article distributed concinna under (table the1terms). of the CC-BY 4.0 license. https://creativecommons.org/licenses/by/4.0/ FIGURE 19 Reproductive systems of the genus Cuthonella . A, Cuthonella abyssicola abyssicola ; B, Cuthonella abyssicola kryos subsp. nov. ; C, Cuthonella ainu sp. nov. ; D, Cuthonella benedykti sp. nov. ; E, Cuthonella concinna concinna ; F, Cuthonella concinna bellatula subsp. nov. Abbreviations: a, ampulla; fgm, female gland mass; fo, female opening; ps, penial sheath; rs, receptaculum seminis; sg, supplementary gland; vd, vas deferens. By a combination of morphological ceratal rows makes C. vasentsovichi sp. nov. characters Cuthonella vasentsovichi sp. nov. partially resemble Cuthonella abyssicola readily differs from any previously described s.l. (figs 4, 5), but C. vasentsovichi differs Cuthonella species. Morphological analysis in having a broader body with greyish to also reveals considerable differences in the greenish colouration instead of reddish denticulation of the central teeth between or light pinkish, and by the morphology C. vasentsovichi sp. nov. (fig. 18) and any of its radula and reproductive system. related species, e.g., C. ainu sp. nov. , C. denbei Such multilevel differences between the sp.nov., C. hiemalis , and others from this new species and the type species are clade (figs 6, 7, 10–12, 14, 17). Externally C. remarkable and align well with the recently vasentsovichi sp. nov. differs from all known proposed scheme of multilevel organismal species of the genus Cuthonella by a peculiar diversity (Korshunova et al., 2019b). For “shaggy” appearance of numerous, densely a morphological Downloaded comparison from with Brill.com 12/12/2023 other 04:16:22PM placed cerata (fig. 18A). The large number via Open of Cuthonella Access. This is an open species access , see article table 2. distributed under the terms of the CC-BY 4.0 license. https://creativecommons.org/licenses/by/4.0/ FIGURE 20 Reproductive systems of the genus Cuthonella . A, Cuthonella denbei sp. nov. ; B, Cuthonella georgstelleri sp. nov. ; C, Cuthonella hiemalis ; D, Cuthonella orientosiberica sp. nov. ; E, Cuthonella osyoro ; F, Cuthonella punicea ; G, Cuthonella soboli ; H, Cuthonella vasentsovichi sp. nov. Abbreviations: a, ampulla; fgm, female gland mass; fo, female opening; ps, penial sheath; rs, receptaculum seminis; sg, supplementary gland; vd, vas deferens. TABLE 2 Morphological comparison of the species of the genus Cuthonella Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and (max) and its penis pattern C.abyssicola 30 mm Possibly reddish to 17, branched 21 × 0.1.0 Up to 14 lateral Long, Long, inserts into On a very long abyssicola (preserved) pinkish, tips without denticles, moderately a long vas deferens stalk, tubular, Bergh, 1884 distinct spots or bands which are rarely swollen, at a considerable widened in of opaque white clustered.Cusp convoluted distance from middle part pigment is rather clearly penial sheath. with a small delineated from Penis conical, oval reservoir the adjacent strong, unarmed lateral denticles which do not reach top of the teeth C.abyssicola kryos 25 mm Light pinkish to 17, branched 27 × 0.1.0 Central teeth Long, Long, inserts into On a very long subsp. nov. (preserved) whitish, tips with have up to c. 36 moderately a long vas deferens stalk, tubular, dispersed white lateral denticles, swollen, at a considerable widened often clustered convoluted distance from basally, and increasingly penial sheath. with a small irregular towards Penis conical, pear-shaped the cusps. Cusp strong, unarmed reservoir is not clearly delineated from the adjacent lateral denticles which may reach top of the cusp North Atlantic and Sub-arctic, commonly at shelf and bathyal depths (up to 1000 m ) High latitude Arctic, shallow waters Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and (max) and its penis pattern C.ainu sp. nov. 4 mm Brownish to light 5, unbranched 18 × 0.1.0 Up to 7 distinct Relatively Long, inserts into a On a short Middle Kuril (preserved) orange, ceratal tips lateral denticles, short, short vas deferens stalk, Islands, with opaque white cusp well slightly at a short distance elongate-oval shallow waters spot delineated bent, from penial swollen sheath. Penis conical, unarmed C.benedykti 6 mm Brownish with darker 5, unbranched 36 × 0.1.0 Up to 5 distinct Relatively Relatively short, On a short Kamchatka , sp. nov. (preserved) reddish to brown lateral denticles, short, inserts into a stalk, oval shallow waters hue, ceratal tips with cusp well swollen moderately long opaque white ring, delineated vas deferens at sometimes with a short distance additional yellow ring from penial sheath. Penis conical, unarmed TABLE 2 Morphological comparison of the species of the genus Cuthonella ( Cont .) Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and (max) and its penis pattern C.cocoachroma 15 mm (live) Dark brown, deep 4, unbranched 39 × 0.1.0 Up to 5 distinct Long, Short, reportedly On short stalk, NE Pacific, (Williams & reddish-brown to dark lateral denticles, moderately inserts into the rounded California , Gosliner,1979) chocolate brown, tips cusp well swollen, penis (Williams & shallow waters with opaque white delineated convoluted Gosliner, 1979), but spot without further confirmation. Unarmed penis was reported as possessed a broadened base, which could potentially conceal the distalmost part of the vas deferens C.concinna 20 mm (live) Brown to purplish- 6, unbranched 30 × 0.1.0 Up to 10 distinct Relatively Relatively long or On a short North Atlantic concinna (Alder & brown, tips with lateral denticles, short or shorter, inserts stalk, without (both sides), Hancock, 1843) opaque white cusp not well folded, into a relatively distinct shallow waters subapical band or spot delineated swollen long vas deferens reservoir, in a with a bluish hue at a relatively short more proximal distance from position penial sheath. Penis conical, unarmed Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and (max) and its penis pattern C.concinna 15 mm (live) Pinkish, brownish- 4, unbranched 17 × 0.1.0 Up to 5 distinct Relatively Short, inserts On a short NE Pacific bellatula orange, reddish, lateral denticles, short, bent, into a short vas stalk, with only from Alaska subsp. nov. grayish-purple to cusp well swollen deferens at a weakly distinct to California , blackish, often with delineated relatively long reservoir, in a shallow waters few scattered white or distance from more proximal bluish spots, tips with penial sheath. position opaque white spots or Penis conical, band unarmed C.denbei sp. nov. 7 mm Brownish to dark- 6, unbranched 19 × 0.1.0 Up to 7 distinct Relatively Relatively short, On a short Middle Kuril (preserved) reddish, tips with ring- lateral denticles, short, inserts into a stalk, Islands, shaped opaque white cusp well swollen moderately long pear-shaped shallow waters pigment delineated vas deferens at a long distance from penial sheath.Penis conical,unarmed C.elenae 45 mm Unknown 15, branched and 26 × 0.1.0 Up to 7 distinct Consists of Short,inserts On a very long Chukchi Sea Martynov , 2000 (preserved) unbranched lateral denticles, few short into a very long stalk, small, off Wrangel cusp not well reservoirs vas deferens at drop-shaped Island region, delineated a considerable shallow waters distance from penial sheath. Penis very wide, unarmed,but with several triangular papillae around opening Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and TABLE 2 Morphological comparison of the species of the genus Cuthonella ( Cont .) (max) and its penis pattern C. georgstelleri 14 mm Light orange-brownish 8, unbranched 30 × 0.1.0 Up to 10 distinct Relatively Long, inserts into On a long stalk, Middle Kuril sp. nov. (preserved) and salmon-brownish plus few lateral denticles, short, a moderately long compressed Islands, to dark, intensive branched cusp well swollen vas deferens at shallow waters brownish reddish, tips delineated a considerable with extended opaque distance from white band or spot penial sheath. Penis conical, unarmed C. hiemalis 26 mm (live) From dark beige to 7, unbranched 23 × 0.1.0 Up to 12 distinct Relatively Long, inserts into On a long White Sea, ( Roginskaya, 1987 ) dark brown, tips with lateral denticles, long, folded, long vas deferens massive stalk, shallow waters peculiar opaque bluish cusp well non-swollen at a considerable oval subapical band or delineated distance from spot, without opaque penial sheath. white pigment Penis conical, unarmed C. orientosiberica 4 mm Light brownish to 6, unbranched 28 × 0.1.0 Up to 9 distinct Relatively Long, inserts into On a short East Siberian sp. nov. (preserved) yellowish in juveniles lateral denticles, long, a moderately long stalk, oval Sea, Laptev and brownish to dark cusp well slightly vas deferens at Sea, shallow brown in adults, tips delineated folded, a considerable waters whitish swollen distance from penial sheath. Penis conical, unarmed Species Body length Cerata colouration Number Radula Central teeth Ampulla Patterns of Rece- Distribution (max) of anterior formula supplementary ptaculum branches of (max) gland, vas seminis digestive gland deferens and (max) and its penis pattern C.osyoro 23 mm (live) Brownish to dark red 6, unbranched 26 × 0.1.0 Up to 11 distinct Moderately Long, inserts into On short stalk, The Sea of (Baba, 1940) or violet, tips with lateral denticles, short,bent, a moderately long rounded Japan and variously expressed cusp well swollen vas deferens at neighbouring red or orange band or delineated a considerable waters, shallow spot, on ceratal surface distance from waters white streaks or dots penial sheath. may be present Penis conical, unarmed C.punicea 24 mm (live) From purple to dark 8, branched and 20 × 0.1.0 Up to 7 distinct Relatively Long, inserts into On a NE Pacific, so (Millen, 1986) wine-red, with white unbranched lateral denticles, long, a long vas deferens moderately far known only spots or streaks, tips cusp clearly swollen at a considerable long stalk, from British with dispersed white delineated from distance from elongate Columbia, the adjacent first penial sheath shallow waters lateral denticles Penis long, narrow, unarmed C.sandrae sp. nov. 4 mm Violet-purple, tips with 7, branched 12 × 0.1.0 Up to 8 distinct Unknown Unknown Unknown Middle Kuril (preserved) dispersed white and lateral denticles, Islands, bluish hue cusp relatively shallow waters unclear delineated from the adjacent first lateral denticles. TABLE 2 Morphological comparison of the species of the genus Cuthonella ( Cont .)

Species	Body length	Cerata colouration	Number	Radula	Central teeth	Ampulla	Patterns of	Rece-	Distribution
(max)	of anterior	formula	supplementary	ptaculum
branches of	(max)	gland, vas	seminis
digestive gland	deferens and
(max) and its	penis
pattern
C.soboli	30 mm (live)	From light brownish	6,unbranched,(in 29 x 0.1.0 Up to 10 distinct			Moderately	Long, inserts into	On a	The Sea of
Martynov , 1992	and sandy to tobacco-	some specimens	lateral denticles,	long,slightly a moderately long		moderately	Japan and
and dark-brown, basal	a few can be	cusp well	bent,swollen vas deferens at		long stalk,	neighbouring
part commonly darker, branched)		delineated	a considerable	pear-shaped	waters, shallow
white spots or streaks	distance from	waters
on ceratal external	penial sheath.
surface, tips colourless		Penis conical,
or with dispersed	unarmed
white pigment
C.vasentsovichi	21 mm	Greyish to light	10(+), branched	40 × 0.1.0 Up to 9 distinct		Relatively	Relatively short,	On a short	Middle Kuril
sp. nov.	(preserved)	greenish, tips	and unbranched		lateral teeth, cusp short,		inserts into a	stalk, oval	Islands,
yellowish	well delineated	partially	moderately long	shallow waters
swollen	vas deferens at
a considerable
distance from
penial sheath.
Penis conical,
unarmed

Discussion temperate conditions of the North Atlantic and the NE Pacific respectively, compared Cold-water biodiversity hotspot: the to the very cold NW Pacific (including the Cuthonella case Kuril Islands ), where negative sea water In the past five years, our knowledge of the temperatures can occur in the wintertime. nudibranch fauna of the Arctic Sea and The Kuril Islands group, including Matua the Northwest Pacific Ocean has advanced Island , are a chain of active volcanic islands substantially (e.g., Martynov et al., 2015a, b, (e.g., Blokh et al., 2018). They are located on 2020b; Korshunova et al., 2016a, b, 2017a, c, the edge of the continental shelf and are in 2018a, b). Prior to that, Cuthonella species the confluence of the southward flowing from these areas, such C.hiemalis and C.soboli, Oyashio current and the Western Subarctic were shown to have direct development, i.e. gyre (Qiu, 2001). Matua is a small island, only without a planktonic stage ( Roginskaya, 1987 ; about 11 × 6.5 km , essentially just the top of a Martynov , 1992). Although we have no data volcano. for the developmental patterns of our newly Five new species ( C. ainu sp. nov. , C. denbei described species from the NW Pacific, five of sp. nov., C. georgstelleri sp. nov. , C. sandrae them belong to the same clade as C. hiemalis sp. nov. and C. vasentsovichi sp. nov. , see and C. soboli according to our molecular data descriptions above, figs 1, 2, 6, 10, 11, 16, 18, (figs 1, 2). Therefore, it is plausible to suggest 21) were discovered in the shallow waters of that these species may also have direct or a this island, plus the new species C. benedykti shortened planktonic development as they sp. nov was discovered from a neighbouring inhabit essentially the same cold-water Kamchatka locality (figs 7, 21). This peculiar environment. Direct development implies geologic composition and the geographic limited dispersal capabilities, and hence position between the warm Japanese waters more opportunities to form separate species. with abundant fauna, the Arctic sea, and the For other marine invertebrates, an increasing oceanic currents, supports a high abundance rate of speciation has been linked to direct of marine life and active speciation. development (e.g., Hurtado et al., 2017). We therefore suggest that the cold- Thorson (1950) , in his study of the water biodiversity hotspot exemplified by reproductive and larval ecology of marine the cuthonellids is a result of the special bottom invertebrates, concluded that direct biogeographic conditions coupled with or other non-feeding development is the direct development among some species. dominate reproductive mode in polar waters. Because several Cuthonella species occur Therefore, a higher proportion of direct- sympatrically in a restricted area, we suggest development nudibranch species might that they could have originated by a directbe found in cold-water and polar regions. development-driven evolution in isolated Although “Thorson rule” has been contested, narrow areas in relatively remote parts of the recent broad-scale analyses confirm its middle Kuril Islands and adjacent regions. In validity in several groups (e.g. Fassio et al., contrast, for the North Atlantic subspecies 2019). Alternately, planktonic development from temperate waters such as C. concinna has been noted for C. concinna s.l. , C. concinna , planktonic development has been cocoachroma and C. punicea (Thompson & documented ( Roginskaya, 1987 ; Martynov Brown, 1984; Goddard, 1992; Millen, 1986), & Korshunova, 2011). This suggests a case however these three species occur in relatively of allopatric Downloaded speciation from Brill.com between 12/12/2023 the North 04:16:22PM 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 21 World map showing the distribution of Cuthonella species. Coloured symbols are indicated on the figure. Atlantic C. concinna concinna and its sister NE 1977), especially after the genus Cuthonella Pacific subspecies C. concinna bellatula subsp. was synonymized with the genus Cuthona nov. Allopatric speciation has previously been (Millen, 1986). After 1986, Cuthonella was well documented from various species of replaced by Cuthona Alder & Hancock, 1855 nudibranchs (e.g., Korshunova et al., 2018b, in descriptive papers and guide books (e.g., 2020a). The reasons why the biodiversity Behrens & Hermosillo, 2005). However, in hotspot for cuthonellids in the Middle Kuril 1992 it was shown that the genus Cuthonella Islands has not been recognised before can be differs considerably from the genus Cuthona explained by both insufficient sampling and and from any other genera of the traditional a deficit of taxonomic reviews for this region. tergipedids according to the morphology of the reproductive system and so it was considered Taxonomy of Cuthonella : a morphological a valid taxon ( Martynov , 1992, 2002, 2006b; prediction and molecular confirmation Martynov & Korshunova, 2011) (fig. 22A). The genus Cuthonella Bergh, 1884 was until Only since the work of Martynov (1992) quite recently only considered valid by a few was a diagnosis for the genus provided which authors (e.g., Odhner in Franc, 1968; Miller, characterized Downloaded the genus from (fig Brill.com . 22A). The 12/12/2023 genus 04:16:22PM 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/ Cuthonella was expanded to encompass families Cuthonidae and Cuthonellidae . The not only the deep-sea type species, but also second is that the supplementary gland in shallow-water species such as C. concinna s.l. , C. cocoachroma in reality inserts into the vas C. hiemalis , C. punicea and C. soboli . Recently, deferens, but closer to the penis, and this was the validity of the genus Cuthonella was missed by Williams & Gosliner (1979) . Except supported by molecular phylogenetic studies for this detail, the genus Cuthonella appears (Korshunova et al., 2017b, 2018a; Martynov et to be very consistent internally among all al., 2020a), albeit with few species involved. examined species, with the presence of an In the present study, we confirm the validity unarmed penis and protruding radulae cusps and monophyly of the genus Cuthonella by in most of the species. involving a considerably broader species External morphological features vary diversity of the genus (figs 1, 2, 21). This is the considerably within the species of the genus largest expansion of the number of species Cuthonella . The type species, Cuthonella of the genus Cuthonella since 1992 and one abyssicola s.l. , and some species such as of the largest recent expansions of described C. sandrae sp. nov. and C. punicea , possess diversity among northern nudibranchs. branched anterior ceratal rows and may have Here we present novel molecular data a cleioproctic anus. Instead, other species, for a species that is morphologically similar such as C. ainu sp. nov. , C. benedykti sp. nov. , C. to C. abyssicola , the type species of the hiemalis , C.concinna s.l. , C.soboli ,and C.osyoro , genus Cuthonella . It is separated here as C. possess unbranched anterior ceratal rows abyssicola kryos subspec. nov. This subspecies and an acleioproctic anus. The correlation of clusters together with other species included these features with molecular phylogenetic in this study, forming a well-supported data is quite a mosaic (figs 1, 2, 4 –9, 14, 17), monophyletic group (fig. 1). In total, we so at this stage we have not separated more obtained and analysed molecular data for 13 genera, but retained just the one the genus of the 15 currently recognised species of the Cuthonella within the family Cuthonellidae , genus. For all species of Cuthonella , except for though with more data more genera will C. cocoachroma (which was unavailable for our most likely be necessary. Therefore, we do morphological study), we confirmed that the not synonymise the previously established supplementary gland in the male part of the subgenus Fiocuthona with the type species reproductive system is inserted into the vas C. concinna s.l. ( Martynov , 1992) or further deferens instead of the penis. Hence, this is a differentiating the taxonomic structure of the well-supported morphological synapomorphy family Cuthonellidae pending more data from for the genus Cuthonella . For C. cocoachroma , other species. Williams & Gosliner (1979) reported that the In total, the species diversity within the supplementary gland inserts into the penis genus Cuthonella has now increased over instead of the vas deferens.Since the insertion of threefold, from five valid species ( Martynov , the supplementary gland into the vas deferens 1992) plus two which are verified here as is a very stable morphological character among synonyms, C. marisalbi (Roginskaya, 1963) and species in the genus Cuthonella according to C. distans ( Odhner, 1922 ) , to the current 15 our data, there are at least two possibilities species and two subspecies (figs 1, 2, 21), for C. cocoachroma . The first is that in this thus confirming the phylogenetic pattern of species, a supplementary gland inserting the almost 30-year-old prediction based on into the penis has evolved in parallel to the morphology Downloaded( Martynov from Brill, 1992.com). 12/12/2023 04:16:22PM 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 22 Discussion of the radula characters and fine-scale diagnostics in the taxonomy of the former “tergipedid” families. A. Taxonomic composition of the tergipedid aeolidacean nudibranchs before 2016. B. A ‘superlumping’ aggregation of the “family Fionidae sensu latissimo ” (Cella et al., 2016; Epstein et al., 2019) lacking morphological apomorphies. C. Modern fine-scale tergipedid taxonomy that integrates molecular data and provides morphological apomorphies for several separate families and genera (Korshunova et al., 2017a, b; 2018a,b, 2019a, b; Mehrotra et al., 2020). The crossed-out taxon names signify a change in the genus status, the normally displayed names signify valid taxa at every consequential level of the history of the taxonomy of this group. All drawing schemes and SEM images are original. Fine-scale differentiation of the family more genera. The old notion that if genera Cuthonellidae have some putative overlap of morphological One practical question should be particularly patterns (Mayr, 1969; Gosliner & Griffiths, addressed in respect to the revision of the 1981) they should be merged into a single large genus Cuthonella . Marcus (1958) noted that genus, without morphological apomorphies the degree of protrusion of the central cusp (fig.22B), is counterproductive to phylogenetic of the radular teeth can vary within the same investigation. species among the traditional “tergipedid” Obviously, with such an approach an group. Recently, Korshunova et al. (2017a) integrative taxonomy involving morphology demonstrated that various genera or groups and molecular analysis will be contradictory. of genera, particularly within the family We have already clearly demonstrated this fact Trinchesiidae , have their own peculiar for the “superlumping” concept of the “family patterns of radular teeth, not just because of Fionidae ” s.l. (fig. 22), which has no reliable the degree of the relative height of the central morphological apomorphies (see discussion cusp and lateral teeth, but also because of in Korshunova et al., 2017a). Only narrower, patterns that integrate several specific traits. more finely defined taxa of genus- and family For example, the genera Trinchesia s.str. and groups can be used to integrate morphological Diaphoreolis have arch-shaped teeth with the and molecular data (Korshunova et al., 2017b, central cusp similar in length to the central 2020a, b, c) (fig. 22C). teeth. The genus Catriona , as another example, These integrative arguments were not has a central cusp, not just lower than the understood and were contradicted recently lateral denticles but strongly retracted, making and labelled “cumbersome” and based on the general shape of the teeth a distinctive “dubious, minor characters” by Epstein et al. trait (fig. 22). The genus Phestilla also has a (2019).Notably,itwasareversereiterationofthe special combination of long needle-like teeth argument from our previous study ( Martynov , and a lower central cusp covered with smaller 1992) regarding the genus Cuthona : “if (one) denticles (fig. 22). None of these trinchesiid does not intend to create a cumbersome, radular patterns show similarity to those of the unnatural genus Cuthona , it is necessary to family Cuthonellidae and the genus Cuthonella apply a less lumping approach than what has (fig. 22B). The genus Tenellia s.str. (the family been applied by most of the recent authors” Trinchesiidae , fig. 22C) has a peculiar tooth (translated from Russian; Martynov , 1992: 23). shape, displaying only little variation, contrary Further molecular analysis (see discussions in to the statement in Epstein et al. (2019). Korshunova et al., 2017a, 2018a, b, c; Martynov According to the molecular phylogenetic et al., 2020a) confirmed the conclusions of data, the family Cuthonellidae forms a well- that almost 30-year-old study. The “ Cuthona supported clade, which is only distantly sensu lato ” was revealed as a large polyphyletic related to the Trinchesiidae (Korshunova assemblage and Cuthona s.str. was then et al., 2017b, 2018a; Martynov et al., 2019, limited to only a few morphologically similar 2020a).When more of the diversity within the species.Importantly, the genus Cuthonella was essentially tropical Trinchesiidae and cold- shown to be neither closely related to Cuthona water Cuthonellidae will be investigated, with nor Trinchesia . When defining the characters successively finer differentiated characters of the “family Fionidae sensu latissmo” Cella and an increasing number of monophyletic et al. (2016) (fig. 22B) used characters that subclades, it will be necessary to establish are not present Downloaded in from the Brill type .com genus12/12 Fiona /2023,04 like:16:22 a PM 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/ penial gland, and hence the real Fionidae s.str. is pointless to make a classification using has a reproductive system as well as patterns only radular characters and to argue that if of external morphology that are drastically radulae among some taxa demonstrate some different from any other “Fionoidea”. In similarities or similar variabilities these taxa table 3 of our 2017 study (Korshunova et al., must automatically be synonymized. 2017a) we mentioned the relative height of Instead, every taxon at the family- and the central cusp and formally described the genus-level demonstrates a complicated differences in the shape of the teeth along multilevel mosaic of morphological characters with several other characters, and thus did (including potentially a big disparity between not build a classification solely on a single characters of different organ systems) character. Moreover, Eubranchidae have and molecular features. Any diagnosis a triserial radula, Calmidae have radula that professes to encompass a complex with fused teeth, and both conditions are evolutionary history in a classification must very different from the uniserial radula of be based on such multilevel differences, and Cuthonella (fig. 22C). Furthermore, Epstein not on simplistic binary alternatives such as et al. (2019) based their arguments on an older “presence” or “absence”, “lower” or “higher” or drawing based on light microscopy studies in on an overestimated “variability”. Williams & Gosliner (1979 , fig. 5) without any Recently, the obvious problems of the additional SEM study. ‘superlumping’ approach were revealed within To present modern comparative the large aeolidacean group in which a very morphological data, in this study we complex molecular pattern was shown to be made a thorough SEM investigation of aligned with an extremely mosaic distribution a majority of the species of the genus of morphological characters (Korshunova et Cuthonella (figs 4–18). We specially show al., 2017b, 2019a, b; Martynov et al., 2020a). In that in some species of Cuthonella , e.g., conclusion, to have a ‘superlumping’ name for C. concinna s.l. , C. denbei sp. nov. , and such a group, one has to go much further than to C.osyoro ,the relative height of the central cusp unite many disparate taxa into a single “family and lateral denticles can vary to some degree Fionidae ” but to unite all order-level diversity of between the anterior and posterior teeth (figs the Aeolidacea into a single family, Aeolidiidae . 8O–R, 10G –I, 14J–L), but they never attain any This would lead to a morphologically non similarity in the general radular pattern to any finely diagnosable group, with only the most of the trinchesiid genera (fig. 22). general potential apomorphy (possession of a Furthermore, in this study we made a cnidosac at the extremity of each ceras) which novel review of data for all species of the corresponded to the taxonomic level of order/ genus Cuthonella , including seven new ones suborder, and not to the family level, because (figs 1–21), and none of the species possess a majority of aeolidaceans from any family radular teeth that have a similar pattern to any possess a cnidosac. trinchesiid genera (Korshunova et al., 2017a) However, even such a potential general (fig. 22C). Therefore, the conclusion that the apomorphy would be problematic since shape of the radular teeth cannot be used as several non-related genera lack cnidosacs, taxonomic characters in Fionoidea (fig. 22B) is e.g., Phestilla Bergh, 1874 in the family incorrect, and to the contrary, these characters Trinchesiidae or Phyllodesmium Ehrenberg , are very useful for taxonomy in an integrative 1831 in the family Myrrhinidae . In contrast, context. It is important to highlight that it when separating Downloaded from many Brill.com finely 12/12/2023 defined04:16:22PM 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/ families and genera, including Abronicidae, Most recently, our fine-scale approach Calmidae , Cuthonellidae , Cuthonidae , was supported by an independent study Eubranchidae , Fionidae s.str., Tergipedidae , of the tropical trinchesiid genus Phestilla Trinchesiidae , Xenocratenidae , Murmaniidae, (Mehrotra et al., 2020) . The review presented and potentially several others (fig. 22C), it here of the genus Cuthonella and the family facilitates making complex morphological Cuthonellidae is therefore of high relevance for diagnoses and a list of morphological demonstrating the benefits of this approach, apomorphies that is maximally consistent. since this is a properly narrow family and Importantly, it is also concordant with the genus, whose validity has been confirmed molecular data. Every narrowly defined family first by using morphological data ( Martynov , and genus has its own set of finely scaled 1992; Martynov & Korshunova, 2011) then characters, that, if taken separately, may be recently by the application of molecular data incorrectly considered “overlapping” ones. in Korshunova et al. (2018a) and finally by the The pitfalls of the ‘superlumping’ approach addition of seven new species and two new can immediately influence practical subspecies detailed in this study. taxonomy. For example, the maximally broad approach that evoked the single huge “family Fionidae ” (which then “overlaps” by almost Acknowledgements all possible morphological apomorphies with all other aeolid families, see Korshunova Sandra Millen (University of British et al., 2017a, 2019a) led to the result (Cella et Columbia) is thanked for providing the type al., 2016) of failing to distinguish two externally specimens of Cuthonella punicea and helping similar taxa with drastically different internal to organize the collecting trip. Doug Miller morphologies: Cuthonella punicea (Millen, 1986) and Neil McDaniel are warmly thanked and Zelentia nepunicea Korshunova et al., 2018 . for collection of specimens of C. punicea . Thus, the maximally broad approach (e.g., Oleg Savinkin (The Institute of Ecology and Williams & Gosliner, 1979 ; Epstein et al., 2019) Evolution RAS) is thanked for collecting and not only “does not permit other users of the providing specimen from Franz Josef Land. classification (largely other comparative B.I. Sirenko, S.Y. Gagaev, and A.Y. Voronkov biologists) to identify taxa readily from living (Zoological Institute RAS) are thanked for examples”, but clearly misleads nudibranch collecting and providing specimens from taxonomists per se. Alternately, the fine-scale East Siberian Sea and images. Our gratitude approach of numerous narrowly-defined goes to Bernard Picton (National Museums families and genera easily avoids such pitfalls: of North Ireland) for collection of specimens Cuthonella punicea belongs to the family of C. concinna concinna from the British Cuthonellidae , whereas Zelentia nepunicea Isles and to Klas Malmberg (Universeum belongs to the family Trinchesiidae . Both and Aquatilis, Gothenburg) for collection families have a minimally overlapping of specimens of C. concinna concinna from particular set of morphological characters Sweden . T.A. Bakke and Kjersti Kvalsvik are (which of course are not absolutely “stable” thanked for the loan of specimen from the becauseofthecontinuingevolutionaryprocess) Oslo Natural History Museum. So Ishida and show significant molecular divergence, and (Osaka Museum of Natural History) and thus are only distantly related to each other Sho Kashio (Natural History Museum of the (Korshunova et al., 2017a, b, 2018a, b, 2019b). Kishiwada Downloaded City, Osaka from ) are Brill.com thanked 12/12/2023 for help 04:16:22PM 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/ with access to the archived material of Dr. org/10.15468/ddbs14 accessed via GBIF.org on Kikutaro Baba. The team of Gulen Dive Resort 2020-08-04. (Christian Skauge, Ørjan Sandnes, Monica Barman, A.S., Singh, M., Singh, S.K., Saha, H., Bakkeli and Guido Schmitz) are generously Singh, Yu. J., Laishram, M. & Pandey, P.K. (2018) thanked for their help during fieldwork in DNA barcoding of freshwater fishes of Indo- Norway , as the specimens collected there Myanmar biodiversity hotspot. Sci. Rep. , 8, 8579. were used for comparative purposes in this Behrens, D. (1980) Pacific coast nudibranchs, a study, and the #sneglebuss project field team guide to the opisthobranchs of the northeastern for assistance during field work in Finnmark , Pacific . Los Osos, CA, Sea Challengers. Norway . Anna Zhadan (Moscow State Behrens, D. & Hermosillo, A. (2005) Eastern Pacific University) is thanked for providing some nudibranchs, a guide to the opisthobranchs material and images on C. hiemalis . Reviewers from Alaska to Central America . Monterey, Sea are thanked for providing comments that Challengers. helped to improve the paper. 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