Three new deep-sea species of Thyasiridae (Mollusca: Bivalvia) from the northwestern Pacific Ocean

. The Thyasiridae is one of the species-richest families in the abyssal and hadal zones of the northwestern Pacific Ocean. Many thyasirid species dominate benthic communities in terms of abundance and play an important role in the functioning of deep-sea ecosystems. Most of the thyasirid species in the region are new to science and have not been described. Based on the material collected from 1954 to 2016 by seven deep-sea expeditions, three new species of Thyasiridae ( Parathyasira coani sp. nov., P. pauli sp. nov., and Thyasira kharkovensis sp. nov.) are described from the abyssal and hadal zones (3210–7540 m depth) of the Sea of Okhotsk, the Bering Sea, as well as the Kuril-Kamchatka and Japan trenches. The new species are remarkable among their congeners due to the combination of the following characters: an obliquely-rhomboidal shell with a weak and shallow posterior sulcus and a large prodissoconch with sculpture of lamellated folds. Comparisons with related species are provided.

In the last decade, an international team of scientists has intensively sampled the deep-sea fauna of several northwestern Pacific areas, such as the Seas of Japan and Okhotsk, and the Kuril-Kamchatka Trench and adjacent abyssal plain (Malyutina & Brandt 2013;Brandt & Malyutina 2015;Malyutina et al. 2018;Brandt et al. 2020).These studies accounted for a rich bivalve fauna, with thyasirids being dominant in species richness.At least 14 thyasirid species were found at depths below 3000 m (Kamenev 2013(Kamenev , 2015(Kamenev , 2018a(Kamenev , 2019)).In addition, no less than 10 thyasirid species were found in many trenches of the western Pacific at the depth of more than 6000 m (Belyaev 1989).None of the species have been identified to the species level, and most of them are most probably new to science.In recent years, a study of these species was started by the author of the paper.As a first step, three new species were described from the abyssal and hadal zones of the Kuril-Kamchatka Trench region (Kamenev 2020).This paper is a continuation of the previous study and addresses another three, morphologically similar deep-sea species which are described herein as new.

Material and methods
The material examined in this study was collected between 1954 and 1990 by expeditions of the P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow (IO RAS) (RV Vityaz, cruise no. 19, 17 Oct.-29 Oct. 1954;RV Vityaz, cruise no. 45, 24 Apr.-10 Jul. 1969;RV Vityaz, cruise no. 59, 26 May-7 Jul. 1976;RV Akademik Mstislav Keldysh, cruise no. 22, 7 Jul.-27 Nov. 1990) from the Pacific abyssal plain adjacent to the Kuril-Kamchatka Trench, from the bottom of the Japan Trench, from the oceanic slope of the Kamchatka Peninsula, and from the bottom of the Commander Basin (Bering Sea), by the German-Russian deep-sea expeditions KuramBio (RV Sonne, cruise no. 223, 21 Jul.-7 Sep. 2012) and KuramBio II (RV Sonne, cruise no. 250, 16 Aug.-29 Sep. 2016) from the Pacific abyssal plain adjacent to the Kuril-Kamchatka Trench and in the hadal zone of the Kuril-Kamchatka Trench; and by the Russian-German deep-sea expedition SokhoBio from the bottom of the Kuril Basin (Sea of Okhotsk) (RV Akademik M. A. Lavrentyev, cruise no. 71, 6 Jul.-6 Aug. 2015).The new species of Thyasiridae described here were found in 30 samples at depths of 3210-7540 m.Samplings during the IO RAS expeditions were carried out by using an Okean grab (sampling area: 0.25 m 2 ), and Sigsbee and Galathea trawls (Monin 1983).During the KuramBio, KuramBio II, and SokhoBio expeditions a large box corer (sampling area: 0.25 m 2 ), epibenthic sledge, and Agassiz trawl were used (Brandt & Malyutina 2015;Malyutina et al. 2018;Brandt et al. 2020).All samples collected by the IO RAS were fixed in 4% buffered formaldehyde, transferred to 70% ethanol, and stored in the IO RAS Ocean Benthic Fauna collection (OBF).Samples collected by the KuramBio, KuramBio II, and SokhoBio expeditions were fixed in pre-cooled 96% ethanol, transferred to 70% ethanol, and stored in the Museum of the Institute of Marine Biology (MIMB), A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences (NSCMB FEB RAS), Vladivostok.The type material of the new species described here was deposited in the collection of the MIMB, IO RAS OBF, and Senckenberg Museum Frankfurt, Germany (SMF).
For scanning electron microscopy, shells were cleaned in 50% water-diluted commercial bleach, washed in distilled water, dried, mounted in aluminum stubs with adhesive tape and coated with chromium.Photographs were obtained with a SIGMA 300VP (Carl Zeiss, Cambridge, UK).Anatomical descriptions come from ethanol fixed specimens.Microscopic observations of shells and bodies were performed in a Zeiss Discovery 8 stereo microscope at the Far Eastern Center of Electron Microscopy of NSCMB FEB RAS.Shell and body anatomy's terminology follows Payne & Allen (1991) and Oliver & Killeen (2002).When determining the taxonomic position of new species, I follow the diagnoses of the genera Parathyasira Iredale, 1930 and Thyasira Lamarck, 1818 provided by Kamenev (2020) and Oliver & Holmes (2006), respectively.

Etymology
The species epithet honors Dr Eugene V. Coan, a well-known researcher of eastern Pacific bivalves who made an enormous contribution to the study of the bivalve fauna of the Pacific Ocean.
GroSS anatomy.Mantle edge thick, no obvious proliferation of glandular tissue on its anterior inner edge.Mantle fused posteriorly forming small exhalant aperture below posterior adductor muscle (Fig. 5A-C).
Anterior adductor muscle elongate (Fig. 5J).Posterior adductor muscle small, ovate, 2 × as short and as narrow as anterior adductor muscle.Ctenidium wide, consisting of two demibranchs with fully reflected filaments (up to 80 filaments in specimen 7.5 mm in length); outer demibranch approximately half the size of inner demibranch.Demibranchs covering greater part of lateral body pouches (Fig. 5A-B).
Labial palps relatively large (to 0.9 mm length) (Fig. 5F).Lateral body pouches large, extensively lobed; each lobe is a short and thick process; each pouch connecting to body by a rounded neck (Fig. 5B, E).Kidneys large, dorsoventrally elongated along posterodorsal shell margin, with numerous, red-brown or yellow, small (to 30 µm in diameter), different-size granules (Fig. 5G).Alimentary system with short oesophagus leading to a relatively large, elongate stomach; combined style sac and midgut strongly curved; hind gut forming anterior, deep, narrow loop producing rounded distinct angle, passing through heart and running posteriorly dorsal to kidney and posterior adductor muscle, opening at ventral side of posterior adductor muscle (Fig. 5H-J).Foot long, vermiform, distally bulbous, with muscular ring at junction with visceral mass.Bulbous portion not divided into two distinct parts; surface with numerous wrinkles; heel absent (Fig. 5B, D).Anterior and posterior pedal retractors wide, short, well developed.

Variability
In small specimens (up to 3 mm in shell length) the shell is relatively low, angular, with a strongly curved and anteriorly drawn-out ventral margin; the anterodorsal and posterodorsal margins gently sloping from beaks; the anterodorsal margin is concave (Fig. 2J).The shell shape and proportions, the length of the lunule and escutcheon, the degree of bending of shell margins vary among larger specimens (Fig. 2A-I, Table 1).Some of large specimens have a shell rather elongated dorsoventrally (Fig. 2I).

Differential diagnosis
The  Oliver, 2015) have a shell microsculpture consisting of calcareous spines arranged in dense radial rows (Oliver 2015).The new species described herein lacks this microsculpture.Parathyasira coani sp.nov.differs from most of other species of Parathyasira by having an anteriorly drawn-out shell, a flat, a nonexcavated lunule, and a large prodissoconch with sculpture of lamellated folds (Table 2).C).However, in contrast to P. biscayensis, P. coani sp.nov.has only about half as many filaments in the gills, compared to almost similar-sized specimens of the former species, up to 80 (specimen 7.5 mm in length) vs 150 (specimen 8.2 mm in length), respectively, and a longer ligament.Moreover, in P. biscayensis the lunule is medially elevated, while in P. coani the lunule is flat.Parathyasira coani is similar to Parathyasira fragilis Kamenev, 2020 from which it differs in having a thick, opaque and white shell, a long and thick ligament, the greater part of which is well visible externally, the foot with a bulbous distal portion not differentiated into two parts, and a different sculpture of the prodissoconch (Table 2).Parathyasira coani is also similar to Parathyasira dearborni (Nicol, 1965) in shell shape and ratios, as well as in the shape of the lunule and escutcheon, but differs by lacking microscopic irregular corrugations and pustules on the shell and a second siphonal opening, by having a larger (more than 2 ×) prodissoconch with a different sculpture (Table 2), and the lateral body pouches with a greater number of folds.

Remarks
To date, the benthic fauna of the Kuril-Kamchatka Trench is the most studied one, compared to other oceanic trenches (Belyaev 1989;Brandt et al. 2019Brandt et al. , 2020)), and the largest number of macrofaunal samples were collected with various sampling gears in its hadal zone.As a result of studying the entire material of bivalves collected in this trench (Kamenev 2019), P. coani sp.nov.was recorded only in two samples collected from the uppermost part of the trench slope at a depth of more than 6000 m.Outside of the Kuril-Kamchatka Trench, P. coani was found in many samples from the abyssal zone at depths less than 6000 m.Therefore, this species is probably a predominantly abyssal one and depths of slightly more than 6000 m are the lower limit of its vertical distribution.Apart from P. coani, seven bivalve species have a similar vertical distribution in the Kuril-Kamchatka Trench area (Kamenev 2019).As shown in the example of distribution of many macrofaunal species, depths of 6000-7000 m are a zone of transition between abyssal and hadal faunas and are the lower and upper boundaries of the vertical distribution of many abyssal and hadal macrofauna species, respectively (Belyaev 1989

Etymology
The species epithet honors Dr Paul Valentich-Scott, a well-known researcher of bivalves, who made an enormous contribution to the study of the bivalve fauna of the Pacific Ocean.His scientific works and personal assistance have been invaluably helpful in my studies of bivalves of the northwestern Pacific Ocean.(Fig. 8, Table 3).Periostracum thin, colorless, adherent.Dissoconch sculptured with closely spaced, thin, commarginal ribs and conspicuous, irregular undulations, more conspicuous near ventral margin (Figs 8C, 9A-B).Micro-sculpture of small (to 3 µm), shallow, closely spaced pits (Fig. 9C-D).Beaks small, raised, pointed, prosogyrate, anterior to midline (A/L = 0.41 ± 0.02) (Fig. 9B, Table 3).Anterodorsal shell margin long, straight, sloping rather steeply from beaks.Anterior shell margin curved, smoothly transitioning to ventral margin.Ventral margin strongly curved (Fig. 8H-K).Posterodorsal shell margin long, slightly convex, sloping steeply from beaks, forming distinct angle at transition to posterior margin.
Posterior adductor muscle small, 2 × as small as anterior one, oval.Ctenidium thin, wide, composed of both inner and outer demibranchs with fully reflected filaments (up to 45 filaments in specimen 4.3 mm in length); outer demibranch is less than half size of inner demibranch.Labial palps relatively large (to 0.5 mm in length in specimen 4.3 mm long) with small zone of sorting ridges close to junction with ctenidium (Fig. 11C).Lateral body pouches large, extensively lobed; lobes short and thick, with rounded tips; each pouch connecting to body by large, rounded neck at base of stomach (Fig. 11B, E).Kidneys large, situated below hind gut, without granules (Fig. 11E-G).Oesophagus short; stomach large, strongly elongated; combined style sac and midgut strongly curved, lying over the stomach; hind gut running posteriorly dorsal to kidney and posterior adductor muscle (Fig. 11G).Foot long, vermiform, distally bulbous, with muscular ring at junction with visceral mass.Bulbous tip not divided into two distinct parts; surface with numerous warts; heel absent (Fig. 11D).Anterior and posterior pedal retractors wide, short, well developed.

Variability
In small specimens (up to 4-5 mm in shell length) the shell is low, angulate with a strongly curved and anteriorly drawn-out ventral margin; the anterodorsal and posterodorsal margins are sloped gently from beaks; the anterodorsal margin is concave (Figs 8K, 9A, E, H).In larger specimens, the degree of obliqueness and relative length of the anterodorsal and posterodorsal shell margins vary (Fig. 8H-J).

Differential diagnosis
As was the case of P. coani sp.nov., this species differs from most species of Parathyasira in having an obliquely-rhomboidal shell with a long anterodorsal margin and a large prodissoconch with sculpture of lamellated folds (Table 2), and in lacking the dissoconch of calcareous spines.Parathyasira pauli sp.nov. is most similar to P. coani from which it differs in having a deeply excavated lunule, shorter ligament, small flattened peg beneath beak at the hinge plate.In addition, the prodissoconch of P. pauli has six lamellated folds versus five lamellated folds in P. coani The new species is also similar to P. dearborni, from which it differs in having a strongly excavated lunule, a less distinct posterior sulcus, a twice as large prodissoconch with a different number and position of lamellated folds and in lacking corrugations and pustules in the dissoconch and a second siphonal opening (Table 2).Furthermore, P. pauli is similar to P. biscayensis (Fig. 7A-C) but differs from it in having a deeply excavated lunule.

Etymology
The species epithet honors the city of Kharkov, where I was born, grew up, and was educated.
GroSS anatomy.Mantle thin, transparent; mantle edge free except at junction with gill axis (Fig. 16).
Anterior adductor muscle large, strongly elongated, curved almost parallel to anterior shell margin.
Posterior adductor muscle 3 × as short as anterior, oval.Ctenidium thin, wide, both demibranchs with fully reflected filaments (up to 60 filaments in specimen 5.2 mm in length); outer demibranch about half depth of inner demibranch (Fig. 16A, D-E).Labial palps relatively large (to 0.8 mm in length) (Fig. 16B).Lateral body pouches large, extensively lobed; numerous lobes thick, cloven or single; each pouch connecting to body by a wide neck (Fig. 16D-E).Kidneys extremely large, dorsoventrally elongated along entire posterodorsal shell margin, with numerous, pink or orange, large (to 100 µm in diameter), different-size granules well visible through transparent shell (Figs 14, 16D-H).Oesophagus short; stomach large, strongly elongated; combined style sac and midgut strongly curved, lies over stomach; hind gut forming anterior loop dorsal to style sac, running posteriorly dorsal to kidney and posterior adductor muscle.Food remains present in hindgut (Fig. 16G-H).Foot long, vermiform, distally bulbous, with muscular ring at junction with visceral mass.Bulbous tip not divided into two parts; surface with numerous, longitudinal, curved gathers; heel small (Fig. 16C, E).Anterior and posterior pedal retractors wide, long, well developed.

Variability
In small specimens (up to 5 mm in shell length), the shell is relatively low, angulate, with a strongly curved and anteriorly drawn-out ventral margin, and weakly defined lunule with valve margin junction raised; anterodorsal and posterodorsal margins are sloped more gently from beaks (Fig. 13G-H).In larger specimens, the shell shape and proportions do not vary.

Differential diagnosis
The new species described herein differs from the vast majority of species of Thyasira in having an obliquely-pyriform, anteriorly drawn-out, non-sulcate shell, with very narrow, indistinct posterior folds, large prodissoconch with thin, lamellated folds, strongly elongated, narrow adductor muscles,  I assumed that very probably the ctenidium of this species consists of two demibranchs, and after further anatomical investigation A. obliquus could be placed in the genus Thyasira (Kamenev 2020).Based on my assumption, A. obliquus was listed in the WoRMS Editorial Board (2022) under the name of Thyasira obliqua (Okutani, 1968).On the other hand, the WoRMS Editorial Board (2022) classifies the status of A. obliquus as a "taxon inquirendum".Unfortunately, it is currently not possible to examine the gills of A. obliquus, because only dry material is deposited at the NSMT (Dr Hiroshi Saito, pers.comm.).Therefore, the species still falls under the category of a taxon of uncertain taxonomic validity.

Remarks
Thyasira kharkovensis sp.nov.was recorded in the Sea of Okhotsk and on the oceanic slope of the Kuril Islands at 9 of 10 stations at depths less than 4000 m.However, this species was not found any of the 24 stations conducted in the Kuril-Kamchatka Trench area by the KuramBio (2012), SokhoBio (2015) and KuramBio II (2016) expeditions at depths greater than 5000 m (Kamenev 2015(Kamenev , 2018a(Kamenev , 2019)).Probably, T. kharkovensis sp.nov.does not occur at depths greater than 5000 m, preferring the upper abyssal zone.Previous studies showed that the deep-sea benthic fauna of the Sea of Okhotsk is closely related to the western Pacific fauna.Many species from various groups of animals that were discovered on the Kuril Basin floor (Sea of Okhotsk) were also found at the Pacific side of the Kuril Islands (e.g., Alalykina 2018, Downey et al. 2018;Fukumori et al. 2018;Kamenev 2018a;Malyutina & Brandt 2018;Mironov et al. 2018;Ostermair et al. 2018).A number of studies showed that the deep-sea Pacific fauna mainly penetrates into the Sea of Okhotsk through the deep straits of the Kuril Islands, primarily through the wide and deepest Bussol Strait (depth of 2318 m) (Ushakov 1953;Savilov 1961;Kamenev 2018a;Mironov et al. 2018).Most of deep-sea bivalve species from the Sea of Okhotsk were found in the Pacific Ocean to depths of 4000 m (Kamenev 2018a;Kamenev et al. 2022).In the Pacific Ocean, at depths greater than 5000 m, only two out of 25 species found in the abyssal zone of the Sea of Okhotsk were recorded (Kamenev 2018a(Kamenev , 2019)).Perhaps, T. kharkovensis lives in the upper abyssal zone on the oceanic slopes of the Kuril Islands and the Kamchatka Peninsula.It also penetrated into the Bering Sea through the wide and deep Kamchatka Strait (depths of more than 4000 m) and was found on the floor of the Commander Basin located opposite the Kamchatka Strait.The Bering Sea has three deepwater basins (Commander, Bowers, and Aleutian basins) connected to one another.It is possible that T. kharkovensis lives on the floor of all the basins of the Bering Sea and has a continuous distributional range from the Asian to American continent along the Aleutian Islands, inhabiting the slope of the islands.For example, the deep-sea propeamussiid bivalve Catillopecten squamiformis (Bernard, 1978) has a similar geographic and vertical distribution in the northern Pacific (Kamenev 2018b).

Discussion
Analysis of the distribution of deep-sea bivalves and thyasirids in the Atlantic Ocean showed that out of 79 thyasirid species found in the Atlantic at depths exceeding 500 m only four species are confined solely to the abyssal zone (Payne & Allen 1991;Allen 2008).Most species of thyasirids occur on the slope and were recorded at depths less than 3000 m.Down slope migration was reported for many thyasirid species (Payne & Allen 1991).
Recent studies of the benthic fauna of the deep-sea ecosystems of the northwestern Pacific Ocean have shown that thyasirids are the most species-rich bivalve family in the abyssal and hadal zones (Kamenev 2015(Kamenev , 2018a(Kamenev , 2019(Kamenev , 2020)).Many thyasirid species were found to be dominant in abundance in the abyssal benthic communities of the Seas of Japan and Okhotsk and in the hadal communities of the Kuril-Kamchatka, Japanese, Javanese, Philippine, and Kermadec trenches (Belyaev & Mironov 1977;Belyaev 1989;Kamenev 2013Kamenev , 2018aKamenev , 2019Kamenev , 2020;;Allen 2015;Kamenev et al. 2022).To date, no less than 20 species of thyasirids are known in the northwestern Pacific Ocean, which were found only in the abyssal and hadal zones (Belyaev & Mironov 1977;Belyaev 1989;Okutani et al. 1999;Okutani 2000;Allen 2015;Kamenev 2015Kamenev , 2018aKamenev , 2019Kamenev , 2020)).Thus, in contrast to the Atlantic Ocean, a species-rich deep-sea thyasirid fauna most likely lives in the northwestern Pacific Ocean solely at depths of more than 3000 m.
The sculpture of the prodissoconch of many thyasirid species is a good diagnostic character to separate and identify a number of species of the family Thyasiridae (Zelaya 2009;Kamenev 2020).In most thyasirids, the prodissoconch is smooth (Oliver & Killeen 2002;Oliver & Holmes 2007).However, some species from different regions of the world oceans have a prodissoconch sculpture of differently arranged lamellate folds or ridges (Table 2) (Oliver & Killeen 2002;Zelaya 2010;Kamenev 2013Kamenev , 2020)).Thus, in most of these species, curved prominent radial folds are symmetrically arranged along the main central axis of the prodissoconch (Zelaya 2010;Kamenev 2013Kamenev , 2020)).Moreover, the number of the radial folds, as a rule, differs greatly among species, thus being a good diagnostic character.Therefore, the presence of the radial folds on the prodissoconch of the species described herein, as well as their number, provide an additional character to distinguish them from one another and from most species of thyasirids Parathyasira coani sp.nov.and T. kharkovensis sp.nov.were found in different areas of the vast northwestern Pacific region, suggesting their wide distribution in this part of the ocean.At present, the bivalve fauna of the bottom of the Kuril Basin of the Sea of Okhotsk, the Kuril-Kamchatka Trench, the oceanic abyssal plain adjacent to the Kuril-Kamchatka Trench have been studied quite well (Filatova 1964(Filatova , 1971;;Okutani 1968Okutani , 2000;;Kamenev 2015Kamenev , 2018aKamenev , 2019)).It is possible that after a more detailed study of the fauna of the bathyal and abyssal zones of the oceanic slopes of the Japanese, Kuril, and Aleutian Islands, as well as the hadal zone of the Izu-Ogasawara, Japan, and Aleutian trenches, the ranges of these species may be expanded significantly.

Fig 3 .
Fig 3. Scanning electron micrographs of Parathyasira coani sp.nov.(MIMB 43819).A. Exterior view of right valve.B. Sculpture of beak region.C-D.Sculpture of central shell part.E. Interior view of left valve.F. Hinge plate of left valve.G. Pits under beak of left valve.H. Prodissoconch.I. Interior view of right valve.J. Hinge plate of right valve.K. Pits under beak of right valve.Scale bars: A, E, I = 1 mm; F, J = 500 µm; B-D, G, K = 100 µm; H = 50 µm.

Fig. 9 .
Fig. 9. Scanning electron micrographs of Parathyasira pauli sp.nov.(IORAS OBF collection Cat.BIV00041).A. Exterior view of right valve.B. Sculpture of beak region.C-D.Sculpture of central shell part.E. Interior view of left valve.F. Hinge plate of left valve.G. Pits under beak of left valve.H. Interior view of right valve.I. Hinge plate of right valve.J. Prodissoconch.Abbreviation: see Material and methods.Scale bars: A, E, H = 1 mm; B-C, F-G, I-J = 100 µm; D = 10 µm.

Fig. 14 .
Fig. 14.Scanning electron micrographs of Thyasira kharkovensis sp.nov.(MIMB 43836).A. Exterior view of left valve.B. Sculpture of beak region.C-D.Sculpture of central shell part.E. Interior view of left valve.F. Hinge plate of left valve.G. Interior view of right valve.H. Hinge plate of right valve.I. Hinge plate of right valve with pits.J. Pits under beak of left valve.Scale bars: A, E-H = 1 mm; B-D, I = 100 µm; J = 50 µm.

Table 2
(continued on next page).Main differentiating characters of species of Parathyasira Iredale, 1930 lacking a shell micro-sculpture of calcareous spines.