Tanaidacean faunas of the Sea of Okhotsk and northern slope of the Kuril-Kamchatka Trench

Progress in Oceanography 178 (2019) 102196

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Tanaidacean faunas of the Sea of Okhotsk and northern slope of the KurilKamchatka Trench

T

⁎

Anna Stępień , Krzysztof Pabis, Magdalena Błażewicz Department of Invertebrate Zoology and Hydrobiology, Faculty of Biology and Environmental Protection, University of Łódź, ul. Banacha 12/16, 90-237 Łódź, Poland

A R T I C LE I N FO

A B S T R A C T

Keywords: Peracarida Epibenthic sledge Species richness Faunal connectivity NW Pacific

The Sea of Okhotsk is one of the world’s largest marginal seas; its benthic fauna, especially from deeper parts, remains virtually unexplored. The material for this study was collected in the Sea of Okhotsk, Bussol Strait, and from the northern slope of the Kuril-Kamchatka Trench, during the Russian-German expedition Sea of Okhotsk Biodiversity Studies (SokhoBio) onboard the RV Akademik M.A. Lavrentyev in 2015. Material was collected using a camera-equipped epibenthic sledge (C-EBS). Forty-six tanaidacean species representing 31 genera and 12 families were found in 19 samples collected at depths from 1696 to 4798 m. All the species were new to science. The highest number of species (44) was recorded in the deepest part of the Sea of Okhotsk (Kuril Basin), followed by the northern slope of the Kuril-Kamchatka Trench (16 species) and the Bussol Strait (3 species). Almost onethird of all tanaidaceans (14 species) were common to both sides of the Kuril Island archipelago. Our results reveal a substantial faunal exchange between those two areas, although the small number of samples makes final conclusions about faunal similarity between the Sea of Okhotsk and the Pacific Ocean not fully possible. The level of rarity and patchiness of the tanaidacean fauna was high. The large number of species and individuals per sample observed in the Sea of Okhotsk might reflect high food availability in this area.

1. Introduction The Northwest (NW) Pacific is characterized by the presence of the largest marginal seas in the world: The Sea of Japan and the Sea of Okhotsk were shaped during back-arc spreading processes and are isolated from the ocean by a chain of islands (Kimura and Tamaki, 1986). The exchange of the water masses between those semi-enclosed basins and the Pacific Ocean is limited to a few narrow straits. The Bussol Strait (maximum water depth 2300 m) and Krusenstern Strait (1920 m) are the biggest and the deepest straits allowing exchange of the fauna from both sides of the Kuril Island archipelago (Brandt et al., 2018). The Sea of Okhotsk is highly productive region of the NW Pacific characterized by complex hydrography (Nürnberg and Tiedemann, 2004; Seki et al., 2004; Takahashi, 1998). High nutrient availability for the benthic organisms in this sea is associated with water discharge from one of the largest river systems in the world (Amur River) and upwelling phenomena (Chen et al., 2004; Seki et al., 2004). The presence of natural physical barriers, the complexity of current circulation, and differences in productivity between specific basins are important for speciation processes, making this region of the NW Pacific a natural laboratory for studies of biogeography and endemicity in the deep sea. The benthic fauna of this area was studied during 10 ⁎

Corresponding author. E-mail address: [email protected] (A. Stępień).

https://doi.org/10.1016/j.pocean.2019.102196

Available online 19 September 2019 0079-6611/ © 2019 Elsevier Ltd. All rights reserved.

expeditions onboard the RV Vityaz (1949, 1953–1956, 1957–1958, 1966) (Brandt et al., 2018 and references therein). In 2001, a Japanese expedition to the Kurile Kamchatka Trench and Japanese Trench was organized as a continuation of trench exploration (Larsen and Shimomura, 2007). Ten years later studies at the modern technical level, using specially designed gear, were conducted during four Russian-German research programs: SoJaBio (Sea of Japan Biodiversity Studies in 2010), KuramBio (Kuril-Kamchatka Biodiversity Studies in 2012 and 2016), and SokhoBio (Sea of Okhotsk Biodiversity Studies in 2015), all of which aimed to conduct comprehensive analysis of benthic species richness in the deepest areas of the NW Pacific (Alalykina, 2018; Błażewicz-Paszkowycz et al., 2015; Brandt et al., 2018; Downey et al., 2018; Golovan, 2018; Golovan et al., 2013, 2018; Kamenev, 2018; Maiorova and Adrianov, 2018; Malyutina et al., 2018; Malyutina and Brandt, 2018; Frutos and Jażdżewska, 2019). In some collections the percentage of new species was as much as 90% of the collected fauna (Brandt et al., 2018; Golovan, 2018). The SokhoBio expedition has supported investigation of the poorly studied part of the NW Pacific—the deepest part of the Sea of Okhotsk—and its potential link to the Pacific slope by assessing the composition and distribution of the benthic fauna (Brandt et al., 2018). The tanaidaceans are good model organisms for these kinds of studies.

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A. Stępień, et al.

Table 1 State of knowledge of Tanaidacea in Nortwestern Pacific: Sea of Japan, Sea of Okhotsk, Kurile- Kamchatka Trench (KKT) and Japanese Trench (JS). Species/Family

Depth range

area

Source

Apseudidae Apseudes nipponicus Shiino, 1937 Paradoxapseudes littoralis (Shiino, 1952) Fageapseudes vitjazi (Kudinova-Pasternak, 1970) Fageapseudes bicornis (Kudinova-Pasternak, 1973) Fageapseudes brachyomos Bamber, 2007 Carpoapseudes spinigena Bamber, 2007 Carpoapseudes varindex Bamber, 2007 Carpoapseudes sp.

intertidial intertidial 5050–5095 3350–3620 5473–5733 965–974 3145–3265 1172–1219

Hayama, Pacicfic coastline Seto, Pacicfic coastline KKT Sea of Okhotsk JT and sourrounded area JT and sourrounded area JT and sourrounded area JT and sourrounded area

Shiino, 1937 Shiino, 1952 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1973 Bamber, 2007 Bamber, 2007 Bamber, 2007 Bamber, 2007

Metapseudidae Synapseudes setoensis Shiino, 1951 Apseudomorpha albida (Shiino, 1951)

intertidial intertidial

Seto, Pacicfic coastline Seto, Pacicfic coastline

Shiino, 1951 Shiino, 1951

Parapseudidae Parapseudes algicola (Shiino, 1952)

intertidial

Seto, Pacicfic coastline

Shiino, 1952

455–1356

Sea of Japan

Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

Agathotanaidae Paragathotanais zevinae (Kudinova – Pasternak, 1970) Agathotanais cf. ingolfi Hansen, 1913 Agathotanais splendidus Kudinova-Pasternak, 1970 Paranarthrura vitjazi Kudinova-Pasternak, 1970 Agathotanais hadalis Larsen, 2007 Paragathotanais abyssorum Larsen, 2007 Agathotanais misakiensis Kakui & Kohtsuka, 2015 Agathotanais toyoshioae Kakui & Kohtsuka, 2015

3620–5240 4895–5240 5441 3853–5762 5473–5733 5762–5733 211–493 95

KKT KKT KKT KKT; JT JT JT Sagami Sea Sea of Japan

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970; Larsen, 2007 Larsen, 2007 Larsen, 2007 Kakui and Kohtsuka, 2015 Kakui and Kohtsuka, 2015

Akanthophoreidae Tumidochelia cf. dentifera (Sars, 1896) Akanthophoreus cf. gracilis (Krøyer, 1842)

4895–6225 20–60; 4895–6710 3385–4895 3272–3146 5733–7433 3145–3265 5473–5484 5473–5762 3146–3858 455–2637 455–994

KKT KKT; JT; Sea of Japan; Middle Kurile KKT; Sea of Japan JT JT KKT KKT KKT; JT KKT; JT Sea of Japan Sea of Japan

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970, 1976, 1984; Bird, 2007b; Kussakin and Tzareva, 1972 Kudinova-Pasternak, 1970, 1984 Bird, 2007a Bird, 2007a Bird, 2007a Bird, 2007a Bird, 2007a Bird, 2007a Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013 Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

517–2637

Sea of Japan

Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

3146–7433 7795–8015 200–1113 517–1356

KKT; JT JT Sea of Japan Sea of Japan

Bird, 2007; Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1976 Kudinova-Pasternak, 1984 Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

4895–6135 3146–7433 517–1356

KKT KKT; JT Sea of Japan

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970; Bird, 2007 Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

4895–6710

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 McLelland, 2007

Sphyrapodidae Pseudosphyrapus malyutinae Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013

Chauliopleona cf. armata (Hansen, 1913) Akanthophoreus sp.KK#1 Akanthophoreus sp.KK#3 Akanthophoreus sp.KK#5 Parakanthophoreus crassicaudus (Bird, 2007) Parakanthophoreus imputatus (Bird, 2007) Akanthophoreus undulatus Bird, 2007 Chauliopleona hansknechti Larsen & Shimomura, 2007 Akanthophoreus lispopygmos Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Parakanthophoreus verutus (Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013) Anarthruridae Siphonolabrum tenebrosus Bird, 2007 Anarthruropsis langi Kudinova-Pasternak, 1976 Anarthruropsis longa Kudinova-Pasternak, 1984 Keska sei Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Colletteidae Collettea cf. cylindrata (Sars, 1882) Leptognathiopsis langi (Kudinova-Pasternak, 1970) Nippognathiopsis petila Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Cryptocopidae Cryptocopoides arcticus (Hansen, 1887) Cryptocope sp. Cryptocopoides pacificus McLelland, 2007

3145–5484

KKT KKT KKT; JT

Heterotanoididae Heterotanoides ornatus Kudinova-Pasternak, 1976

7370

JT

Kudinova-Pasternak, 1976

Kalliapseudidae Phoxokalliapseudes tomiokaensis (Shiino, 1966)

intertidial

Tamioka, Pacicfic coastline

Shiino, 1966

Leptocheliidae Makassaritanais modestus (Kussakin & Tzareva, 1972) Makassaritanais itoi (Ishimaru, 1985) Chondrochelia savignyi (Kroyer, 1842)

20–41 intertidial intertidial

Middle Kurile Oshoro Bay, Sea of Japan Oshoro Bay, Sea of Japan

Kussakin and Tzareva, 1972 Ishimaru, 1985 Ishimaru, 1985

Leptognathiidae Leptognathia tuberculata Hansen, 1913 Leptognathia breviremis (Lillieborg, 1864) Leptognathia parelegans Kudinova-Pasternak, 1970

4895 4845–7295 5240

KKT KKT KKT

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970

(continued on next page) 2

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Table 1 (continued) Species/Family

Depth range

area

Source

Leptognathia Leptognathia Leptognathia Leptognathia Leptognathia Leptognathia

4945 7000–8700 3146–4945 8185–8400 5473–5484 3853–7433

KKT KKT KKT; JT JT KKT KKT; JT

Kudinova-Pasternak, Kudinova-Pasternak, Kudinova-Pasternak, Kudinova-Pasternak, Bird, 2007b Bird, 2007b

Neotanaidae Neotanais wolffi Kudinova-Pasternak, 1966 Neotanais americanus Beddard, 1886 Neotanais tuberculatus Kudinova-Pasternak, 1970 Neotanais oyashio Bamber, 2007 Neotanais kuroshio Bamber, 2007 Neotanais sp.

6156–6207 4895–5240 4840–5876 5733–5762 5733–5762 5762–5733

JT KKT KKT JT JT JT

Kudinova-Pasternak, 1966 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Bamber, 2007 Bamber, 2007 Bamber, 2007

Paratanaidae Metatanais cylindricus Shiino, 1952 Paratanais impressus Kussakin & Tzareva, 1972

intertidial 3–40

Seto, Pacicfic coastline Middle Kurile

Shiino, 1952 Kussakin and Tzareva, 1972

4260–6065 510–3425 3145–3858 517–994

KKT KKT Sea of Japan KKT Sea of Japan

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1984 McLelland, 2007 Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

455–521

Sea of Japan

Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

517–1356

Sea of Japan

Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

455–465 3146–3272

Sea of Japan KKT

Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013 Bird, 2007

18–3570

Sea of Japan

Kudinova-Pasternak, 1984

lake

zenkevitchi Kudinova-Pasternak, 1970 sp. rotundicauda Kudinova-Pasternak, 1970 greveae Kudinova-Pasternak, 1976 microcephala Kudinova-Pasternak, 1978 aneristus Bird, 2007

Pseudotanaidae Pseudotanais vitjazi Kudinova-Pasternak, 1966 Pseudotanais sp. 1 Pseudotanais affinis Hansen, 1887 Pseudotanais nipponicus McLelland, 2007 Pseudotanais intortus Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Pseudotanais abathogaster Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Pseudotanais soja Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013 Pseudotanais sp. nov. A Pseudotanais sp. 2 Tanaellidae Tanaella forcifera (Lang, 1968)

1970 1970 1970; Bird, 2007 1976

Tanaididae Sinelobus stanfordi (Richardson, 1901) Tanaididae gen. sp. Protanais birsteini (Kudinova-Pasternak, 1970)

6090–6135

Kurile Islands; river in Osaka KKT KKT; dead wood

Arctotanais alascensis (Richardson, 1899) Zeuxo normani (Richardson, 1905) Zeuxo coralensis Sieg, 1980 Zeuxo kurilensis (Kussakin & Tzareva, 1974)

42–48 10–34 intertidial intertidial

Middle Kurile Middle Kurile Yoshi Island, Sea of Japan Yoshi Island, Sea of Japan

Stephensen, 1936; Ariyama and Ohtani, 1990 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970; Błażewicz-Paszkowycz et al., 2015 Kussakin and Tzareva, 1972 Kussakin and Tzareva, 1972 Sieg, 1980 Sieg, 1980

Tanaopsidae Tanaopsis curtus Kudinova-Pasternak, 1984 Tanaopsis rugaris Błażewicz-Paszkowycz, Bamber & Jóźwiak, 2013

200–510 455–465

Sea of Japan Sea of Japan

Kudinova-Pasternak, 1984 Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013

Typhlotanaidae Torquella grandis (Hansen, 1913) Typhlamia mucronata (Hansen, 1913) Meromonakantha setosa (Kudinova-Pasternak, 1966) Typhlotanais kussakini Kudinova-Pasternak, 1970 Typhlotanais longicephala Kudinova-Pasternak, 1970 Peraeospinosus rectus (Kudinova-Pasternak, 1966) Peraeospinosus magnificus (Kudinova-Pasternak, 1970)

4945–6135 4840–6710 4895–6051 5240–6135 4895–5340 3610–7370 3146–4895

KKT KKT KKT KKT KKT KKT; JT KKT; JT

Typhlotanais cornutus (Sars, 1879) Typhlotanais simplex Kudinova-Pasternak, 1984

20 435–1130

middle Kurile Sea of Japan

Paratyphlotanais japonicus Kudinova-Pasternak, 1984

2511–3560

Sea of Japan

Torquella angularis (Kudinova-Pasternak, 1966) Typhlotanais compactus Kudinova-Pasternak, 1966 Larsenotanais kamchatikus Błażewicz-Paszkowycz, 2007

5473–5484 3146–5484 3145–3265

JT KKT and sourrounding area KKT and sourrounding area

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970, 1976 Kudinova-Pasternak, 1970; Błażewicz-Paszkowycz, 2007 Kussakin and Tzareva, 1972 Kudinova-Pasternak, 1984; Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013 Kudinova-Pasternak, 1984; Błażewicz-Paszkowycz, Bamber and Jóźwiak, 2013 Błażewicz-Paszkowycz, 2007 Błażewicz-Paszkowycz, 2007 Błażewicz-Paszkowycz, 2007

Paratanaoidea incertae sedis Exspina typica Lang, 1968 Robustochelia robusta (Kudinova-Pasternak, 1970) Leptognathioides sp.KK#1

2400–4829 4945–5240 5473–5484

KKT KKT KKT

Kudinova-Pasternak, 1970 Kudinova-Pasternak, 1970 Bird, 2007

species richness of the deep-sea tanaidaceans from various regions of the world (Pabis et al., 2014, 2015; Błażewicz-Paszkowycz et al., 2015; Golovan et al., 2018a). Currently more than 1300 species are recognized, however analysis based on the World Register of Marine

The majority of these species spends their whole lives in mucous tubes incrusted with bottom substrates. They lack planktonic larval stages and are assumed to have limited dispersal abilities (BłażewiczPaszkowycz et al., 2012). Moreover, recent studies demonstrated high 3

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2.2. Sampling

Species (WoRMS) demonstrated that the number of species is probably at least an order of magnitude higher; Most of the species collected during various deep-sea expeditions are new to science (Appeltans et al., 2012; Błażewicz-Paszkowycz et al., 2012). One hundred and seventy-six species of tanaidaceans were recorded from the NW Pacific, including the Sea of Okhotsk and neighbouring areas (Kuril Kamchatka Trench, Japan Trench, and Sea of Japan); 99 of them are formally described (see Table 1) and almost all studies have been concerned with taxonomy. Forty-six species have been recorded in the Kurile Kamchatka Trench, including 34 species described by Kudinova-Pasternak (1970) based on the of the R/V Vitjaz expeditions, and 12 species described in 2007 (Bamber, 2007; Bird, 2007a, 2007b; Błażewicz-Paszkowycz, 2007; Larsen, 2007; Larsen and Shimomura, 2007; McLelland, 2007). In the material collected during the KuramBio expedition, 77 species were recorded, but are not as yet formally described (Golovan et al., 2018a). Twenty-seven species are known so far from the Japanese Trench (Kudinova-Pasternak, 1966, 1970, 1976; Bird, 2007a, 2007b; Błażewicz-Paszkowycz, 2007; Bamber, 2007; Larsen, 2007), while 25 species have been described from the Sea of Japan, (Kudinova-Pasternak, 1984; Błażewicz-Paszkowycz et al., 2013; Kakui and Kohtsuka, 2015). Tanaidacean fauna of the Sea of Okhotsk are poorly studied. Only eight species have been described, with the majority recorded in the shallows (Kussakin and Tzareva, 1972; Stephensen, 1936). Only one species was found in the deep-sea (about 3500 m depth, Kudinova-Pasternak, 1973). Despite all the above-mentioned studies the tanaidacean species composition of this region is still vastly underestimated and many species are waiting for taxonomic descriptions (Golovan et al., 2018a). The aim of our study was to make a first species richness assessment of the deep-sea tanaidacean fauna of the Sea of Okhotsk based on material collected during the SokhoBio expedition. Data collected on both sides of the Kuril Island archipelago also allowed for analysis of distribution patterns and comparison of species composition and abundance between the Sea of Okhotsk, Bussol Strait, and the northern slope of the Kuril-Kamchatka Trench.

Material was collected during the SokhoBio expedition in July and August of 2015 onboard the RV Akademik M.A. Lavrentyev, using a camera-equipped epibenthic sledge (C-EBS, Brandt et al., 2013). The samples collected are semiquantitative. Tanaidacea were found in 19 samples from 11 working sites (Fig. 1, Table 2). Thirteen samples were collected at eight working sites distributed in the Kuril Basin: one from the bathyal zone (1696 m) and 11 from the abyssal zone (3296–3366 m). Two samples from one working site were collected in the Bussol Strait at depths 2267–2333 m and four samples from two working sites were collected on the northern slope of the Kuril-Kamchatka Trench (3206–3574 m, Malyutina et al., 2018). The samples were washed on board with use of cold sea water, sieved on 300 µm mesh, and fixed in 96% ethanol. For the present study the supra- and epibenthic fractions from each sample were combined. The material was sorted according to the cooling chain protocol (Riehl et al., 2014). 2.3. Data analysis Tanaidaceans were identified to morphospecies using a Leica M125 microscope. Mean species richness (S = number of species per sample) and mean number of individuals were calculated with standard deviations for the Sea of Okhotsk (13 samples) and for the northern slope of the Kuril-Kamchatka Trench (4 samples). The level of rarity of tanaidacean species was assessed. Rare species were defined as singletons (represented by only one individual), doubletons (represented by two individuals), and tripletons (represented by three individuals). Additionally, the numbers of unique species (species found in one sample only) and duplicates (species found in two samples) were recorded. The frequency of occurrence (F = percentage of samples containing a species relative to the total number of samples) was calculated for each species in the whole material, and for the Sea of Okhotsk and northern slope of the Kuril-Kamchatka Trench separately. Similarity among all 19 samples was calculated based on standardized abundance data (relative abundance as a percentage was used) because trawling distances of EBS samples were not standardized to 1000 m (see Brandt et al., 2018). This procedure is appropriate for samples that are not fully comparable. Hierarchical agglomerative clustering was performed using the group average method based on the Bray-Curtis formula (Bray and Curtis, 1957). Data were square root transformed before the analysis in order to reduce the influence of dominant species on the results. A SIMPROF test with 5% significance level was performed in order to check multivariate structure within groups (Clarke and Gorley, 2015). The species accumulation curve was constructed with 999 permutations. The curve plotted the cumulative number of different species observed as each new sample was added. All calculations were performed in Primer 6 (Clarke and Gorley, 2006).

2. Material and methods 2.1. Study area The Sea of Okhotsk is a semi-enclosed basin, located between 60°N and 55°N (Preller and Hogan, 1998). The sea is divided into a shallow northern part, less than 200 m deep, and a southern deep-sea basin (3372 m maximum depth), called the Kuril Basin (Preller and Hogan, 1998). Low oxygen concentration (10% saturation) is typical at depths of about 1000 m (Freeland et al., 1998), whereas below 1000 m oxygen concentrations increase, reaching about 20–25% saturation at depths of 2000–3000 m. During the SokhoBio expedition biochemical components of sediments were measured. Organic carbon concentrations varied between 0.84 and 1.92%, with the highest values in the western part of the Kuril Basin (Table 2). The southwestern part of the Sea of Okhotsk is surrounded by the Kuril Islands archipelago (Seki et al., 2004). The sea is connected with the Pacific Ocean through about 26 straits, of which Kruzenshtern Strait (1900 m) and Bussol Strait (2300 m) are the deepest (Brandt et al., 2018). Warm, salty, nutrient-poor Pacific waters of the East Kamchatka Current flow through Kruzenshtern Strait to the Sea of Okhotsk. This water mass moves in a northern direction, and anticlockwise, so the flow within the sea is cyclonical. The water mass later spreads southward with the East Sakhalin Current. The East Kamchatka Current flows out from the sea via Bussol Strait (Ohshima, 2002). In the south, the Sea of Okhotsk is connected to the Sea of Japan via the shallow Soya and Tartary Straits.

3. Results Altogether 46 tanaidacean species (2112 specimens) representing 31 genera and 12 families were recorded from the Kuril Basin, Bussol Strait, and northern slope of the Kuril-Kamchatka Trench. All the species are new to the science (Table 3). The majority of species belonged to the suborder Tanaidomorpha; only two species represented suborder Apseudomorpha. The most speciose families were Typhlotanaidae, with eight species and three genera, followed by Pseudotanaidae with seven species and three genera (Table 3). The highest number of individuals was reported for family Agathotanaidae (799, 37% of the material) and Typhlotanaidae (330, 15% of the material). The species accumulation curve did not reach an asymptote, demonstrating under-sampling of the area (Fig. 2). The number of rare species was relatively low. Six singletons (13%), three doubletons (6%) and three tripletons (3%) were recorded in the studied material. Twenty-eight species were 4

5 26.07.2015 26.07.2015 28.07.2015 29.07.2015

9–7

10–5

10–7

24.07.2015

8–5

9–6

24.07.2015

8–4

46°16.097N 152°02.706E 46°16.164N 152°03.095E 46°07.410N 152°11.292E 46°06.027N 152°14.439E

46°08.875N 146°00.256E 46°05.037N 146°00.465E 46°40.961N 147°28.283E 46°41.094N 147°27.386E 46°37.996N 148°59.363E 47°12.127N 149°37.136E 47°12.039N 149°36.950E 48°37.377N 150°00.546E 48°03.258N 150°00.581E 48°03.234N 150°00.468E 46°56.556N 151°05.013E 46°57.466N 151°05.068E 45°36.792N 146°22.589E 46°36.388N 151°34.567E 46°36.357N 151°34.912E

Start of trawling*

* Based on Artemova et al. (2018), Golovan (2018) and Malyutina et al. (2018).

Northern slope of the KurilKamchatka Trench

Bussol Strait

20.07.2015

6–6

01.08.2015

18.−19.07.2015

5–7

11–6

17.07.2015

4–10

22.07.2015

17.07.2015

4–9

7–4

15.07.2015

3–9

22.07.2015

13.07.2015

2–8

7–3

13.07.2015

2–7

20.07.2015

10.07.2015

1–9

6–7

10.07.2015

1–8

Sea of Okhock

Date*

Stationsample*

Region

46°16.132N 152°03.036E 46°16.070N 152°03.324E 46°07.310N 152°11.537E 46°05.827N 152°14.576E

46°08.441N 145°59.259E 46°08.727N 146°00.227E 46°40.761N 147°28.467E 46°41.157N 147°27.710E 46°37.821N 148°59.822E 47°11.951N 149°36.990E 47°12.212N 149°36.754E 48°37.269N 150°00.334E 48°03.200N 150°00.517E 48°03.122N 150°00.145E 46°56.791N 151°04.860E 46°57.494N 151°04.917E 45°36.882N 146°22.502E 46°36.477N 151°34.464E 46°36.390N 151°34.780E

End of trawling*

Table 2 Depth and location of samples, together with number of species and individuals per sample.

4769–4798

4681–4702

3371–3377

3386–3377

2327–2330

2333–2341

3210

3300

3299

3350–3351

3347

1696–1699

3366

34.582 – – – – – – – –

– – – – – – – –

34.589

34.593

34.493

1.849

1.877

1.875

2.107

34.593

–

– 1.882

34.580

1.882

3363 3366

–

–

3351–3352

34.575

34.609

Salinity [PSU] *

34.580

1.883

1.882

Temperature [°C] *

1.890

3351–3353

3307

3307

Depth [m] *

1.92 1.56

– –

1.83

1.83

– –

1.34

1.34

0.95

0.95

1.36–1.92

–

–

–

–

–

0.84

0.84

– –

1.24

3

20

16

1

2

6

609

43

276

5

14

1

– 1.24

120

75

7

276

422

96

120

number of individuals [N]

1.18

1.18

1.45

–

1.872

1.204

1.835

–

1.833

1.56

1.92

–

–

Corg [%]*

Oxygen [mg/ L] *

2

10

7

1

2

1

29

15

30

4

10

1

12

11

4

20

26

16

19

number of species [S]

A. Stępień, et al.

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Fig. 1. Distribution of sampling stations (SO – Sea of Okhotsk, BS – Bussol Strait, KK - northern slope of the Kuril-Kamchatka Trench).

4. Discussion

represented by less than 20 individuals (Table 3). Twelve species were classified as unique, and eight as duplicates. Only nine species had frequency of occurrence higher than 40% (Table 2). Only five species were recorded in more than 10 samples (Fig. 3). Samples collected in the Sea of Okhotsk were generally more speciose and characterized by higher numbers of individuals than in the Bussol Strait and northern slope of the Kuril-Kamchatka Trench. In total 44 species were found in the Sea of Okhotsk, 16 species were recorded on the northern slope of the Kuril-Kamchatka Trench, and only three species were found in the Bussol Strait. The number of species per sample in the Sea of Okhotsk ranged from 1 to 30, with a mean of 15.1 ± 9.4. There were 1–2 species/sample in the Bussol Strait and 1–10 species/sample in the northern slope of the Kuril-Kamchatka Trench, with mean 5.0 ± 4.2. Numbers of individuals in samples from the Sea of Okhotsk varied from 1 to 609 (mean 158.7 ± 186.9), in the Bussol Strait from 2 to 6 and in northern slope of the Kuril-Kamchatka Trench from 1 to 20 (mean 10.0 ± 4.2) (Table 2). Fourteen species were common between the Sea of Okhotsk and northern slope of the Kuril-Kamchatka Trench. Three species were common between the Sea of Okhotsk and Bussol Strait. The most frequent species recorded in both areas was Leptognathia sp. 1 (84% of samples from the Sea of Okhotsk and 75% of samples from northern slope of the Kuril-Kamchatka Trench). The second most frequent species was Pseudotanais sp. 1 (61% of samples from the Sea of Okhotsk and 75% of samples from the northern slope of the Kuril-Kamchatka Trench) (Table 3). The similarity analysis based on the Bray-Curtis formula did not reveal a clear pattern: the majority of samples was grouped into a single cluster at a low level of similarity and were not differentiated by SIMPROF. Only the samples collected in the Bussol Strait and two samples from the northern slope of the Kuril-Kamchatka Trench clearly differed from those collected in the Sea of Okhotsk (Fig. 4).

4.1. Species richness in the NW Pacific Tanaidacean fauna of the Sea of Okhotsk, Bussol Strait, and the northern slope of the Kuril-Kamchatka Trench analysed from 19 C-EBS samples yielded a high number of species (Table 2). All of them are new to science, confirming that the deep-sea tanaidacean species number is greatly underestimated (Appeltans et al., 2012; Błażewicz-Paszkowycz et al., 2012). Species richness assessments conducted in earlier tanaidacean studies from other parts of the NW Pacific based on a comparable number of EBS samples demonstrated different results. Seventyseven species from 11 families were recorded in the abyssal plain (4900–5800 m depth) in the vicinity of the Kuril-Kamchatka Trench (Golovan et al., 2018a). A much lower number of species was observed in the Sea of Japan (Błażewicz-Paszkowycz et al., 2013), where tanaidacean fauna were represented by only 15 species recorded from bathyal and upper abyssal zones (455–3666 m) (Błażewicz-Paszkowycz et al., 2013). A similar trend was observed for other peracarids and for polychaetes (Alalykina, 2018; Golovan et al., 2018a). High numbers of isopod species (245), amphipod species (70) and cumacean species (70) were found in the Kuril Kamchatka Trench area (Golovan et al., 2018a), while in the Sea of Japan only 22 species of isopods, 65 species of amphipods, and 36 species of cumaceans were collected (Golovan et al., 2013). Furthermore, 37% of tanaidacean genera found in the Sea of Okhotsk were also found in the region of the Kuril-Kamchatka Trench, but only 8% were found in the Sea of Japan. Differences in total species number between those seas most probably reflect different levels of productivity and different geological history, including level of isolation, which was already suggested in earlier studies (Brandt et al., 2018). Connection between water masses of the Sea of Japan and Pacific Ocean is sustained through shallow straits (< 200 m) resulting in effective isolation of this basin from the Pacific Ocean (Tyler, 2002); The Sea of Okhotsk is connected with the open ocean through the deep straits allowing faunal exchange (Brandt et al., 2018). The connections between the Sea of Japan and the Sea of Okhotsk are shallow 6

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Table 3 Frequency of occurrence (F), total number of individuals (N) in the whole tanaidacean material and in each of studied areas. Family/species

Kuril Basin

Bussol Strait

Northern slope of the Kuril-Kamchatka Trench

Total

F [%]

N

F [%]

N

F [%]

N

F [%]

N

Apseudidae Apseudes sp. 1 Apseudopsis sp. 1

7.7 7.7

1 11

– –

0 0

– –

0 0

5.3 5.3

1 11

Acanthophoreidae Acanthophoreus sp. 1 Chaulipleona sp. 1 Paracanthophoreus sp. 1 Paraleptognathia sp. 1 Paraleptognathia sp. 2

61.5 76.9 30.8 7.7 15.4

33 51 4 1 5

– – 50 50 –

0 0 1 6 0

– 25.0 – – –

0 1 0 0 0

42.1 57.9 26.3 10.5 10.5

33 52 5 7 5

Agathotanaidea Agathotanais sp. 1 Paranarthrura sp. 1 Paragathotanais sp. 1 Paragathotanais sp. 2

84.6 84.6 38.5 46.2

484 113 37 46

– – – –

0 0 0 0

25.0 – – 25.0

1 0 0 1

63.2 57.9 26.3 36.8

485 113 37 47

53.8 23.1 7.7 53.8 7.7

10 5 1 20 1

– – – – –

0 0 0 0 0

– – 25.0 – 25.0

0 0 1 0 1

36.8 15.8 10.5 36.8 10.5

10 5 2 20 2

Colleteidae Colletea sp. 1 Leptognahiopsis sp. 1 Leptognahiopsis sp. 2 Leptognathiella sensu abyssi

7.7 38.5 7.7 7.7

1 37 2 1

– – – –

0 0 0 0

– – – 25.0

0 0 0 2

5.3 26.3 5.3 10.5

1 37 2 3

Cryptocopoidae Cryptocopoides sp.1

38.5

43

50

1

25.0

1

36.8

45

Leptognathidae Leptognathia sp. 1 Leptognathia sp. 2

84.6 69.2

166 41

– –

0 0

75.0 –

3 0

73.7 47.4

169 41

Neotanaidae Neotanais sp. 1

76.9

85

–

0

–

0

52.6

85

Pseudotanaidae Pseudotanais sp. 1 Pseudotanais sp. 2 Pseudotanais sp. 3 Pseudotanais sp. 4 Pseudotanais sp. 5 Pseudotanais sp. 6 Pseudotanais sp. 7

61.5 7.7 38.5 7.7 23.1 30.8 7.7

24 2 19 1 13 19 3

– – – – – – –

0 0 0 0 0 0 0

75.0 – 25.0 – – – –

8 0 1 0 0 0 0

57.9 5.3 31.6 5.3 15.8 21.1 5.3

32 2 20 1 13 19 3

Tanaellidae Araphura sp. 1 Tanaella sp. 1

61.5 38.5

47 266

– –

0 0

– –

0 0

42.1 26.3

47 266

Typhlotanaidae Torquella sp. 1 Typhlamia sp. 1 Typhlotanais sp. 1 Typhlotanais sp. 2 Typhlotanais sp. 3 Typhlotanais sp. 4 Typhlotanais sp. 5 Typhlotanais sp. 6

46.2 69.2 15.4 61.5 30.8 7.7 15.4 30.8

26 98 3 154 6 9 3 13

– – – – – – – –

0 0 0 0 0 0 0 0

25.0 25.0 – 25.0 – 25.0 – –

1 2 0 3 0 3 0 0

36.8 52.6 10.5 47.4 21.1 10.5 10.5 21.1

27 100 3 157 6 12 3 13

incerte sedis Leptognathoides sp. 1 Paranarthrurella sp. 1 Pseudoarthrura sp. 1 incerte sedis gen sp. 1 incerte sedis gen sp. 2

– 7.7 7.7 – 7.7

0 3 1 0 2

– – – – –

0 0 0 0 0

25.0 – – 25.0 –

1 0 0 1 0

5.3 5.3 5.3 5.3 5.3

1 3 1 1 2

Anathruridae Anarthruridae gen Anarthruridae gen Anarthruridae gen Anarthruridae gen Anarthruridae gen

sp. sp. sp. sp. sp.

1 2 3 4 5

result, the number of species of this sea is generally low and some species representing typical shallow water fauna were recorded in the abyssal depths of the Sea of Japan. In the case of tanaidaceans one such species is Chaulipleona chansknechti Larsen and Shimomura (2007). It was primarily known from the shelf of the Pacific coast of Japan (260–278 m) (Larsen and Shimomura, 2007) and it was later found in

(< 150 m) (Seki et al., 2004). It is also hypothesized that an anoxic period during the Last Glacial Maximum had consequences for distribution and composition of current fauna in the Sea of Japan (Tyler, 2002; Golovan et al., 2013). According to Tyler (2002), the postglacial period, when the Sea of Japan was anoxic, was too short for the benthic organisms to colonize and radiate in the deeper part of the sea. As a 7

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Fig. 2. Species accumulation curve of Tanaidacea from the Sea of Okhotsk and northern slope of the Kuril-Kamchatka Trench.

Fig. 3. Species richness related to the number of stations (number of species found in one, two, three… twenty EBS samples).

the Kuril Island chain (Maiorova and Adrianov, 2018) as well as 17 out of 25 species of bivalves (Kamenev, 2018). Similar patterns were observed for other peracarids collected during the SokhoBio expedition. Golovan (2018) found 10 species of isopods common to the Sea of Okhotsk and the abyssal zone in the vicinity of the Kurile-Kamchatka Trench. Nevertheless, tanaidaceans are assumed to have restricted dispersal abilities associated for example with a tubiculous life style (Błażewicz-Paszkowycz et al., 2012) and it is somewhat surprising that almost one third of the species were recorded in both areas. Moreover, the number of samples collected on the northern slope of the KurilKamchatka Trench was low and we might expect higher similarity of species composition.

the Sea of Japan between 450 and 2600 m (Błażewicz-Paszkowycz et al., 2013; Golovan et al., 2013).

4.2. Species composition on both sides of the Kuril Islands Our study indicated tanaidacean species that were found on both sides of the Kuril Islands chain. Thirty percent of species were common to both areas, which is high taking into account the low mobility of tanaidaceans and the large scale of the sampled area. Almost all species recorded in 4 samples collected on the northern slope of the KurilKamchatka Trench and all 3 species found in the Bussol Strait were also recorded in the Sea of Okhotsk. Contact of water masses between the Pacific Ocean and the Sea of Okhotsk allows for faunal exchange and it was already demonstrated that those two basins share many species, especially those associated with the continental shelf (Brandt et al., 2018 and references therein). More than half of 160 species of deep-sea polychaetes were common to both above-mentioned areas (Alalykina, 2018), although molecular differentiation of species of the family Sternaspidae recorded presence of cryptic species (Kobayashi et al., 2018). A few species of sipunculans were also common to both sides of

4.3. Abundance and species richness per sample The comparatively high number of species and specimens per sample observed in the Sea of Okhotsk in relation to Pacific stations might be related to differences in local conditions, e.g. in food availability, although large standard deviations, low numbers of samples, and semiquantitative character of the sampling gear allows for only 8

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dataset at the higher taxonomic level, but temperature, salinity and oxygen content were relatively homogeneous at all sites, except for station 5, which was characterized by lower oxygen saturation and higher temperature (Brandt et al., 2018; Kamenev, 2018). Similarity analysis (Fig. 4) did not reveal a clear pattern due to low abundance of species, patchy distribution, and high number of singletons. Division between Kurile Basin and northern slope of Kurile Kamchatka Trench was found in the study based on analysis of desmosomatid isopods from the same set of samples (Golovan, 2018). High level of rarity and/or patchiness (30 to even 80% of singletons) and generally low abundance are typical features of the deep-sea tanaidacean communities (Pabis et al., 2014, 2015; Błażewicz-Paszkowycz et al., 2015). Nevertheless, the number of singletons (13% of all species) recorded in the Sea of Okhotsk was relatively low compared to earlier deep-sea tanaidacean studies, although it is difficult to compare results collected at different spatial scales and in different geographic areas. High level of rarity might also result from under-sampling bias (Błażewicz-Paszkowycz et al., 2015; Jóźwiak et al., in Press; Kaiser and Barnes, 2008; Kaiser et al., 2009). For example, some of the rare species, such as Anarthruridae gen sp. 5 (only two specimens recorded in two samples only) were found in the Kuril Basin and on the Pacific slope, so its distribution is wider than we would expect based on the number of individuals collected. 4.4. Concluding remarks Our study indicated a high number of species in the Kuril Basin, with much lower species number in the Bussol Strait and the northern slope of the Kuril-Kamchatka Trench. The relatively large number of species (30%) occurring on both sides of the Kuril Islands chain, or presence of very frequently encountered species like Leptognathia sp. 1 (found in 84% of the samples) shows a great need for more detailed studies describing possible dispersion routes of the deep-sea tanaidaceans by molecular techniques. There is also a great need for more intensive sampling in the Bussol Strait. If the species richness and abundance of this strait is really as low as observed in our results, the environmental conditions along the strait are most probably crucial for faunal linkage between the Pacific Ocean and the Sea of Okhotsk, especially in the case of the smallest representatives of macrozoobenthos characterized by direct development, such as the Tanaidacea.

Fig. 4. Dendrogram of samples for Bray-Curtis similarity (group average method) based on standardized and square-root transformed data. (Spotted lines indicate the stations that cannot be significantly differentiated by SIMPROF; SO – Sea of Okhotsk, BS – Bussol Strait, KK - northern slope of the Kuril-Kamchatka Trench).

Declaration of Competing Interest

very preliminary conclusions. The Kuril Basin is in general recognized as rich in nutrients owing to the East Sakhalin Current transporting organic particles from the shelf to deeper parts of the sea (Seki et al., 2004). The concentration of total organic carbon (TOM) is highest in the southwestern part of the Kuril Basin (1.6–1.9%) and decreases to the northeast, with the lowest concentrations near the Bussol Strait (0.8–1.1%) (Artemova et al., 2018). Moreover, the strong current that flows through the Bussol Strait prevents accumulation of the sediments and potential colonization by endobenthic invertebrates (Alalykina, 2018), while on the Pacific slope the concentration of TOC was lower (1.3–1.8%) compared to the Kuril Basin (Artemova et al., 2018). Our results might reflect those differences. For example, a high number of species and high abundance were found at stations 11, 1, and 2 located in the southwestern part of the Kuril Basin, where food availability is higher, while low abundance was found in samples collected in Bussol Strait, although only one station was sampled in this area. A similar pattern was found for polychaetes and bivalves based on the analysis of the same set of SokhoBio samples and it was also linked with differences in organic matter content (Alalykina, 2018; Kamenev, 2018). Generally, our results showed highly patchy distribution of tanaidaceans. For example, 193 out 266 specimens of Tanaella sp. 1 were recorded in one sample. Similar results were obtained for the same

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements This is KuramBio publication # 66. The material from the Sea of Okhotsk was collected during the SokhoBio expedition with the RV Akademik M.A. Lavrentyev with the financial support of the Russian Science Foundation (Project No. 14-50-00034) and sorted with the financial support of the PTJ (German Ministry for Science and Education), grant 03G0857A to Prof. Dr. Angelika Brandt, University of Hamburg. This study was financed by NCN grant 2016/13/B/NZ8/ 02495. References Alalykina, I.L., 2018. Composition of deep-sea polychaetes from the SokhoBio expedition with a description of a new species of Labioleanira (Annelida: Sigalionidae) from the Sea of Okhotsk. Deep. Res. Part II Top. Stud. Oceanogr. 154, 140–158. https://doi. org/10.1016/j.dsr2.2018.04.004. Appeltans, W., Ahyong, S.T., Anderson, G., Angel, M.V., Artois, T., Bailly, N., Bamber, R., Barber, A., Bartsch, I., Berta, A., Błazewicz-Paszkowycz, M., Bock, P., Boxshall, G.,

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