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Biogeographic Atlas of the Deep NW Pacific Fauna
expand article infoHanieh Saeedi§|, Angelika Brandt§
‡ Senckenberg Research Institute and Natural History Museum, Frankfurt am Main, Germany
§ Goethe University Frankfurt, Biosciences, Institute for Ecology, Evolution und Diversity, Frankfurt am Main, Germany
| OBIS Data Manager, Deep-Sea Node, Frankfurt am Main, Germany
Open Access

FOREWORD

University of Southampton, UK & Tammy Horton – National Oceanography Centre, Southampton, UK

Only 150 years ago, life in the deep oceans was virtually unknown. Reaching these depths was a goal of early explorers and naturalists, such as those of the Challenger Expedition (1872–76). They were rewarded with astonishing discoveries of a wealth of diverse life in the deep sea. Since these early ventures, expeditions to study this realm have increased in regularity and scope, continuing to reveal extraordinary life-forms across the globe.

Experts in deep-sea taxonomy and ecology have worked together for four Russian-German and German-Russian expeditions in the NW Pacific deep sea (Sea of Japan, Sea of Okhotsk, Kuril-Kamchatka abyssal plain and the Kuril-Kamchatka Trench). This book provides a summary of the findings of these experts following the many hours of subsequent sample-processing and analyses, revealing a treasure trove of critical fundamental knowledge of life in our deep oceans.

Human influence in remote deep-sea ecosystems is rapidly increasing. Exploitation of abiotic and biotic resources and the varied use of the vast space on the seafloor and deep water-column is realised through advancing technologies and the growing need by a growing population for materials, food and new genetic resources. Today, the entire deep ocean is affected by human pressures including fishing, pollution, climate change, with new emerging industries such as deep seabed mining on the horizon. A quarter of all species described on our planet are threatened with extinction due to human activities, yet most deep-sea animals are not yet even known to science. Their discovery and description of unknown species is at the heart of biology. Taxonomists provide this critical baseline knowledge. The Deep-Ocean Stewardship Initiative (www.dosi-project.org) has a vision of a healthy deep ocean able to contribute to the wider Earth system, through its sustainable management informed by independent science. The information gleaned by this project and published in the “Biogeographic Atlas of the Deep NW Pacific Fauna” will be used to further deep-ocean stewardship via the dedicated science-policy interface facilitated by DOSI.

In order to effectively manage activities in the deep sea, fundamental baseline biodiversity data are needed upon which to base predictive models and appropriate and operational legislation. Such datasets are rare, with basic information on the taxonomy, biodiversity, and biogeography of many faunal groups lacking, or found across numerous disparate sources. This new volume brings together for the first time this much-needed knowledge on the NW Pacific fauna > 2,000 m.

We wish to applaud the devoted and timely work of the chief editors of this book, Hanieh Saeedi and Angelika Brandt, for bringing together this rich, revealing and important work of global significance. The importance of taxonomic expertise in the provision of baseline biogeographic data is clearly evident in this book. A comparatively small group of dedicated experts worldwide work hard to identify, describe and study our deep-sea fauna gaining indispensableknowledge for humankind. We thank them all.

Chapter 1. INTRODUCTION: BIOGEOGRAPHIC ATLAS OF THE DEEP NW PACIFIC FAUNA

aSenckenberg Research Institute and Natural History Museum, Marine Zoology Department, Senckenberganlage 25, 60325 Frankfurt am Main, Germany
bGoethe University Frankfurt, Biosciences, Institute for Ecology, Evolution und Diversity, Max-von-Laue-Str. 13, 60438 Frankfurt am Main, Germany
cOBIS Data Manager, Deep-Sea Node, Frankfurt am Main, Germany
Email: hanieh.saeedi@senckenberg.de*

1. The deep NW Pacific

The deep sea is the largest, but the least explored environment on Earth. However, less than 0.0001% of the deep sea (deeper than 200 m) has been explored so far, making it the least explored environment on Earth (Brandt and Malyutina 2015; Danovaro et al. 2017). Deep-sea macrobenthos are speculated to comprise about 25 million species; meiofauna seems to be composed of 20 to 30 million species (Adrianov 2004), in contradiction with what was estimated previously for deep-sea macrofauna (between 0.5 and 10 million species) (Brandt et al. 2007a; Brandt et al. 2007b; Grassle and Maciolek 1992). Appeltans et al. (2012) predicted that 100,000 species will be described in the next 50 years if the rate of 2,000 new species description per year maintains in the future (Appeltans et al. 2012). Recent expeditions in the framework of the Census of Marine Life have documented that deep-sea biodiversity is very unevenly distributed in different oceans and ocean basins (Ramirez-Llodra et al. 2010). However, some mechanisms have been identified that can cause high local species concentrations (e.g., productivity and isolation) (Brandt et al. 2007a; Gibson et al. 2002; Levin et al. 2001; Saeedi et al. 2019a; Smith and Stockley 2005).

The NW Pacific is one of the most productive, nutrient rich, and diverse regions of the World Ocean, and includes several deep-sea basins diverging in depths, hydrology, and isolation (Grebmeier et al. 2006; Leprieur et al. 2016; Renema et al. 2008; Saeedi et al. 2019b). The Sea of Japan, the warm temperate zone of the NW Pacific, and the Kuril-Kamchatka Trench (KKT) receive two major currents: the warm Tsushima and cold Oyashio currents (Fujikura et al. 2010; Su et al. 1990) (Map 1). The Tsushima Current splits from the Kuroshio Current and flows from off Kyushu into the Sea of Japan. The Oyashio Current flows southward through Japanese waters from off Hokkaido along the Pacific coast (Fujikura et al. 2010; Su et al. 1990). The tropical and subtropical parts of the western Pacific host the highest number of marine species around the world (Asaad et al. 2018; Crame 2000; Jablonski et al. 2006; Krug et al. 2008; Sanciangco et al. 2013). Some areas of the Sea of Japan, Sea of Okhotsk, and Kuril-Kamchatka Trench (KKT) have been specifically sampled and studied by deep-sea scientists (Brandt et al. 2020; Brandt and Malyutina 2015; Malyutina and Brandt 2013; Malyutina et al. 2018). In the next few paragraphs we review the geography and hydrology of these three ecosystems.

Map 1.

Study area, sampling locations, and currents in three areas from four expeditions. Colored circles show 418 sampling effort coordinate points (per sampling gear per station per cruise) during four deep-sea cruises including Sea of Japan Biodiversity Study (SoJaBio, 2010), Kuril-Kamchatka Biodiversity Study (KuramBio I and II, 2012–2016), and Sea of Okhotsk Biodiversity Study (SokhoBio, 2015). The area KuramBio is represented by the two expeditions KuramBio I in 2012 (open abyssal of NW Pacific) and Sea of Okhotsk; SoJ: Sea of Japan; KKT: Kuril-Kamchatka Trench; EKC: East Kuril Current; ESC: East Sakhalin Current; KC: Kuroshio Current; NPC: North Pacific Current; OC: Oyashio Current; OG: Okhotsk Gyre; SC: Soya Warm Current; WKC: West Kuril Current. ArcMap 10.5.1 was used to create this figure.

1.1. Sea of Japan

The Sea of Japan is a young and broadly enclosed marginal sea of the NW Pacific (Fujikura et al. 2010; Malyutina and Brandt 2013; Su et al. 1990). The Sea of Japan is geographically isolated and has an abnormally high level of dissolved oxygen in its deeper parts; however, its bottom-water oxygen level has declined up to 8–10% in the past three decades (Elsner et al. 2013; Huang et al. 2019; Huang et al. 2018). The abyssal depths of the Sea of Japan were formed in the Cenozoic as a caldera of the mainland (Malyutina and Brandt 2013). The largest and deepest part of the Sea of Japan is the Japan Basin, reaching a depth of ca. 3,800 m. The two other deep basins are the Yamato and the Tsushima (Ulleung), which are separated from the Japan Basin by the Yamato Rise (Fig. 1 in Malyutina and Brandt 2013). The Sea of Japan has been and still is connectedto the Pacific Ocean through two shallow straits, the Tsushima Strait in the south (about 140 m depth), and the Tsugaru Strait between Honshu and Hokkaido in the north (about 130 m depth) (Malyutina and Brandt 2013). Two even shallower straits, the Soya Strait (La Perouse) between Hokkaido and Sakhalin (50–53 m depth), and the Tatar Strait between Sakhalin and the Asian continent (around 10 m depth) connect the Sea of Japan to the Sea of Okhotsk (Malyutina and Brandt 2013). However, the Sea of Japan is isolated by shallower straits compared to the Sea of Okhotsk and this isolation may affect species and community composition, endemicity, and biodiversity in this area (Brandt et al. 2019; Brandt et al. 2013; Golovan et al. 2013; Kamenev 2013; Malyutina and Brandt 2013; Saeedi et al. 2019b; Saeedi et al. 2019d; 2020).

1.2. Sea of Okhotsk

The Sea of Okhotsk is a marginal sea which is separated by the Kuril Islands (on the southeast) and the Kamchatka Peninsula (on the east) from the Pacific Ocean. The Sakhalin Islands are located in the western part of the Sea of Okhotsk where it is connected to the Sea of Japan on either side of Sakhalin. The total area of the Sea of Okhotsk is 1,616,700 km2 and the abyssal zone occupies ca. 8% of this total area (Glukhovsky 1998; Malyutina et al. 2018). The Kuril Basin with a maximum depth of 3,372 m is the deepest and oldest part of the Sea of Okhotsk. There is water exchange between the abyssal Kuril Basin and the Pacific Ocean via the bathyal depths of the Krusenstern and Bussol straits allowing the exchange of reproductive propagules of the pelagic and benthic fauna between these two body waters (Malyutina et al. 2018; Tyler 2002).

1.3. Kuril-Kamchatka Trench (KKT)

The KKT is an oceanic trench in the NW Pacific. The Kamchatka Strait (KS) with a width of 190 km is located between the Kamchatka Peninsula and the Bering Island, and occupies 46% of the total area of the straits connecting the Bering Sea and the Pacific Ocean (Prants et al. 2013; Stabeno 1999). The maximum depth of the Kamchatka Strait, connecting the Kuril-Kamchatka Trench to the Aleutian Trench, is 4,420 m, and because it is deeper than the maximum depth of the Bering Sea, Kamchatka Strait water content can penetrate all the depths of the basin (Prants et al. 2013; Stabeno 1999). The KKT area is strongly influenced by the Kamchatka Current, which transports water from the Bering Sea (Prants et al. 2013; Sattarova and Artemova 2015). The water temperature of the Kamchatka Current ranges between 0 to 5°C in winter and 8 to 16°C in summer depending on winter conditions in the Okhotsk and Bering seas (Sattarova and Artemova 2015). The water transport through the KS and straits of the Aleutian Island chain plays an important role in the volume, heat, and nutrient fluxes between the Bering Sea and the North Pacific (Prants et al. 2013; Sattarova and Artemova 2015; Stabeno 1999). The climate of this area is controlled by monsoon circulation, which defines the climatological features and weather conditions, particularly large seasonal variations in temperature as well as air and water in the surface layers (Sattarova and Artemova 2015).

2. Expedition history and motivation

Several biological expeditions to the deep NW Pacific onboard the Russian RV Vityaz were performed between 1949 to 1966. The data found on faunal taxonomic description, hydrology, topography, chemical characteristics, and organic matter of the Kuril-Kamchatka Trench (KKT) and the adjacent abyssal plain area were reported in many publications (Belyaev 1989; Belyaev 1983; Ushakov 1953; Vinogradova 1977; Zenkevitch et al. 1955). Moreover, Sirenko et al. (2013) published a check list of species of free-living invertebrates of the Russian Far Eastern Seas. Isopoda (Crustacea) was one of the dominant taxa in species richness of the abyssal KKT area and one of the most well studied (Birstein 1970; 1971; Birstein 1963; Kussakin 1971; 1988; 1999; Kussakin and Vasina 1990; Kussakin 2004).

In the past decade, the biology of the bathyal, abyssal, and hadal faunas of all size classes (meio- macro-, and megabenthos) of the NW Pacific have been intensively investigated based on a Memorandum of Understanding (2007) between Russian and German partners. A total of four Russian-German and German-Russian expeditions (with the RV Akademik M.A. Lavrentyev and RV Sonne) have provided a wealth of data on the systematics, evolution, and biogeography of the deep-sea faunas of the Sea of Japan (SoJaBio 2010) (Malyutina and Brandt 2013), Sea of Okhotsk (SokhoBio 2015) (Malyutina et al. 2018), the Kuril-Kamchatka Trench (KKT), and the NW Pacific open abyssal plain adjacent to the KKT (KuramBio I and II, 2012–2016) (Brandt et al. 2019; Brandt et al. 2018; Brandt et al. 2020; Brandt and Malyutina 2015) (Map 1). All specimens were collected using standard gear (CTD, MUC (multicorer), GKG (giant box corer), EBS (epibenthic sledge), AGT (Agassiz Trawl), WT (bottom trawl) (Brandt and Malyutina 2014), BC (box corer) (Brandt et al. 2010), and PN (plankton net) (Chernyshev and Polyakova 2018)being deployed following a standardized method (Brandt and Malyutina 2014).

The goals of these expeditions were to study the biodiversity, biogeography, and evolution of the benthic organisms in different NW Pacific deep-sea environments. We aimed to compare more isolated deep-sea basins with more easily accessible ones (Sea of Japan vs. Sea of Okhotsk) and to test whether the hadal bottom of the trench of the KKT isolates the fauna from the Sea of Okhotsk to the fauna of the open NW Pacific area. The faunal composition of these areas comprising systematic, ecological, and biogeographical data, as well as evolution of protists, selected invertebrate taxa and fish, has been published in four scientific volumes, and includes the formal descriptions of many species, some genera, and one family (Brandt et al. 2020; Brandt and Malyutina 2015; Malyutina and Brandt 2013; Malyutina et al. 2018; Saeedi et al. 2020).

Based on these expeditions, the Beneficial project (Biogeography of the northwest Pacific fauna. A benchmark study for estimations of alien invasions into the Arctic Ocean in times of rapid climate chance) was designed. The main aims of the Beneficial project were 1- digitizing the biodiversity and environmental data collected during our expeditions, 2- discovering the deep-sea biogeography and biodiversity patterns in the NW Pacific, 3- predicting the potential future distribution range shifts of key species from the NW Pacific to the Arctic Ocean under rapid climate change, and 4- compiling a novel book on the taxonomy and biogeography of the highly abundant key species. All the data, publications, and the book arising from this project provide crucial benchmarks and datasets for any deep-sea biodiversity assessment, and help predict the future status of the Arctic marine ecosystem in a changing environment (Brandt et al. 2020; Canonico et al. 2019; Saeedi et al. 2019b; Saeedi et al. 2019c; Saeedi et al. 2019d; 2020; Saeedi et al. 2019e).

3. The Beneficial project highlights

We mined and mobilized 7,042 unique deep-sea benthos taxa records, with 1,723 records at the species level (more than 50% at the speciesand genus level, the rest were at the higher taxa level, mostly family, order, and class) from our four deep-sea cruises including SoJaBio, SokhoBio, and KuramBio I and II (Saeedi et al. 2019e). Using this dataset and data collected from the open-access databases, we analysed species richness, endemicity, and community composition in the shallow and deep NW Pacific and its adjacent Arctic Ocean (Saeedi et al. 2020, Brandt et al. 2020; Canonico et al. 2019; Saeedi et al. 2019b; Saeedi et al. 2019c; Saeedi et al. 2019d; Saeedi et al. 2019e). Our findings supported the hypothesis that biodiversity, while highest in the tropics and coastal depths (mostly in the Philippines), decreases at the equator and decreases at depths below ca. 2,000 m (Saeedi et al. 2019b; Saeedi et al. 2019d). Despite high species richness in the eastern Philippines, the Yellow Sea and Gulf of Tonkin had the highest benthic species endemicity rates (ca. 70%), while the Aleutian Islands had the highest pelagic endemicity rate (ca. 45%) among all different ecoregions (Saeedi et al. 2019b; Saeedi et al. 2019d). Our generalized linear models (GAMs) showed that the combined effects of all environmental predictors produced the best model driving species richness in both shallow and deep sea in the NW Pacific (Saeedi et al. 2019b; Saeedi et al. 2019d; 2020). However, among all predictors, dissolved oxygen, bottom temperature, and salinity were the most important environmental drivers of the deep-sea species richness in the NW Pacific and the adjacent Arctic Ocean (Saeedi et al. 2019b; Saeedi et al. 2019d; 2020). These investigations should strengthen and inform marine protection plans as species richness and endemicity hotspots could be profoundly compelling in helping to pinpoint and prevent biodiversity loss.

4. Book outline

This book is designed as a guide, synthesis, and review of the current knowledge of the benthic fauna in the NW Pacific. This book includes benthic species that are distributed in the bathyal and abyssal zones (below 2,000 m) of the NW Pacific (latitude ca. 30 to 60°N, longitude ca. 120 to 180°E) (Map 2). This book consists of 21 chapters, with an introduction followed by 20 chapters on taxonomy and biogeography of different deep-sea taxa including Porifera, Cnidaria, Brachiopoda, Entoprocta, Nemertea, Solenogastres, Bivalvia, Sipuncula, Polychaeta, Echiura, Nematoda, Kinorhyncha, Pygnogonida, Ascothoracida, Ostracoda, Decapoda, Amphipoda, Isopoda, Ascothoracida, Tanaidacea, Echinoidea and Asteroidea. The editors worked closely with the authors and ensured that the work being produced has suitable literary merit and is free from inconsistencies, including grammatical and spelling errors. However, all the chapters proofread by the authors and all authors must take public responsibility for the content of their chapter. A total number of 2,503 distribution records belonged to 503 deep-sea taxa were used in the 20 chapters of this book (Map 2). A list of species represented in this book is given in supplementary table 1 (https://doi.org/10.3897/ab.e51315.suppl-1). The highest numbers of distribution records used in this book were from latitudes 40–48°N belonging to the materials were collected during the four joint Russia-Germany expeditions (Map 3).

Map 2.

Distribution records of all 503 deep-sea taxa used in 20 chapters of this book (see supplementary table 1).

Map 3.

Total number of distribution records used in 20 chapters of this book calculated per ca. 50,000 km2 hexagonal cells. The highest numbers of distribution records (100 to 362 records) used in this book were from latitudes 40–48°N belonging to the materials were collected during our four expeditions.

5. Taxonomic impediment

In this book, we aimed to include chapters on the major groups of benthic fauna that are especially species rich (or being very diverse). However, for some taxa including Bryozoa, Harpacticoida, Crinoidea, Ophiuroidea, Holothuroidea, and Tunicata we were not able to find expert taxonomists with the time and/or the necessary skills to complete chapters.

6. Impacts of this book

In times of rapid climate change and increasing anthropogenic impact, a compilation of life at the seafloor in the deep sea, where environmental parameters resemble those of the Arctic Ocean, is urgently needed. To date; however, there has been no compilation and synthesis of deep-sea biodiversity in the deep NW Pacific excluding Sirenko’s (2013) species list of free-living invertebrates of the Russian Far Eastern seas (Sirenko 2013). It is thus necessary to accurately assess deep-sea areas to establish biodiversity conservation plans and Marine Protected Areas (MPAs).

6.1. Biodiversity and ecosystem services

Based on such urgent needs, this book is very timely and provides not only insights into NW Pacific deep-sea benthic biodiversity and species compositions; but also forms a fundamental regional study of the NW Pacific required for understanding the ecosystem services (e.g., culture and human well-being, fisheries, watercirculation and CO2 exchange, and nutrient cycling) and decision-making assessments in order to prioritize conservation criteria across multiple biodiversity conservation initiatives and groups such as the Deep Ocean Stewardship Initiative (DOSI), International Seabed Authority (ISA), the Polar Prediction Project (PPP), the Intergovernmental Panel on Climate Change (IPCC), and Conservation of Arctic Flora and Fauna (CAFF). This book also represents an important backbone study for the United Nations Decade of Ocean Science for Sustainable Development assessment (2021–2030) to ensure that ocean science can support nations’ activities to sustainably manage the oceans and to in particular to reach the goals of the 2030 Agenda for Sustainable Development such as sustainable consumption and production, natural resources management, effective institutions, good governance, and the rule of law and peaceful societies.

6.2. Climate change implications

Understanding and preserving the biodiversity of the NW Pacific is an important challenge in this area of rapid climate change, particularly given the potential of alien species invasions into the Arctic Ocean. There are already many benthic species shared between the NW Pacific and the adjacent Arctic Ocean (Saeedi et al. 2019d). Initially, an embayment of the North Pacific, the deep Arctic Ocean was impacted by the northern Pacific fauna until ca. 80 million years prior to the deep-water connection closed (Bodil et al. 2011). As Arctic Sea ice loss continues with its implications for governance, economics, and society (Carmack et al. 2015), this book provides information on highly abundant key species which might potentially invade the Arctic Ocean in future (both from hadal and also shallower deep-sea depths of the NW Pacific) under climate change scenarios including decreasing sea-ice conditions. Our data and book will serve as a solid basis and benchmark for predicting potential species invasions or migrations supported by the retreat of the Arctic Ocean sea ice.

6.3. Community and citizen science

This book is published as open-access and is this publically available to a broad range of communities including the deep-sea researchers and citizen scientists. The book contains taxonomic information and images that can be used by scientists as identification keys or for citizen science projects such as iNaturalist. The geographic distribution data provided in this book are a significant contribution to the open-access database communities, including the Global Biodiversity Information Facility (GBIF) and Ocean Biogeographic Information System (OBIS).

6.4. Science-policy interface

This book integrates information on distribution and biodiversity of many unique deep-sea species in the NW Pacific for the first time, providing fundamental information required by intergovernmental bodies such as the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES). This information can be used to assess the present and future status of deep-sea biodiversity as requested by governors and decision makers to improve the strategic plans for the conservation and sustainable use of biodiversity, long-term human well-being, and sustainable development.

Acknowledgements

This book could not be published without the financial support of “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project“ (BENEFICIAL project)” funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany (grant number 03F0780A). We also gratefully acknowledge the generous funding of this book publication by the Open Access Publication Fund of Goethe University. We would like to thank the captains and crews of RVs ‘Akademik M.A. Lavrentyev’ and ‘Sonne’, student helpers, and anyone else who contributed to sample management and sorting the specimens. Special thanks to Mark Costello for his advice and Marianna Simões for her help in this book project. A very special thanks to James Reimer for editing and English proofreading of this chapter and to Rachel Downey for English proofreading most of the chapters of this book.

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Chapter 2. PORIFERA: TAXONOMY AND BIOGEOGRAPHY OF PORIFERA ALONG THE NW PACIFIC

aFenner School of Environment and Society, Australian National University, Linnaeus Way, Canberra, ACT 2601, Australia
bBiowissenschaften, Goethe Universität, Max–von–Laue Strasse 9, D–60438 Frankfurt am Main, Germany
cForschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, D–60325 Frankfurt am Main, Germany
Email: rachel.v.downey@gmail.com*

1. Introduction

1.1. Biology and Ecology

Despite being the largest biome on Earth, deep-sea environments remain poorly mapped and understood, with our current knowledge of sponge distribution biased to regions with a history of deep-sea research (Hogg et al. 2010; Ramirez-Llodra et al. 2010). In the deep sea, below 2,000 m, 60 sponge families, 158 genera and 387 species are known to science (OBIS 2019). Globally, 4% of sponge species are known to occur at depths greater than 2,000 m and these are dominated by firstly demosponges (66% families, and 55% of both genera and species) and secondly hexactinellids (glass sponges) (23% families, 41% genera, and 44% species). Calcareous (five families, five genera, five spp.) and homoscleromorph sponges (1 family, genus and species) are not known to be rich in species, genera or families in the deep sea (van Soest et al. 2012).

In general, demosponges are far more dominant in the deep NW Pacific Ocean, in terms of species, compared to hexactinellids; however, there is variability noted in abundance, with the Sea of Okhotsk greatly dominated by hexactinellid individuals, whereas demosponge individuals dominate the Kuril-Kamchatka abyssal plain (Downey and Janussen 2015; Downey et al., 2018). Only one calcareous sponge specimen is known from the NW Pacific (Koltun 1972). All demosponges are composed of siliceous spicules and/or skeleton of spongin fibres, hexactinellids (glass sponges), are composed entirely of siliceous spicules, and calcareous sponges have calcified spicules (Van Soest et al. 2012). Many irregular growth forms are found within the demosponge class (Bergquist 1978); however, in the deep NW Pacific Ocean, stalked sponges were dominant (Figure 1). Hexactinellids are generally symmetrical, and can be composed of a stalk with a cup, or vase-like in shape, and these growth forms were both encountered in the NW Pacific Ocean. The small calcareous specimenhas not been observed by our team; however, it was likely to be either encrusting or tubular in morphology. Many hexactinellids and several deep-sea demosponge genera possess basal root tufts, stalks, and a fringe at the base of their bodies, which enable them to successfully anchor their bodies in deep-sea environments, where soft sediments are common (van Soest et al. 2012).

Figure 1.

From left to right, several examples of branched carnivorous sponges and stalk and cup, and vase morphologies of hexactinellid sponges from the NW Pacific.

Sponges are generally filter feeders; however, in the deep sea, food supply can be scarce, and limited to particular seasons or oceanic current systems, and so sponge genera and species that live in this part of the ocean are highly adapted to sporadic food supplies (Gage and Tyler 1991; Smith et al. 2008). It has been found that filter-feeding sponges in the same habitat consume picoplankton to different efficiencies (Perea-Blázquez et al. 2013), and so despite food limitation, potentially many species can thrive in deep-sea regions. Hexactinellid sponges are often dominant components in the deep sea, including sectors of the NW Pacific (Koltun 1966, 1967, 1972; Downey et al. 2018), and contribute significantly to the biomass, species diversity and abundance in all deep-sea oceans (Tabachnick 1994; Reiswig 2002; Leys 2003). However, one diverse and abundant deep-sea sponge family has evolved carnivory, the Cladorhizidae Dendy, 1922, within the Demospongiae Sollas, 1885 class (Hestetun et al. 2016), likely as a novel adaptive response to reduced nutrient supply in the deep sea (Vacelet and Boury-Esnault 1995, 1996). These sponges have modified micro-skeletal features that are hook-like, enabling them to catch small invertebrates, such as crustaceans (Vacelet and Duport 2004). The Cladorhizidae family dominate in terms of species richness in the NW Pacific Ocean (Koltun 1972), particularly in the Sea of Okhotsk, in which they comprise two-thirds of all demosponges, and the Kuril-Kamchatka abyssal plain, in which nearly 90% of demosponge species are from this carnivorous family (Downey and Janussen 2015; Downey et al. 2018). Global analyses have indicated that the NW Pacific Ocean may be a global hotspot of this carnivorous family, with one known endemic genus (Koltunicladia Hestetun, Vacelet, Boury-Esnault, Borchiellini, Kelly, Rios, Cristobo & Rapp, 2016) and at this point 20% (35 spp.) of all known Cladorhizid species (173 spp., WORMS 2019), which includes identified species morphotypes from recent studies that have not been formerly described.

Deep-sea sponges are characteristically slow growing, can reach vast sizes, and are often long-lived (Hogg et al. 2010). Growth measurements of NW Pacific sponges have not been undertaken; however, deep-sea sponges in other sectors of the North Pacific have indicated that hexactinellid species grew very slowly, at 1.98 cm per year and individuals were likely to be 220 years old (Leys and Lauzon 1998). Another study dated deep-sea hexactinellid siliceous spicules from another species, and estimated an age of 11,000 years (Jochum et al. 2012). Due to their long lives, some deep-sea sponges can exhibit gigantism, growing to immense sizes, with the largest known individual, a hexactinellid from 2,117 m depth from the NW Hawaiian Islands, which was greater than 3.5 m in length (Wagner and Kelley 2016). However, in the NW Pacific Ocean, referring to the Sea of Okhotsk and the Kuril-Kamchatka abyssal plain, most sponges were less than 2 cm in height, with only small numbers of demosponges (typically from the Cladorhizidae family), and stalked hexactinellids, achievingsizes greater than 5 cm (Downey and Janussen 2015). This dominance of smaller specimens could partly be due to the use of the epi-benthic sledge, which collects smaller macrofauna, picking up greater numbers of younger sponges and/or species exhibiting dwarfism. The use of trawl gear damages sponges, and so fragile glass sponges could have been significantly larger in the NW Pacific, and more characteristically typical of gigantism as seen in other sectors of the North Pacific Ocean.

Despite the likely slow-life of deep-sea sponges, recent research has found that these sponges are far more dynamic. There are few long-term studies of sponge demography and metabolism; however, one long-term study of hexactinellids in the adjacent NE Pacific found that these sponges responded positively to increases in food particulates, increasing their density and body size, and these fluctuated with changes in the ocean currents and gyres in this region (Kahn et al. 2012). This indicates that NW Pacific sponges could respond in a similar fashion, likely being dynamic in their response to seasonal changes in food supply. Sponge metabolisms are known to vary considerably (Witte and Graf 1996), between species, genera, and families; however, there are no known studies in the NW Pacific Ocean. One study in the Southern Ocean, which has highly seasonal productive waters, found that some sponges had a 25% metabolic decrease in the food-poor winter, compared to up to a 6-fold increase in the food-rich summer months (Morley et al. 2016). This could indicate that deep-sea sponges are likely to be able to adjust their metabolic physiology, at species level, to feed, grow, and reproduce when conditions alter in the deep sea. Our knowledge of growth, metabolism, and demography of many sponge species, particularly smaller and encrusting deep-sea sponges, is limited, due to the difficulty in sampling and monitoring species that grow very slowly and variably (McMurray et al. 2008).

Deep-sea sponges are likely to be ‘K-strategists’, with low reproduction rates and reproductive efforts due to limited energy availability (Ramirez-Llodra et al. 2010). No reproductive research has been undertaken on NW Pacific deep-sea sponges; however, reproduction is expected to be seasonal, with key triggers for reproduction likely to be a rise in water temperature and/or primary production (Lanna et al. 2007; Hogg et al. 2010). Most sponge species are hermaphrodites; however, in some species, separate individuals produce sperm and egg cells. Patterns of sexual and asexual reproduction vary from one family to another; however, they are still poorly known, especially for deep-sea species (Hogg et al. 2010). Sponges currently known from the NW Pacific, according to general literature on sponge reproduction (Ereskovsky 2018), are likely to be hermaphrodites which exhibit viviparity (eggs are retained in the body until they develop), which includes hexactinellids and most of the demosponges found in this region. A small selection of demosponges in the deep NW Pacific, in the families and order of Polymastiidae, Suberitidae, and Tetractinellida, are typically not hermaphrodites, and practice oviparity (eggs develop outside of the sponge). Many of the NW Pacific sponges are likely to produce lecithotrophic (non-feeding) larvae, which enable sponges to disperse and thereby have broader ranges (Maldonado 2006). Most sponges are also likely to reproduce asexually, by either budding, fragmentation or gemmulogensis.Despite little being known about the specific reproductive strategies of deep-sea sponges, it appears that there are likely multiple reproductive options. In the NW Pacific Ocean, sponges are more likely to be hermaphrodites, they also, more often than not, protect their eggs, they generally release larvae that could disperse across the vast deep-sea regions, and they can reproduce both sexually and asexually, which could increase their opportunities to increase their abundance and distribution when the environment changes rapidly.

1.2. Habitat

Most deep-sea habitats are heterotrophic, dependent upon the flux of organic matter (marine snow) photosynthetically produced in the surface ocean (Ramirez-Llodra et al. 2010). Food limitation has and continues to shape many deep-sea habitats, yielding some of the lowest biomass and productivity of faunal communities (Rex et al. 2006; Rowe et al. 2006). However, this is not the case with seamounts, seabed beneath upwelling regions, and canyons, which have higher levels of productivity, and therefore, biomass and diversity, due to topographic modification of currents and enhanced food particle transport (Ramirez-Llodra et al. 2010). Large sectors of the NW Pacific Ocean are known to be areas of upwelling, such as the Sea of Okhotsk, the Kuril-Kamchatka Trench, Kamchatka Peninsula, Sea of Japan, and the Bering Sea (Zhabin et al. 2017). Results from the Sea of Okhotsk indicate that sponges in this region are richer and more abundant than areas sampled on the Kuril-Kamchatka abyssal plain, which is not in an area of upwelling (Downey et al. 2018). However, we do not know enough about other regions in this sector to understand the potential role of upwelling in structuring sponge habitats; however, there is the possibility that sponge fauna could be richer in these regions.

So far, 28 deep-sea habitats have been described globally, and geological, physical and geochemical processes (GOODS 2009; Ramirez-Llodra et al. 2010) likely drive their differences. For many of these habitats, their coverage is still unknown and very few of them have been sampled adequately. Much of the Sea of Okhotsk and Kuril-Kamchatka abyssal plain were found to be composed of fine muds, with occasional stones, which appeared to be more common in the Sea of Okhotsk. Some deep-sea sponges anchor themselves on hard substrata, such as rock, cobbles and gravel found on ridges and trenches, which have been found in this region (Downey and Janussen 2015; Downey et al. 2018). Sponges are typically more diverse on harder substrates (Ramirez-Llodra et al. 2010; van Soest et al. 2012), and this could partly explain the differences in richness and composition of sponge habitats found closer to the Kuril islands (Downey et al. 2018). However, hard substrate habitats are not present throughout most of the deep sea, and that includes the NW Pacific Ocean too. Several demosponge and hexactinellid families and genera, are adapted to live in these soft-bottom, bathyal and abyssal environments (75% of the deep-sea floor) (Hogg et al. 2010), and many of these were encountered in the Kuril-Kamchatka abyssal plain, although they tended to be less diverse sponge habitats (Downey and Janussen 2015).

Deep-sea sponges are known to provide living, complex-structured habitat on the seabed, and sponge habitats are found to be potentiallysignificant centres of invertebrate and vertebrate (fish) diversity (Klitgaard 1995; McCormick 1994; Cleary and de Voogd 2007; Hogg et al. 2010). Tubes and stalks of dead and living sponges provide elevated structures in the vast areas of soft, muddy floor in bathyal and abyssal regions. They act as habitat structures for many encrusting and motile suspension feeders, producing ‘habitat islands’ in the deep sea which can be used as nurseries, feeding platforms, and areas of refuge for predators and prey (Beaulieu 2001). Complex, hard substrate is scarce in the deep sea, and so episodic recruitment of living (and the death of sponges) creates habitats, that are likely to play a critical role in deep-sea biodiversity, as they increase the area and type of micro-habitats at differing stages of succession (Hogg et al. 2010). In the NW Pacific Ocean, several dead sponge stalks were found that were encrusted with corals (refer to Chapter 15), which highlights that some sponges do provide deep-sea habitat in this sector of the ocean. However, our current understanding of the roles sponges play in sustaining deep-sea biodiversity, and the connectivity of these habitats of the NW Pacific Ocean, remains limited due to the difficulty in sampling and monitoring these patchy habitats.

1.3. Geographical Distribution

There are currently 3907 online records of deep-sea (>2,000 m) sponges globally, with over half of these records from the North Pacific Ocean (OBIS 2019). Previously, our knowledge of North Pacific Ocean sponge fauna had been partial (e.g. reviewed in Downey and Janussen 2015; Downey et al. 2018), with less than 6% of databased global sponge distribution records found in this deep-sea region in 2017. However, our knowledge of deep-sea sponge fauna in the NW Pacific Ocean has increased with the systematic sampling during the Russian-German collaboration in the NW Pacific Ocean (refer to Chapter 1). Over 700 sponge specimens were retrieved from these four expeditions in this region, and results from the identified fauna from the Sea of Okhotsk and the Kuril-Kamchatka abyssal plain indicate that many of the sponges are likely to be endemic to the NW Pacific Ocean (Downey and Janussen 2015; Downey et al. 2018). Over two-thirds of sponges found in the Sea of Okhotsk and Bussol Strait are likely endemic, and a third of sponges found in the Kuril-Kamchatka abyssal plain, are likely to be endemic to the NW Pacific Ocean (Downey et al. 2018; Downey and Janussen 2015). Despite high levels of endemism in the semi-enclosed Sea of Okhotsk, likely due to the limited number of deep-sea straits, some species were found to have much broader distributions throughout the North and NW Pacific Ocean. These broader longitudinal, latitudinal and depth distributions were more common in the Kuril-Kamchatka abyssal plain, which found that these species were generally found throughout the North Pacific Ocean (Downey and Janussen 2015). It was also found that hexactinellids had much greater depth distributions (eurybathy), than demosponges, with only 15% of demosponges were found to have broad depth distributions (Downey and Janussen 2015; Downey et al. 2018).

In the deep sea, rarity is considered a characteristic of taxa, with ca. 74% of macrofaunal species were found in less than 10% of samples in the West Atlantic, and 25% of species were singletons (Carney 1997). Within the NW Pacific Ocean, more than half of sponge species found on theKuril-Kamchatka abyssal plain, and nearly two-thirds of species from the Sea of Okhotsk, are rare through geographical limitation, only being found at one station (Downey and Janussen 2015; Downey et al. 2018). Several stations, particularly in the Sea of Okhotsk, were found to have high levels of localised diversity, despite most stations having found very few or no sponges in the adjacent abyssal plain.

The majority of deep-sea sponge records are from the lower bathyal and abyssal depths, with less than 1% (19 records) of deep-sea records from the hadal (>6,000 m) (OBIS 2019). Hadal regions are common throughout the North Pacific Ocean, as well as around Indonesia, Puerto Rico in the Atlantic Ocean, and the South Sandwich Islands in the Southern Ocean (GOODS 2009). The most recent expedition to the Kuril-Kamchatka Trench hadal region has yielded 87 sponge specimens, with several demosponges and hexactinellids achieving depth records greater than all previously collected deep-sea sponges (Koltun 1959; Vacelet and Boury-Esnault 1995; van Soest et al. 2012).

2. Objectives

The main objectives of this study were to analyse our current knowledge of deep-sea sponge species, genera, and family diversity, endemism and richness, sponge abundance, and latitudinal and depth gradients in the NW Pacific Ocean, as well as to investigate deep-sea faunal biogeographical patterns within this region and with adjacent deep-sea regions utilising new and previously identified sponge collections.

3. Material and Methods

3.1. Coverage Area and Occurrence Data

Sponge specimens were collected on four separate expeditions in the NW Pacific (Sea of Japan, Sea of Okhotsk, Kuril-Kamchatka abyssal plain and the Kuril-Kamchatka Trench), using Agassiz trawls, epi-benthic sledges and box corers, a joint collaboration between the Russians and Germans, between 2010 and 2016 (refer to Chapter 1 in this issue). All previous deep-sea data from this study region was collated from OBIS (2019) and additional publications (Hôzawa 1918; Okada 1932; Koltun 1955a, 1958, 1959, 1962, 1966, 1967, 1972; Samaai and Krasokhin 2002; Ereskovsky and Willenz 2007). Maps have been produced, documenting most of the deep-sea sponge species found in the NW Pacific Ocean, including both widely distributed, and species that have only been found once. Data for these species distributions was compiled from these new expeditions, as well as previously published data. In this study, the NW Pacific Ocean was defined as 120–180°E and 40–60°N. All sponge taxonomy was checked using World Porifera Database (WPD: Van Soest et al. 2012); however, several hexactinellid species described by Koltun (1967), have not yet been accepted by WPD, but were considered as a distinct species morphotypes despite current uncertainty. This sector of the NW Pacific Ocean contains several distinct deep-sea areas: abyssal plains, abyssal basins of the semi-enclosed Sea of Okhotsk, Sea of Japan and the Bering Sea, the hadal Kuril-Kamchatka Trench, and the Emperor Seamounts.

3.2. Depth Gradient

All deep-sea sponge data was collated for the NW Pacific Ocean; however, only sponge records from depths greater than 2,000 m were used to analyse variations in species diversity at depth. Depths were categorised into both stenobathic (restricted) zones: lower bathyal (2,000–3,000 m), abyssal (3,000–6,000 m), and hadal (6,000 m +). Eurybathic (species occurring across multiple depths) zones were also included to determine which species had broad depth distributions in the deep sea. Shallower depth data from these deep-sea species was added into a table to fully understand biogeographic patterns, and potentially enable our understanding of submergence and emergence processes.

3.3. Latitudinal Gradient

In this study region, the temperate and sub-polar NW Pacific Ocean has a latitudinal gradient of 40–60°N. In some deep-sea species, there is a known reduction in diversity with increasing latitudinal gradient (Gray 2001), and therefore latitudinal data was utilised to determine if there was a reduction in species with an increased latitude at these depths. Five-degree latitude intervals were compiled, and longitudinal and depth ranges of stations were recorded for overview. Each unique latitude and longitude was taken to be a station, so that sampling intensity could also be explored in these latitudinal bands.

4. Results

4.1. Richness Patterns

The minimum number of known sponge specimens from this deep-sea region is 938, which is likely an underestimation of sponge records from below 2,000 m, as older records did not always provide exact numbers of specimens (Table 1). Overall, results indicate that hexactinellid sponges are far more abundant throughout the NW Pacific deep sea, with close to 60% of known specimens found in this class. Nearly 40% of specimens found are from the demosponge class, with the remaining few percent not yet identified from the phylum. These are similar to findings from the Sea of Okhotsk, which found 74% hexactinellid species and 26% demosponges (Downey et al. 2015). However, they are in opposition to sponges collected in the Kuril-Kamchatka abyssal plain, which found that 57% of specimens were demosponges, and 43% were hexactinellids (Downey et al. 2018). So far, only one calcareous sponge specimen has been found (Order: Calcarea Bowerbank, 1862) in the deep-sea sector of the NW Pacific, which is not unexpected, as only one calcareous species (Sycon escanabense Duplessis & Reiswig, 2000) has so far been found in the adjacent abyssal NE Pacific region (Duplessis and Reiswig 2000) and only 145 specimens of calcareous sponges are known from below 2,000 m (OBIS 2019).

Numbers of families, genera, species and specimens of demosponges and hexactinellids found in the NW Pacific deep sea.

Deep-sea families Deep-sea genera Deep-sea species* No. of specimens
Porifera - - - 48
Demospongiae 10 17 46** 347
Hexactinellida 6 10 23*** 542
Calcarea 1 1 1 1
Total 17 28 70 938

This region has so far yielded at least 70 sponge species morphotypes, and 2 subspecies, with many new species not yet fully described from recent expeditions, including specimens from the Sea of Japan, and many from the most recent Kuril-Kamchatka Trench expedition (Table 2). These 70 species morphotypes are found within 28 genera, and 17 families. These are conservative lower estimates of the species, genera and family richness from the deep NW Pacific Ocean, with the numbers likely to increase substantially with each new expedition into this region.Two-thirds of these species morphotypes are demosponges, with the remaining third found to be hexactinellids, and 1% calcareous sponges. In general, demosponges are twice as diverse in genera and families represented in the deep NW Pacific Ocean compared with hexactinellids, with demosponge species found within 17 genera, and 10 families, whereas, and hexactinellids are found within 10 genera and 6 families.

List of all species morphotypes and subspecies of deep-sea sponges found in the NW Pacific. Depth, longitude and latitude include all information about a species distribution.

Class Family Species Depth range Latitudinal range Longitudinal range Distribution
Calcarea Bowerbank, 1862 - - 5,005–5,045 m 44 N 156 E Kuril-Kamchatka abyssal plain
Demospongiae Sollas, 1885 Acarnidae Dendy, 1922 Cornulum clathriata (Koltun, 1955) 89–2,440 m 51–53 N 170 E – 170 W Aleutian Islands
Demospongiae Sollas, 1885 Acarnidae Dendy, 1922 Megaciella ochotensis (Koltun, 1959) 83–3,363 m 46–59 N 147–156 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Abyssocladia claviformis Koltun, 1970 5,005–6,069 m 33–44 N 149–156 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Abyssocladia koltuni (Ereskovsky & Willenz, 2007) 500–2,358 m 46–50 N 145–151 E Sea of Okhotsk and Bussol Strait
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 1 3,307 m 46 N 146 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 2 3,307 m 46 N 146 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 3 3,299–3,366 m 46–48 N 147–151 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 4 3,347–3,350 m 48 N 150 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 5 3,361–4,469 m 46 N 152 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 6 3,350 m 48 N 150 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 7 3,347–3,351 m 48 N 150 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 8 3,301–3,351 m 48 N 150–151 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 9 3,248–3,377 m 46 N 152 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) sp. nov 10 3,347–3,350m 48 N 150 E Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) biserialis (Ridley & Dendy, 1886) 941–6,282 m 42 S – 48 N 150 E – 118 W Pacific Ocean and Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) ramosa Koltun, 1958 188–3,347 m 45–51 N 147 E – 173 W N/NW Pacific Ocean and Bussol Strait
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Asbestopluma (Asbestopluma) wolffi Lévi, 1964 6,675–8,120 m 43–45 N 149–153 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) sp. nov 1 5,125–5,127 m 42 N 152 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) clavata Ridley & Dendy, 1886 25–5,711 m 78 S – 47 N 180 W – 178 E Pacific Ocean, Southern Ocean and Indian Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) concrescens (Schmidt, 1880) 200–8,660 m 24 S – 50 N 177 W – 167 E Pacific Ocean, Sea of Okhotsk, Atlantic Ocean, Norwegian seas and Indian Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) crinita Ridley & Dendy, 1886 3,658–5,998 m 3–46 N 134–156 E North and West Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) dichotoma Lévi, 1964 3,310–6,282 m 1–48 N 77–169 E North Pacific Ocean and Indian Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) grandis (Verrill, 1879) 30–3,948 m 70 S – 38 N 8 E – 1 W N/NW/S Atlantic Ocean, Arctic Ocean, Southern Ocean, Sea of Okhotsk, Kuril Islands and Aleutian Islands
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) koltuni Vacelet, 2006 4,976–5,249 m 43–55 N 153–166 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Chondrocladia (Chondrocladia) aff. virgata 5,191 m 43 N 151 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza sp. nov 1 5,250–5,408 m 41 N 155 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza sp. nov 2 4,976–4,980 m 47 N 150–151 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza aff. abyssicola 7,077 m 45 N 152 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza bathycrinoides Koltun, 1955 150–3,800 m 44–49 N 147–157 E NW Pacific Ocean and Sea of Okhotsk
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza longipinna Ridley & Dendy, 1886 3,000–6,282 m 14–48 N 143 E – 175 W North Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza mirabilis (Ridley & Dendy, 1886) 4,115–5,127 m 39 S – 42 N 151 E – 118 W Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza rectangularis Ridley & Dendy, 1887 3,325–6,065 m 7 S – 49 N 146 E – 152 W Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Cladorhiza septemdentalis Koltun, 1970 4,891–7,295 m 25–46 N 143–153 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Koltunicladia flabelliformis (Koltun, 1970) 5,390 m 44 N 170 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Lycopodina infundibulum f. orientalis (Koltun, 1970) 2,665–5,450 m 38–44 N 146–149 E NW Pacific Ocean
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Lycopodina occidentalis (Lambe, 1893) 820–8,840 m 38–53 N 151 E – 130 W North Pacific
Demospongiae Sollas, 1885 Cladorhizidae Dendy, 1922 Lycopodina globularis (Lévi, 1964) 3,570–5,400 m 9–46 N 150 E – 89 W North Pacific Ocean
Demospongiae Sollas, 1885 Coelosphaeridae Dendy, 1922 Forcepia (Leptolabis) uschakowi (Burton, 1935) 34–2,358 m 43–51 N 146–157 E NW Pacific Ocean, Sea of Japan and Bussol Strait
Demospongiae Sollas, 1885 Esperiopsidae Hentschel, 1923 Esperiopsis plumosa Tanita, 1965 150–6,860 m 34–48 N 127–153 E NW Pacific and Sea of Japan
Demospongiae Sollas, 1885 Myxillidae Dendy, 1922 Melonanchora tetradentifera Koltun, 1970 4,45–3,352 m 46 N 147–152 E Sea of Okhotsk, Bussol Strait and NW Pacific
Demospongiae Sollas, 1885 Phellodermidae van Soest & Hajdu, 2002 Echinostylinos mycaloides Koltun, 1970 2,265–3,351 m 44–48 N 149–150 E NW Pacific and Sea of Okhotsk
Demospongiae Sollas, 1885 Polymastiidae Gray, 1867 Polymastia pacifica Koltun, 1966 3,940–6,065 m 34–56 N 156 E – 132 W North Pacific Ocean
Demospongiae Sollas, 1885 Polymastiidae Gray, 1867 Sphaerotylus sp. 1 5,418–5,419 m 43 N 157 E
Demospongiae Sollas, 1885 Suberitidae Schmidt, 1870 Suberites sp. 1 2,350–3,366 m 46–48 N 149–151 E
Demospongiae Sollas, 1885 Tedaniidae Ridley & Dendy, 1886 Tedania (Tedania) sp. 1 3,351–3,352 m 46 N 147 E
Demospongiae Sollas, 1885 Vulcanellidae Cárdenas, Xavier, Reveillaud, Schander & Rapp, 2011 Poecillastra japonica (Thiele, 1898) 47–2,440 m 36–54 N 151 E – 129 W North Pacific Ocean
Hexactinellida Schmidt, 1870 Aphrocallistidae Gray, 1867 Aphrocallistidae sp. 1 3,300–3,301 m 46 N 151 E Sea of Okhotsk
Hexactinellida Schmidt, 1870 Aphrocallistidae Gray, 1867 Aphrocallistidae sp. 2 3,300–3,301 m 46 N 151 E Sea of Okhotsk
Hexactinellida Schmidt, 1870 Euplectellidae Gray, 1867 Holascus undulatus Schulze, 1899 2,868–6,328 m 45–55 N 155 E – 136 W North Pacific
Hexactinellida Schmidt, 1870 Euplectellidae Gray, 1867 Ijimaiella beringiana Tabachnick, 2002 6,272–6,282 m 55 N 167 E Aleutian Islands
Hexactinellida Schmidt, 1870 Euretidae Zittel, 1877 Eurete irregular Okada, 1932 1,676–4,798 m 45–48 N 145–174 E Sea of Okhotsk, Bussol Strait and NW Pacific
Hexactinellida Schmidt, 1870 Euretidae Zittel, 1877 Pinulasma fistulosum Reiswig & Stone, 2013 2,084 m 51 N 179 E Aleutian islands
Hexactinellida Schmidt, 1870 Farreidae Gray, 1872 Farrea sp. 1 4,859–5,419 m 40–46 N 150–157 E NW Pacific Ocean
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Corynonema) populiferum harpagonis Koltun 1967 3,400 m 45 N 156 E Sea of Okhotsk
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Cyliconema) apertum Schulze, 1886 320–6,235 m 44S–51 N 92E–175 W Pacific and Indian Oceans
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Cyliconema) apertum simplex Koltun, 1967 1,699–3,964 m 44–59 N 145–174 E NW Pacific, Bering Sea, Bussol Strait and Sea of Okhotsk
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Cyliconema) hozawai vicarium Koltun, 1967 3,920-3,964 m 55–59 N 169–174 E Bering Sea
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Cyliconema) tenerum vitiazi Koltun, 1967 3,812 m 53 N 172 E Bering Sea
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Onconema) obtusum Lendenfeld, 1915 4,346-5,258 m 0–43 N 151 E – 117 W North Pacific
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Oonema) robustum Schulze, 1886 3,347-4,140 m 35–48 N 150–157 E Sea of Okhotsk and NW Pacific
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Paradisconema) sp. nov 1 2,350-3,303 m 46 N 151 E Sea of Okhotsk
Hexactinellida Schmidt, 1870 Hyalonematidae Gray, 1857 Hyalonema (Prionema) aff. agujanum Lendenfeld, 1915 5,229 m 43 N 151 E NW Pacific
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Acanthascus profundum Koltun, 1967 342-2,440 m 36–55 N 164 E – 121 W North Pacific Ocean
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Bathydorus echinus Koltun, 1967 2,440-3,353 m 46–61 N 147 E, 167–164 W North Pacific Ocean, Bering Sea and Sea of Okhotsk
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Bathydorus fimbriatus Schulze, 1886 2,167-6,135 m 35–46 N 149 E – 177 W North Pacific Ocean
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Bathydorus laevis pseudospinosus Tabachnick & Menshenina, 2013 2,167-3,940 m 1–41 N 153 E – 80 W North Pacific Ocean
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Caulophacus (Caulodiscus) lotifolium Ijima, 1903 3,299–6,710 m 38–48 N 146–178 E NW Pacific Ocean and Sea of Okhotsk
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Caulophacus (Caulophacus) elegans Schulze, 1886 3,680–4,202 m 35–58 N 157–177 E NW Pacific Ocean
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Caulophacus (Caulophacus) schulzei Wilson, 1904 2,350–3,366 m 46–47 N 147–151 E Sea of Okhotsk
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Caulophacus (Caulophacus) schulzei hyperboreus Koltun, 1967 3,932–3,400 m 46–57 N 150–175 E Sea of Okhotsk and Bering Sea
Hexactinellida Schmidt, 1870 Rossellidae Schulze, 1885 Sympagella cantharellus (Lendenfeld, 1915) 4,063–5,045 m 5 S– 45 N 156 E – 82 W Pacific Ocean

Over a third (26 spp.) of deep-sea species morphotypes found in the NW Pacific Ocean are either new to the region or new to science (Downey and Janussen 2015; Downey et al. 2018). Fifteen new species are currently being described, and eleven species are new to this region. Of the fifteen new species, thirteen are demosponges from the Cladorhizidae family. The eleven new species to this region include nine demosponges in nine genera, and two hexactinellids in two genera. Six of the demosponge genera and one of the hexactinellid genera, have never been recorded from this deep-sea sector of the ocean. Very little is known about the calcareous specimen; however, it is likely to be a new species, and potentially a new genus.

There is a high likelihood that more new cladorhizid species will be described from the Kuril-Kamchatka Trench, including an undescribed Asbestopluma sp. from 9,013 m, and 6 cladorhizid specimens from between 8,111–8,358 m. Until now, the deepest known living sponge, a cladorhizid (Lycopodina occidentalis (Lambe, 1893)), was collected from this region (8,840 m), (Koltun 1959; Vacelet and Boury-Esnault 1995; van Soest et al. 2012), and this new Asbestopluma (Asbestopluma) Topsent, 1901 record, is nearly 200 m deeper. However, one unidentified hexactinellid sponge from the same region and expedition was collected from a greater depth of 9,292–9,301 m, up to 461 m deeper than the previously deepest known record for all sponges in the global oceans. However, more importantly, it is more than 2,500 m deeper than the previously found glass sponges globally (Lévi 1964; OBIS 2019) and from this region (Koltun 1966, 1967).

Currently, more than half of species found in this region (35 spp.) are from the Cladorhizidae family (including species morphotyped but not yet to be fully described), which indicates the diversity anddominance of this demosponge family within this region (Table 2). However, this does not include an additional 29 specimens from the recent Kuril-Kamchatka Trench expedition, which have not been identified to species level, and are likely to increase species numbers from this family further. Six genera are represented from this family, with Asbestopluma (A.) dominating in terms of species (13 spp.), followed by Chondrocladia Thomson, 1873 and Cladorhiza Sars, 1872 (both 8 spp.). All other demosponge families (9), are generally only represented by one or two genera in the NW Pacific Ocean (total of 11 species).

Previously, Koltun (1972) had documented 15 species of carnivorous sponges in the deep NW Pacific Ocean, which has now more than doubled in number after these recent NW Pacific Ocean campaigns (Table 2). No carnivorous sponges were found in the Sea of Japan; however, 11 spp. were found on the Kuril-Kamchatka abyssal plain, 15 spp. in the Sea of Okhotsk, two spp. at the northern end of the Emperor Seamounts, and seven spp. currently from the Kuril-Kamchatka Trench. Hexactinellids are far more abundant than demosponges in the deep NW Pacific Ocean, despite not being as species rich as demosponges. However, two hexactinellid families were found to be particularly diverse in either genera and/or species in the deep NW Pacific Ocean. Both the Hyalonematidae Gray, 1857 and Rossellidae Schulze, 1885 families are represented by eight spp., which accounts for close to a quarter of species found in this region. The Hyalonematidae family are only represented by the species-rich genus Hyalonema Gray, 1832, whereas the Rossellidae family are represented by five genera, with Bathydorus Schulze, 1886 and Caulophacus Schulze, 1886 dominating in numbers of species.

Recent studies, which explored the diversity of sponge species, using a Shannon-Wiener index, in the Sea of Okhotsk and the Kuril-Kamchatka abyssal plain, found that the Sea of Okhotsk was generally far more diverse, particularly the NE sector of the basin and the Bussol Strait, than the adjacent abyssal plain (Downey et al. 2018). Stations in the northern and central sector of the Kuril-Kamchatka abyssal plain tended to be slightly richer than those in the southern sector (Downey and Janussen 2015). However, sites sampled in the Sea of Okhotsk tended to be shallower than in the adjacent Kuril-Kamchatka abyssal plain. All sites sampled in these adjacent regions are found to be fairly even too, with evenness found to be slightly greater in the Kuril-Kamchatka abyssal plain (Downey and Janussen 2015). Diversity and evenness measures have not been analysed for the Sea of Japan and the Kuril-Kamchatka Trench; however, it is likely that the sparsity of samples for the Sea of Japan represents low sponge diversity and evenness; however, the hadal sector of the Kuril-Kamchatka Trench could yield similar levels of diversity and evenness to the adjacent abyssal plain.

Sampling across the deep NW Pacific Ocean has been sporadic, with depths and longitudinal ranges varying considerably in this region, and therefore analysis of latitudinal changes in diversity is complex. However, results indicate that 45-50°N latitude band appears to be the richest in species, with nearly twice as many found than the next richest latitudinal band (40–45°N) (Table 3). Depth ranges were similar for both of these species-rich latitudinal bands; however, there were at least 50% more unique sampling stations in the richest latitudinal band, and therefore, if the second-most rich band had had moresampling stations, it potentially could be found to be nearly as rich in species. However, the second-richest latitudinal band has an additional 15° longitude of sampling (over 60% more longitude than the richest latitudinal band), which would require additional sampling to be comparable in terms of sampling intensity. In the two most northerly latitudinal bands, very few stations with samples have been recorded, and this is further impacted by the rapid reduction in deep sea and longitudinal range availability at these high latitudes. Despite limited sampling, many species have been found at these higher latitudes, and hypothetically, these latitudinal bands could be as rich as or richer in species than latitudes further south, if sampled comparably. Both hexactinellid and demosponge species are most speciose in the richest latitudinal band (45–50°N); however, hexactinellids also have many species found in the furthest southerly and northerly latitudinal bands. Demosponges are at their most diverse at the two most southerly latitudinal sectors of the NW Pacific Ocean. Results indicate that demosponge species dominate the two southerly latitudinal bands (both have over 70% of all species found), whereas hexactinellids dominate diversity in the two northerly latitudinal bands in the NW Pacific Ocean (90% species representation at 55–60°N).

Latitudinal bands detailing numbers of species found in each five degree interval in the NW Pacific deep-sea. Information on the number of unique stations sampled (unique latitude and longitude), longitudinal range and sampled depth range is given.

Latitudinal band Total Porifera Demospongiae Hexactinellida Calcarea Unique sampling stations Longitudinal range (°) Depth range (m)
40–45°N 31 22 8 1 60 38.67 7,136
45–50°N 50 36 14 0 91 23.89 6,806
50–55°N 8 3 5 0 7 22.34 4,212
55–60°N 10 1 9 0 13 18.97 1,854

In the NW Pacific Ocean, sponge species were distributed from 2,084–9,301 m, utilising both older records from previous expeditions, and newer records from the four recent Russian-German expedition (Downey and Janussen 2015; Downey et al. 2018; refer to Chapter 1). Nearly 80% (55 spp.) of sponge species in the NW Pacific are found to be stenobathic, distributed in only one depth zone, whereas over 20% (15 spp.) are eurybathic, found in two or more depth zones (Table 4). Nearly 60% of all species are restricted to the abyss, whereas over 15% are restricted to the lower bathyal, and 4% restricted to hadal depths. Abyssal depths are found to be the richest in terms of species, with close to 80% (56 spp., 34 demosponges, 21 hexactinellids, and 1 calcareous sponge) of all deep-sea species distributed in this broad depth zone. Twenty-species are distributed in the lower bathyal (13 demosponges and seven hexactinellids), and thirteen are known from hadal depths (nine demosponges and four hexactinellids). At each greater depth zone, there is a slight increase in the proportion of demosponge species, although only from 61 to 69%. Eighty-five percent (39 spp.) of demosponge species are restricted to a particular depth zone, with the remainder found to be eurybathic. Whereas, 65% (15 spp.)of hexactinellids are restricted to one depth zone, with a third of species found distributed in multiple depth zones.

Depth ranges of all species found in the NW Pacific, with defined depth ranges for each depth zone.

Total Demospongiae Hexactinellida Calcarea
Stenobathic zones
Lower bathyal (2,000–3,000 m) 11 9 2 0
Abyssal (3,000–6,000 m) 41 27 13 1
Hadal (6,000 m +) 3 3 0 0
Eurybathic zones
Lower bathyal-Abyssal (2000–6,000 m) 5 1 4 0
Lower bathyal-Abyssal-Hadal (2,000–6,000 m +) 4 3 1 0
Abyssal and Hadal (3,000 m +) 6 3 3 0

4. 2. Biogeographic Patterns

Demosponges are the most diverse in terms of represented families, genera and species in the NW Pacific Ocean, and carnivorous sponges (Cladorhizidae family) are dominant parts of the deep-sea assemblage, represented in six genera (Table 2). The genus Asbestopluma (A.) is particularly species-rich in this region, comprising of 13 species, with many of them new to science. The majority of these species (13 spp.) are likely to be endemic to this region, with many only found at one or two stations, and most species found in the Sea of Okhotsk and the Kuril-Kamchatka ridge and trench (Downey and Janussen 2015; Downey et al. 2018). Unusually, Asbestopluma (A.) biserialis (Ridley and Dendy 1886) does have a much broader range in the NW Pacific compared to most other species of this genus (Map 1). One other species, Asbestopluma (A.) ramosa Koltun, 1958, is also found to be distributed throughout the North Pacific Ocean and have much broader known depth ranges as well (Table 2).

Map 1.

Distribution of Asbestopluma species from the NW Pacific (Cladorhizidae family).

Chondrocladia (Chondrocladia) is another species rich genus found within the NW Pacific Ocean, represented by at least eight species, with many other specimens not yet fully identified (Table 2). However, so far, only three spp. are likely to be endemic, including one new to science species, with the remainder of species found to be distributed broadly in the Pacific Ocean and for one species, globally (Map 2; Table 2). Half of the species within this genus have broad ranges in the NW Pacific, which include C. (C.) clavata Ridley & Dendy, 1886, C. (C.) dichotoma Lévi, 1964, C. (C.) concrescens (Schmidt, 1880), and C. (C.) koltuni Vacelet, 2006. Chondrocladia species are not found to be distributed in the Kuril Basin of the Sea of Okhotsk.

Map 2.

Distribution of Chondrocladia species from the NW Pacific (Cladorhizidae family).

Cladorhiza is another species-rich genus within the Cladorhizidae family, comprising of eight spp. in the deep NW Pacific Ocean (Table 2). Half of these species are likely to be endemic in this region, with two of these species new to science. Three species are found more broadly in thePacific Ocean, C. mirabilis (Ridley & Dendy, 1886) and C. rectangularis Ridley & Dendy, 1887, with C. longipinna Ridley & Dendy, 1886 distributed only in the North Pacific (Map 3). Endemic C. bathycrinoides Koltun, 1955 is found to have a broad distribution in the Sea of Okhotsk and the Kuril-Kamchatka ridge, whereas broadly distributed C. longipinna is only found in the NW Pacific abyssal plains. Similar to Chondrocladia, most Cladorhiza species are not found to be distributed in the Kuril Basin of the Sea of Okhotsk.

Map 3.

Distribution of Cladorhiza species from the NW Pacific (Cladorhizidae family).

All remaining genera within the Cladorhizidae family, Abyssocladia Lévi, 1964, Lycopodina Lundbeck, 1905 and Koltunicladia, are found to be species-poor (Table 2). Apart from the genus Lycopodina, which is broadly distributed within the NW Pacific and the North Pacific generally, all other species are found to be endemic and restricted in distribution (Map 4). K. flabelliformis (Koltun, 1970) has only been found on the Emperor Seamounts, and the two species of Abyssocladia are restricted to either the NW Pacific abyssalplain or the Bussol Strait. Many new specimens from the Cladorhizidae family have been found in the Kuril-Kamchatka Trench, including an Asbestopluma (A.) recorded from the depth of 9,013 m. Very few cladorhizid sponges have so far been found close to the Aleutian Trench and Bering Sea; however, with increased sampling, it is likely that this species-rich family is found throughout the NW Pacific Ocean.

Map 4.

Distribution of remaining species from the Cladorhizidae family in the NW Pacific.

Seven demosponge species were found from six other families (Acarnidae, Dendy, 1922, Coelosphaeridae Dendy, 1922, Esperiopsidae Hentschel, 1923, Myxillidae Dendy, 1922, Phellodermidae van Soest & Hajdu, 2002, and Tedaniidae Ridley & Dendy, 1886), in the Poecilosclerida Topsent, 1928 Order in the NW Pacific Ocean (Table 2). All known species are endemic to the NW Pacific, apart from Cornulum clathriata (Koltun, 1955), which is found distributed in the North Pacific. More than half of these species have distributions in the semi-enclosed Sea of Okhotsk, whereas the remainder are distributed on the southerly edge of the Kuril Islands or on the abyssal plain (Map 5).

Map 5.

Distribution of remaining demosponge species from the Poecilosclerida order.

All remaining demosponge species (4 spp.) are found within either the Tetractinellida Marshall, 1876, Polymastiida Morrow & Cárdenas, 2015 or Suberitida Chombard & Boury-Esnault, 1999 orders (Table 2). None of these species are known to be endemic to the region, with Poecillastra japonica (Thiele, 1898), Polymastia pacifica Koltun, 1966, and Cornulum clathriata (Koltun, 1955) known to be broadly distributed in the North Pacific Ocean (Map 6). However, the remaining species have not been identified to the species level, and so these species could be endemic, with many restricted in distribution within the Sea of Okhotsk and the Bussol Strait.

Map 6.

Distribution of demosponges from the Polymastiida, Suberitida, and Tetractinellida orders.

Overall, NW Pacific hexactinellids are not rich in genera or species, compared to demosponges; however, the genus Hyalonema, within the order Amphidiscosida Schrammen, 1924, has recorded eight species and one subspecies within this deep-sea region (Table 2). At least six of these species (including the subspecies)are likely be endemic to this region and have generally restricted distributions, like the, as yet unrecognised, subspecies, H. (C.) hozawai vicarium Koltun, 1967, which is only distributed in the Bering Sea (Map 7). H. (C.) apertum simplex Koltun, 1967 appears to be distributed broadly in the NW Pacific, being found at both the semi-enclosed Sea of Okhotsk and the Bering Sea; however, interestingly H. (C.) apertum Schulze, 1886 is distributed throughout the Pacific and Indian oceans, but is not known within the semi-enclosed seas of this region. H. (Onconema) obtusum Lendenfeld, 1915 is known to be distributed broadly in the North Pacific Ocean.

Map 7.

Distribution of Hyalonema species from the NW Pacific (Amphidiscosida order).

Within the Hexactinellida Schmidt, 1870 order Lyssacinosida Zittel, 1877, two families, the Rossellidae Schulze, 1885 and the Euplectellidae Gray, 1867 are represented within the NW Pacific (Table 2). In these two families, ten speciesand one subspecies in six genera have been found. The most species rich of these genera, is Caulophacus Schulze, 1886, with three species and one subspecies represented. All of these Caulophacus species and subspecies are likely endemic to this region. All other species, apart from Ijimaiella beringiana Tabachnick, 2002, are found to be broadly distributed throughout the North Pacific, with Sympagella cantharellus (Lendenfeld, 1915) distributed throughout the Pacific Ocean (Map 8). Most of these species are found to have broad distributions throughout the NW Pacific, including some of the endemic species. Interestingly, C. (Caulophacus) schulzei Wilson, 1904 appears to be distributed only in the Sea of Okhotsk and Bussol Strait, whereas, C. (C.) schulzei hyperboreus Koltun, 1967 is distributed both within the semi-enclosed Seaof Okhotsk and Bering Sea. I. beringiana is only found in the Bering Sea and Holascus undulatus Schulze, 1899 is the only hexactinellid known from the Emperor Seamounts.

Map 8.

Distribution of hexactinellid species from the NW Pacific (Lyssacionosida order).

The final Hexactinellida order of Sceptrulophora Mehl, 1992, is comprised of three families, Euretidae Zittel, 1877, Aphrocallistidae Gray, 1867, and Farreidae Gray, 1872 in the NW Pacific (Table 2). These families comprise of at least four genera, and five species. Due to lower levels of taxonomic identification in this order, only two of the species are so far known to be endemic in the NW Pacific Ocean, and it is unclear if the remainder are endemic or of broadly distributed fauna. Endemic Pinulasma fistulosum Reiswig & Stone, 2013 is only found within the Bering Sea, whereas Eurete iregulare Okada, 1932 is found to be broadly distributed in both the Sea of Okhotsk, the Bussol Strait and the Bering Sea (Map 9). All representatives of the Farrea Bowerbank, 1862 genus are found to be broadly distributed only on the abyssal plain, and specimens of the Aphrocallistidae family wereonly found in the Kuril Basin of the Okhotsk Sea, with no known representatives from other parts of the deep NW Pacific.

Map 9.

Distribution of hexactinellid species from the NW Pacific (Sceptrulophora order).

Close to 60% of all deep-sea species found in this region (40 spp.) are likely to be endemic to the NW Pacific Ocean (Table 2). Seventy-percent of these endemic species are demosponges (28 spp.), mainly found within the Cladorhizidae family, and 30% are hexactinellids (12 spp.), with most of these found within the Hyalonematidae family. Within the NW Pacific, three sponge genera are found to be monotypic (only having one species known to that genus), two are hexactinellid genera: Pinulasma Reiswig & Stone, 2013, Ijimaiella Tabachnick, 2002, and one demosponge genus Koltunicladia. This is greater than 10% of all genera known from depths greater than 2,000 m in the NW Pacific. With high levels of both genera and species endemism, this region is found to be faunistically distinct for deep-sea sponges. At least half of endemicsponge fauna appear to be restricted to the semi-enclosed Bering Sea and Sea of Okhotsk, with the remainder distributed in either the NW Pacific abyssal plain, the Bussol Strait, the Kuril-Kamchatka Trench, or the Emperor Seamounts.

Strong faunal connections are still found with sponge fauna in the North Pacific Ocean, with close to 20% (13 spp.) of species known to have this broad distribution, split generally evenly between both demosponges and hexactinellids, but dominated by the Rossellidae and Cladorhizidae families (Table 2). Weaker connections are seen within the entire Pacific Ocean, with less than 10% of NW Pacific species (five spp.) having this distribution, and these are dominated by four species in the Cladorhizidae family, and hexactinellid S. cantharellus. Very weak connections are seen globally; with only two Chondrocladia species found globally. Nine species morphotypes haveunknown distributions due to the low level of identification, and this information could in the future aid our understanding of biogeographic patterns in the NW Pacific deep-sea fauna.

Previous studies have indicated that eurybathy is a relatively common distribution characteristic in the deep NW Pacific (Downey and Janussen 2015; Downey et al. 2018). Eurybathy appeared to be far more common for species found in the broad NW abyssal plains compared to the semi-enclosed Sea of Okhotsk (Downey et al. 2018). These differences appear to be due to the strongly eurybathic demosponges in the abyssal plain, compared to the more stenobathic species in the Sea of Okhotsk. Hexactinellids found in both the Sea of Okhotsk and the NW Pacific abyssal plains appear to have similar numbers of species with eurybathic ranges. However, newer analysis indicates that less than a quarter of species (15 spp.) throughout the NW Pacific have eurybathic characteristics, which arerepresented roughly equally by demosponges and hexactinellids (Table 4). The most common restricted distribution was the abyss, with more than half of species (41 spp.) found only in this depth zone, and more than two-thirds of these represented by demosponges. Demosponges are more likely to be found in a restricted depth zone (39 spp., c. 85%), compared to hexactinellids (15 spp., c. 65%) in the NW Pacific.

5. Discussion

The deep NW Pacific sponge fauna was first sampled over a century ago (Okada 1932); however, it was systematically investigated during the 1940s to the 1960s during several campaigns from the RV Vitiaz (Koltun 1955a, 1955b, 1958, 1959, 1962, 1966, 1967, 1972). Until the most recent Russian-German expeditions, only 33 species and one subspecies, were known from this region. This figure has now more than doubled to 70 species morphotypes, two subspecies, with a high-likelihood of increased species numbers from the Sea of Japan and the Kuril-Kamchatka Trench, which have yet to be fully identified (Table 2). The number of genera known to this entire region has increased by a third from these recent expeditions (10 additional genera). The KuramBio (Kuril–Kamchatka Biodiversity Studies) expedition to the Kuril-Kamchatka abyssal plain found an additional eight species and two new genera (Downey and Janussen 2015). During the SokhoBio (Sea of Okhotsk Biodiversity Studies) expedition, new specimens close to tripled the number of known species for this region and increased the number of genera by c. 50% (six new genera to region) (Downey et al. 2018). Only five sponge specimens were collected from stations deeper than 2,000 m during the 2010 SoJaBio (Sea of Japan Biodiversity Studies), and these are yet to be investigated, but are believed to represent one hexactinellid morphotype. No known sponges have been previously found below 2,000 m in the Sea of Japan (OBIS 2019), and so these would be the first sponges from this region. Thirteen species were previously known from the Kuril-Kamchatka Trench, and with an additional 87 sponge specimens from KuramBio II in 2016, it is likely that many new species will be described from this region. This expedition also collected specimens of both demosponges and hexactinellids at deeper depths than ever before, with one hexactinellid found at a depth of 9,301 m, and one demosponge at 9,013 m, several hundred metres deeper than the previous global records of depth for sponges (Koltun 1959). Early Russian expeditions also explored the Bering Sea, and so far 15 spp. are known from this and later expeditions (Koltun 1967; Reiswig and Stone 2013; OBIS 2019); and in the Emperor Seamounts, five spp. are known as well from earlier Russian expeditions (Koltun 1959, 1962, 1972). A new expedition in 2019 to the Emperor Seamounts (Nintoku Seamount) has recorded many species from depths of 2,100-2,400 m that are not known from previous expeditions in the NW Pacific Ocean, with several morphotypes noted from the families of Farreidae, Euplectellidae (particularly the genus Walteria Schulze, 1886), Rossellidae and some encrusting demosponges (pers. com L. Watling, August 2019) (Figure 2). These initial results indicate that this seamount ridge has families, genera, and species that are unusual compared to the rest of the NW Pacific deep-sea region.

Figure 2.

Examples of two hexactinellids sponges from the deep Emperor Seamounts (2019), Nintoku Seamount. Schmidt Ocean Institute. Les Watling.

Currently, over 20% (14 spp.) of species collected by these new Russian-German expeditions are new to science, which is similar to other deep–sea expeditions, such as the ANDEEP I–III (Janussen and Tendal 2007), and the abyssal Clarion Clipperton Zone in the mid–Pacific (Kersken et al., 2017), which both found 20–33% of species were new to science. However, with many specimens not fully identified, this is likely to increase substantially, indicating that the deep NW Pacific Ocean is likely richer in species but also limited in terms of sampling.

More than half of sponge species found on the Kuril-Kamchatka abyssal plain, and nearly two-thirds of species from the Sea of Okhotsk, appear to be geographically limited, only being found at one station (Downey and Janussen 2015; Downey et al. 2018). Close to 60% of species have apparent restricted geographical ranges and are represented by few specimens (Table 2). This is a known characteristic of deep-sea fauna, with many species either found in few samples, or found as singletons, indicating a low population density (Carney 1997; Ebbe et al. 2010; Hardy et al. 2015; Costello and Chaudhary 2017; Danovaro et al. 2017). Sponge growth and reproductive regimes in the deep sea are not well known (Hogg et al. 2010); however, it is likely that most sponges reproduce both sexually by releasing larvae and asexually by budding and fragmentation episodically. As reproduction is likely seasonal and recruitment episodic, these small, patchily rich areas of sponge singletons, could be due to rare reproductive events.

As well as a low population density, localised habitat features could be driving habitat-specific rarity (Ramirez-Llodra et al. 2010). The deep seafloor is formed of hundreds of millions of kilometres of continental slope and abyssal plain; however, small geological features within these are varied, such as seamounts, trenches, and ridges, which are common in the NW Pacific Ocean, and could be driving localised habitat specific rarity, potentially seen in a number of sponge species, such as K. flabelliformis, H. (C.) ternerum vitiazi Koltun, 1967, and S. cantharellus. Sponges tend to be more abundant and diverse on harder substrates, particularly seamounts, canyon heads and walls, ridges, and banks (Ramirez-Llodra et al. 2010; van Soest et al. 2012). The diversity of hard habitats in the NW Pacific could explain some of the localised higher diversity and/or abundance observed closer to the Kuril Islands ridge, trench and on the Emperor Seamounts (Table 2). Theseregions also tend to be areas of localised upwelling, generating greater food availability for sponges in these regions (Ramirez-Llodra et al. 2010), which is potentially another factor determining the greater numbers of sponges found at some stations in the Sea of Okhotsk and around the Kuril-Kamchatka ridge and trench. These unique abiotic attributes and biotic processes have likely helped to create varied levels of patchy sponge presence and diversity across the NW Pacific region.

Demosponges dominate the deep NW Pacific region, accounting for two-thirds (46 spp.) of all species currently found (Table 2). Many of these newly added species were found in both the Sea of Okhotsk, as well as several from the Kuril-Kamchatka abyssal plain (Downey and Janussen 2015; Downey et al. 2018). Cladorhizid sponges dominate the faunal composition in the NW Pacific region, accounting for more than three quarters (35 spp.) of known demosponge species, and accounting for more than a third (6) of all demosponge genera. Cladorhizid sponges are typical deep-sea sponge fauna, having likely evolved carnivory in the food–poor depths of the ocean (Vacelet and Boury–Esnault 1995). More than 10% (20 spp.) of globally described cladorhizids (173 spp., WORMS 2019) are found from this region, and with the addition of new species in the future (currently 13 new spp. and 2 spp. aff.), this will increase. Currently, two-thirds of cladorhizid species (23 spp.) are endemic to the deep NW Pacific Ocean. This region contains 100% of Koltunicladia species (1 sp.), 43% of all Asbestopluma (A.) species (13 spp.), 22% of all Chondrocladia (C.) species (3 spp.), 18% of all Cladorhiza species (8 spp.), 10% of all Lycopodina species (3 spp.), and 8% of all Abyssocladia species (2 spp.). It is likely that with an increase in deep-sea exploration of the North Pacific, and identification of new specimens from the Kuril-Kamchatka Trench, that many more new cladorhizid species and genera will be found in the NW Pacific, which could have been an important region for the evolution of this family, potentially due to the variety of deep-sea habitats and numerous currents and upwelling areas (Lundsten et al. 2014; Downey and Janussen 2015).

Glass sponges (Hexactinellida) are not as rich as demosponges at the species (23), genera (10) or family (6) level in the deep NW Pacific (Table 2). However, glass sponges outweigh demosponges in abundance, accounting for nearly 60% of all specimens found in this region (Table 1), and were found to be particularly rich in the Sea of Okhotsk, accounting for three-quarters of all specimens found (Downey et al. 2018). Many species of hexactinellid, including Hyalonema, Caulophacus, Eurete Semper, 1868 and Bathydorus are found across many stations (Maps 79), highlighting their broad distributions across the NW Pacific (Table 2). Nine species morphotypes of hexactinellids were found in the Kuril Basin of the Sea of Okhotsk, indicating the richness of hexactinellids in this semi-enclosed deep-sea region (Downey et al. 2018). Hexactinellid species richness also occurs in the Bering Sea (12 spp.), the Kuril-Kamchatka abyssal plain (8 spp. and 1 subsp.), and the Kuril-Kamchatka Trench (6 spp.) (Table 2). Hexactinellid diversity is found to be at its least in the Bussol Strait (4 spp.) and the Emperor Seamounts (1 spp.). However, with a new expedition to the Emperor Seamounts, it is likely that hexactinellid richness will increase (pers. com L. Watling, August 2019). Hexactinellid species account for a third (23 spp.) of known speciesin this deep-sea region (Table 2). The SokhoBio expedition has added six new hexactinellid species to the deep Sea of Okhotsk, Bussol Strait and NW Pacific fauna, which has nearly doubled the number of previously known hexactinellid species and added in one new genus (Bathydorus) to this region. One new to science species has been found: Hyalonema (Paradisconema) sp. Nov. 1. Hexactinellid abundance is exceptional in the Sea of Okhotsk, which is found to be at least fourteen orders of magnitude greater than the adjacent Kuril–Kamchatka region (Downey et al. 2018). Most hexactinellid families and genera found in the NW Pacific are found globally in all deep-sea environments (Tabachnick 1994), and the results from these studies indicate the presence of both new species, high levels of abundance, and the broad distributions of many hexactinellid species.

A hypothesised poleward decrease in diversity of deep benthic communities has been proposed, although it remains controversial (Gray 2001; Ramirez-Llodra et al. 2010). Latitudinal bands were compared within this study region, and superficially, diversity does appear to be greater at the southerly sector of the NW Pacific (Table 3). However, large differences in depth range, longitudinal range and sampling intensity, make it difficult to discern if there was a real decrease in diversity with increased latitude. Areas of semi-enclosed seas, such as the Sea of Okhotsk, regional diversity is found to be relatively high (Downey and Janussen 2015; Downey et al. 2018), compared to the adjacent Kuril-Kamchatka abyssal plain, and this high level of richness and diversity of species is likely influencing this poleward trend in reduced diversity above 50°N. What could be detected in this latitudinal analysis was a decrease in demosponge species and an associated increase of hexactinellids with increasing latitude. Hexactinellids are known to be more abundant and diverse in the high latitudes of the North and NE Pacific (Beulieu 2001; Leys et al. 2004; Reiswig 2014), which could be influencing this pattern. This is also found in the high latitudes of the Southern Ocean, with hexactinellids often found in greater numbers due to likely higher levels of dissolved silica, upwelling bottom waters, reduced runoff, and highly seasonable food availability (Downey et al. 2018).

Energy availability (Woolley et al. 2016) and major ocean currents (Lembke–Jene et al. 2017) could partly explain the variations observed in diversity and abundance throughout the NW Pacific Ocean. Large sectors of the NW Pacific Ocean are in areas of upwelling, such as the Sea of Okhotsk, the Kuril-Kamchatka Trench, Kamchatka Peninsula, Sea of Japan, and the Bering Sea (Zhabin et al. 2017), which increases the amount of nutrients available for a diverse range of species to thrive in these regions. Results from the Sea of Okhotsk indicate that sponges in this region are generally richer and more abundant than other areas sampled (Downey et al. 2018). The Sea of Okhotsk is a highly productive region (Sorokin and Sorokin 1999, Arzhanova and Zubarevich 1997, Radchenko et al. 2010, Sahling et al. 2003), and is located within a high carbon import and export latitude (Hays and Morley 2004). High levels of productivity are likely to be important in not only maintaining the high numbers of species in the Sea of Okhotsk, but also in the remarkable abundance of specimens found, which were at least eight orders of magnitude greater than theadjacent Kuril–Kamchatka region (e.g. Downey and Janussen 2015; Downey et al. 2018). Major currents that flow in and out of this region could also explain differences in faunal abundance and composition. The East Kamchatka Current, Soya Warm Current, and Kuroshio Current are warmer, saline, nutrient poor currents, whereas the East Sakhalin Current and Oyashio Current are colder, denser, less saline, nutrient and oxygen–rich currents (Lembke–Jene et al. 2017). Food-rich and highly oxygenated currents flow into NE sector of the Kuril Basin, the Bering Sea, and the northern sector of the Emperor Seamounts, which could partly explain why we find more sponge species and greater abundance in many of these regions.

The source-sink hypothesis predicts that abyssal species distributions are sinks regulated by source populations in bathyal regions (Rex et al. 2005). However, sponge species depth distributions (abyss and shallower depth zones within their entire distribution: 17 spp.) are not common in this region (Table 4), with only a quarter of species with this distribution. Therefore, the source-sink hypothesis does not explain much of abyssal species distributions in the NW Pacific Ocean. A recent study using global data, found that it is unlikely that abyssal faunal populations are sustained only by larvae from bathyal and shelf populations, and that in productive regions, such as the Sea of Okhotsk, Bering Sea, and Emperor Seamounts, reproduction is local, and could actually be important in sustaining smaller populations in less productive regions of the deep sea (Hardy et al. 2015), such as the adjacent Kuril-Kamchatka abyssal plain. Results indicate that there is strong relationship between abyssal and hadal depths, with two-thirds (6 spp.) of species in the hadal, also found in the abyss in the NW Pacific (Table 4). A transition zone between the abyss and hadal has been indicated in previous studies (Belyaev 1966, 1989; Kamenskaya 1981, 1995; Jamieson et al. 2011), and could be due to abyssal populations sustaining hadal depths. However, a third of species in the hadal are not known from any other depth, and thus, hadal regions could be geological features that have evolved their own self-sustaining populations in the NW Pacific Ocean (Ramirez-Llodra et al. 2010).

In the NW Pacific Ocean, emergence and submergence processes are important to consider in understanding the evolution of deep-sea fauna in semi-enclosed seas, such as the Sea of Okhotsk, which has only limited deep-sea straits allowing access of species between this region and adjacent deep-sea regions (e.g. Brown and Thatje 2014), and the Bering Sea, which has multiple deep-sea straits. In the Bering Sea, two hexactinellid species (Acanthascus profundum Koltun, 1967 and H. (C.) apertum simplex) could be classed as pseudo-abyssal, as they are found to be deeper in the Bering Sea than elsewhere in their distribution. Two other species, demosponge P. pacifica, and hexactinellid C. (C.) elegans, are potentially undergoing emergence, as they are found to be shallower in the Bering Sea than elsewhere in their range. The Sea of Okhotsk is connected to the Kuril–Kamchatka abyssal plain through the Krusenstern Strait (1,920 m) and the Bussol Strait (2,318 m) (Radchenko et al. 2010). Analysis of the Sea of Okhotsk sponges indicates that six demosponge species are undergoing submergence, which indicates they could be classed as ‘pseudo-abyssal’, such as Megaciella ochotensis (Koltun, 1959) and Forcepia uschakowi (Burton, 1935), whereas one hexactinellid species, C. (C.) lotifolium Ijima, 1903, could be undergoing emergence from this typically deeper abyssal and hadal ranged species (Downey et al. 2018). These results suggest that some Sea of Okhotsk and Bering Sea sponges are undergoing submergence from bathyal populations within and outside the Sea of Okhotsk, allowing the development of ‘pseudo-abyssal’ species, as well as emergent fauna from deeper distributed species, and therefore deep-sea straits could have been key in connecting these sponge communities. The lower proportion of submergent, pseudo-abyssal fauna in the Bering Sea could be due to limited sampling, but also the greater numbers of deep-sea connections to the NW Pacific abyssal plain enabling improved connectivity. However, the presence of a small number of eurybathic sponge species both within and outside of the Sea of Okhotsk and Bering Sea could indicate that emergence and submergence processes are important in understanding some of the sponge distributions in the semi-enclosed seas of the NW Pacific Ocean.

Utilising all depth information from the NW Pacific deep sea, stenobathy is found to be a common characteristic, with more than three-quarters (55 spp.) of sponges in this sector found with this trait (Table 4). Demosponges are more likely to have restricted depth distributions (39 spp., about 85%), compared to hexactinellids (15 spp., c. 65%) in the NW Pacific. Diversity in species is found to be greatest in the NW Pacific abyss, with 56 spp. found in this depth zone, compared to 20 spp. in the lower bathyal, and 13 spp. in the hadal. A known large-scale diversity pattern of deep-sea benthic communities is a unimodal relationship between diversity and depth, which peaks at intermediate depths (2,000–3,000 m) (Gray 2001). This study found the abyss to be richer in species than the lower bathyal; however, only sponges with deeper depths were analysed, and so a re-analysis of sponges found at shallower depths is needed to confirm these findings. However, abyssal depths could still be found to be richer in the NW Pacific, as there are a number of semi-enclosed basins, seamounts, and ridges at this depth range, which all have unique oceanographic features that could be enabling this abyssal diversity (Ramirez-Llodra et al. 2010). Stenobathy could be also be an artefact of sampling at a limited depth range, or it could be driven by absence of substrate, reduced food-supply at greater depths, and greater distances from deeper or shallower sites, such as in the broad abyssal plain in the NW Pacific. Less common, broader depth ranges found in both demosponges and hexactinellids are potentially driven by their ability to construct root tufts and reproduce both sexually and asexually (Tabachnick 1994), enabling them to colonise a broader range of deep-sea environments in the NW Pacific.

The deep NW Pacific is found to be a distinct biogeographic region, as it is overwhelmingly endemic, both in terms of sponge species and in terms of genera, which had been previously proposed by Menzies et al. (1973). However, the presence of large-scale oceanographic features, such as the similar levels of moderate particulate flux and the dominance of sub-Polar Gyre currents, have made a greater number of researchers to propose a single North Pacific biogeographic region (Vinogradova 1959, 1997; Kussakin and Mezhov 1979; Belyaev 1989; Watling et al. 2013). It is likely that smaller differencesgenerated by localised currents, and geological features (seamounts, trenches, ridges, and semi-enclosed basins), are far more important in the evolution of NW Pacific deep-sea sponge fauna (McClain and Mincks Hardy 2010), and these smaller features are likely important in the adjacent NE Pacific. The apparent richness of fauna surrounding the Kuril Islands, has led other researchers to hypothesise that this region could have been a recent centre of diversification for North Pacific boreal fauna (Kussakin and Mezhov 1979). So far, 15% of species found in the Kuril-Kamchatka Trench are endemic; however, the majority of samples have not been fully identified, and so these lower levels of endemism are likely to increase. Previously, exploration of trenches in the North Pacific found high numbers of endemic species, c. 40–50%, which led researchers to propose a distinct Aleutian-Japan biogeographic hadal province (Belyaev 1989; Vinogradova 1997). New species found around the Emperor Seamounts, which have not yet been found in the NW Pacific (Figure 2), indicate that seamounts are also likely to have distinct sponge communities in the NW Pacific, potentially being more faunistically connected to Hawaiian seamount chain, and they could also be a barrier between the NW Pacific and NE Pacific abyssal sponge fauna.

Moderate abyssal faunal connectivity is found between the NW Pacific region and other sectors of the Pacific Ocean (18 spp.), and this faunal connection is stronger with the rest of North Pacific (Table 2). Several species, which are new to this region, including Lycopodina globularis (Lévi, 1964), Chondrocladia (C.) koltuni Vacelet, 2006, and Cladorhiza mirabilis (Ridley & Dendy, 1886), highlight this faunal connection, as they were previously only known from the N and NE Pacific abyss (Lévi 1964; Koltun 1970; Vacelet 2006). The deep-sea Aleutian Island Archipelago sponge fauna, distributed both in the Bering Sea and abyssal North Pacific, has previously found to have strong taxonomic affinities with the Sea of Okhotsk sponge fauna (30% of species in common) (Stone et al. 2011). In this study, at least 12 spp. and 2 sub. spp. are found to be distributed in the Bering Sea/Aleutian Island area, as well as elsewhere in the NW Pacific. The majority of these species are hexactinellids, which could have come from the North Pacific Bering Sea region, which appears to be richer in glass sponges from latitudinal analysis in this study, and could have been distributed via the anticlockwise currents associated with the sub-Polar Gyre, to the Kamchatka Peninsula, the Sea of Okhotsk and the remainder of the region. Most deep-sea sponges are likely to be hermaphrodites, reproducing both sexually and asexually, and likely producing lecithotrophic (non-feeding) larvae. In one sponge study, researchers found high levels of genetic variability within populations, which indicated contributions from both highly dispersed sexually produced larvae and asexually produced budding/fragmentation (Maldonado and Uriz 1999). Despite vast distances and depths, some sponge species in the deep sea are likely connected through long-distance sexual and asexual dispersal through currents, across broad, often fragmented, distributions.

Acknowledgements

We would like to thank our DFG (Deutsche Forschungsgemeinschaft), project JA-1063/17-1 and the joint Russian–German SokhoBio andKuramBioII expeditions for funding the field research for Melanie Fuchs and Rachel Downey. Rachel Downey would also like to acknowledge her Australian Government Research Training Grant for funding the synthesis of this project. We would also like to especially thank Hanieh Saeedi for the production of maps and the project management of this book, and Angelika Brandt and Marina Malyutina for organising workshops and expeditions, as well as the crew of the RV Akademic M.A. Lavrentyev and RV Sonne for their help and guidance during these expeditions.

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Chapter 3. CNIDARIA AND CTENOPHORA: REVIEW OF DEEP-SEA CNIDARIA AND CTENOPHORA FAUNA IN THE NW PACIFIC OCEAN

aMolecular Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan
bTropical Biosphere Research Center, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan
cCoastal Branch of Natural History Museum and Institute, Chiba, Yoshio 123, Chiba 299-5242, Japan
dSenckenberg Research Institute and Natural History Museum, Senckenberganlage 25, 60325 Frankfurt, Germany
eGoethe University of Frankfurt, FB 15, Institute for Ecology, Evolution and Diversity, Max-von-Laue-Str. 13, 60439 Frankfurt am Main, Germany
fOBIS Data Manager, Deep-sea Node, Senckenberg Research Institute and Natural History Museum, Senckenberganlage 25, 60325 Frankfurt, Germany
gAdvanced Science-Technology Research (ASTER) Program, Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Email: jreimer@sci.u-ryukyu.ac.jp*, dhugal@jamstec.go.jp*

1. Introduction

The marine region encompassed between 40°N and 60°N and 120°E to 180°E contains a large area of the NW Pacific Ocean, including the northern half of the Sea of Japan, the Sea of Okhotsk, the southwestern part of the Bering Sea, and the Pacific Ocean, as well as the Kamchatka Peninsula, the Kuril Islands and the northern Japanese Islands. Much of this marine region is deep sea (>200 m in depth). Economically, the region is among the most productive marine fisheries regions in the world, including not only open-water fisheries but also commercially important crab fisheries (Spiridonov 2005). Despite its obvious importance to the global fishery, research on many marine taxa in the region is lacking, due to the relative remoteness of the region as well as other logistical issues such as severe weather. The lack of data and research in the region thus hampers our knowledge of many marine taxa, making conservation and protection planning difficult.

In this chapter, we will examine the state of knowledge in the NW Pacific Ocean for two phyla of marine invertebrates, the Cnidaria and Ctenophora, at depths below 2,000 m, in the lower bathyal (2,000–3,000 m), abyssal (3,000–6,000 m) and hadal (>6,000 m) zones. These two phyla are among the most ancient of metazoans (Simion et al. 2017), and are often grouped together as “coelenterates”, although the scientific validity of such a group has now been debunked (e.g. Whelan et al. 2015; Simion et al. 2017; Nielsen 2019). Although superficially similar morphologically, this similarity is only at the macromorphological level, with both groups being often fragile and gelatinous. For example, ctenophores have rotational symmetry while cnidarians have diverse symmetries (including bilateral and radial symmetry). In all probability, the Cnidaria and Ctenophora are sister groups that evolved independently from the last common ancestor of Eumetazoa (Nielsen 2019).

Cnidaria (Figure 1) include the various corals, true jellyfish, and related animals, and can be broadly split into three major groupings; 1) the class Anthozoa, primarily benthic corals and allies, 2) the subphylum Medusozoa of true jellyfish (classes Scyphozoa, Cubozoa, Staurozoa) and hydrozoans (class Hydrozoa), and the classes 3) Myxozoa and Polypodiozoa, marine parasites. Cnidaria can be united by cnidocytes (“polar capsules” in Myxozoa), which are specialized cells used for prey capture, defense, and/or attachment. Many Cnidaria have asexual and sexual life-history stages, with two basic body forms, benthic polyps with a single oral opening facing upwards, and a planktonic medusa with the oral opening facing downwards. Around these oral openings, tentacles are aligned in various arrangements.

Figure 1.

Some Cnidaria and Ctenophora species observed in the deep sea of the NW Pacific. (A) Stone with numerous benthic animals, including light pink alcyonarians, dark brown polychaete tubes, and light brown broken-off hydrozoan colony (?) from station 8–5 EBS, depth 2,327-2,330 m. Scale = 5 mm. (B) Actinarian Hormathia spinosa from station XR-10 off Kushiro, depth 5,509-5,561 m. (C) Actinarian Galatheanthemum sp. from station XR-12 off Kushiro, depth 5,471-5,514 m. (D) Octocoral Aspera rosea from station 8-4 EBS, depth 2,333-2,336 m. Scale = 5 mm. (E) Halicreas minimum from 1,043 m in Sagami Bay, Japan; this species has also been reported from >2,000 m within the study area of the NW Pacific. Images A and D by Anna Lavrentieva, B and C by Kensuke Yanagi, and E by Dhugal Lindsay.

Cnidarians are common components of the deep-sea plankton and benthos (e.g. Hunt and Lindsay 1999; Cairns 2007; Dautova 2018a,b), and can often be considered as ecosystem engineers, providing habitat for other marine organisms (Ohtsuka et al. 2009; DiCamillo et al. 2013). As such, their diversity, abundance, and distribution in the water column and on the seafloor are important datasets in establishing conservation and protection planning. Deep-sea Cnidaria contain some of the most well-known and spectacular organisms from these ecosystems, including examples such as Pandearubra, a hydrozoan anthomedusan species that illustrates the run-on effect that ocean acidification can be expected to have on deep-pelagic ecosystems (Lindsay et al. 2008), as well as the huge, red, tentacle-less “fingerfoot medusa” Tiburonia granrojo (Matsumoto et al. 2003), Epizoanthus zoantharian species symbiotic with hermit crabs (Muirhead et al. 1986; Ryland and Ward 2016; Kise et al. 2019), and the enigmatic Relicanthus anemone, a sea anemone with unusual phylogenetic placement (Rodriguez et al. 2014; Xiao et al. 2019).

Ctenophores are also common components of the deep-sea plankton, sometimes being almost as abundant as cnidarians (e.g. Fig. 7 in Lindsay et al. 2000), with members of the benthic ctenophoran order Platyctenida commonly observed as epibionts on other benthic deep-sea animals (DJL, pers. obs.).

2. Objectives

The main objective of this chapter is to provide an overview of the state of current knowledge of the phyla Cnidaria and Ctenophora at depths below 2,000 m in the NW Pacific by examining records and occurrences from the Ocean Biogeographic Information System (OBIS) database combined with additional records from the literature and unpublished data.

3. Materials and Methods

In this review of knowledge of the Cnidaria and Ctenophora of the NW Pacific, we searched for records and occurrence data for each phylum in the Ocean Biogeographic Information System (OBIS 2020) on January 4, 2020. We limited our data search to depths below 2,000 m, and within 40°N to 60°N and 120°E to 180°E. Resulting datasets were downloaded, and assessed by taxonomic experts of each group (Anthozoa: JDR, KY, Medusozoa + Ctenophora: DJL). The OBIS Cnidaria dataset initially included 184 occurrence records, while that of the Ctenophora included three occurrence records. We subsequently removed eight records from the Cnidaria dataset as the species identities and depths were clearly erroneous, and corrected the taxonomic nomenclature of several other records. We also added Actiniaria records from two research cruises that were not previously published; the Japan Agency for Marine Science and Technology’s (JAMSTEC) KH01-2 cruise by the RV Hakuho-Maru in October to November 2001 around Chishima and the Japan Trench (n=38), and the KT08-27 cruise by the RV Tansei-Maru in October 2008 off the Sanriku Coast of northeastern Honshu, Japan (n=5) (both datasets and identifications from KY). We additionally added Octocorallia occurrence records (n=21) from Dautova (2018a) and Hydrozoa and Scyphozoa occurrence records (n=16) from Naumov (1971). After these checks, edits, and additions, the Cnidaria dataset contained 256 records, while the Ctenophora record numbers remained unchanged. Taxonomy of both phyla followed the World Register of Marine Species (WoRMS 2020). It should be noted that the higher taxonomy of the phylum Ctenophora is in desperate need of revision (e.g. Podar et al. 2001; Lindsay and Miyake 2007). Datasets are available as Supplemental Material 1.

We then examined the datasets in detail, and assessed 1) numbers of species (counting only records identified to species), 2) numbers of records by lowest taxonomic rank, 3) numbers of species for each larger taxonomic grouping (class/subclass/order), 4) numbers of records by depths, and 5) numbers of records reported by year. After this, we then reviewed and discussed the state of knowledge for both phyla in the NW Pacific Ocean, and propose ways forward to broaden our knowledge of these taxa in the deep sea of this region.

4. Results

Images of some Cnidaria and Ctenophora species observed in the deep sea of the NW Pacific are shown in Figure 1.

4.1 Cnidaria

Within Cnidaria, of 256 records and occurrences, 86 were for planktonic taxa (=33.6% of Cnidaria records), and 166 (=64.8%) were for benthic anthozoan taxa. Four records (=1.6%) were only noted as “Cnidaria” and could not be placed into either group. No Myxozoa or Polypodiozoa were reported. Within the non-Anthozoan cnidarians, there were 28 Scyphozoa (=10.9% of Cnidaria, 32.6% of Medusozoa), 58 Hydrozoa (=22.6%, 67.4%, respectively), and no Staurozoa or Cubozoa. Within Anthozoa, there were 28 Octocorallia (=10.9% of Cnidaria, 16.9% of Anthozoa), seven Scleractinia (=2.7%, 4.2%), and 83 Actiniaria (=32.3%, 50.0%), with an additional 48 records for “Anthozoa” only (=18.7%, 28.9%).

By lowest taxonomic rank, four records were to phylum (=Cnidaria; 1.6% of Cnidaria), 92 to class (=35.9%), one to subclass (=0.4%), 19 to order (=7.4%), 13 to superfamily (=5.1%), 12 to family (=4.7%), 29 to genus (=11.3%), and 86 to species (=33.6%). The 86 species records consisted of 23 different species: eight Hydrozoa, one Scyphozoa and 14 Anthozoa (eight Actiniaria, five Octocorallia, and one Scleractinia). By numbers of records, the anemone Edwardsia sojabio Sanamyan N. & Sanamyan K., 2013 was by far the most common, with 33 occurrences, followed by the octocoral Radicipes sakhalinensis Dautova, 2018 (n=9), the hydrozoans Opercularella angelikae Stepanjants, 2012 (n=7), Botrynema brucei Browne, 1908(n=5), the anemone Hormathia spinosa (Hertwig, 1882) (n=5), the hydrozoans Halicreas minimum Fewkes, 1882 (n=3), and Pantachogon haeckeli Maas, 1893 (n=3), the scleractinian Fungiacyathus (Bathyactis) marenzelleri (Vaughan, 1906) (n=3), the scyphozoan Atolla wyvillei Haeckel, 1880 (n=2), the octocoral Aspera rosea Dautova, 2018 (n=2), and the actiniarian Bathydactylus kroghi Carlgren, 1956 (n=2, tentative identification). All other species only occurred once in our dataset.

By depth, there were nine records from >6,000 m, 90 from 5,000 to 6,000 m, 29 from 4,000 to 5,000 m, 73 from 3,000 to 4,000 m, and 55 from 2,000 to 3,000 m (Figure 3). The deepest records were for the hydrozoan Pectis profundicola (Naumov, 1971) between 6,800 to 8,700 m (Naumov 1971), an unidentified Anthozoa from 7,366 m, the actiniarians Bathydactylus kroghi from 7,141 m, and Sicyonis sp. (tentative identification), Galatheanthemum sp. and Mesomyaria sp. E from 7,139 m, as well as an unidentified Cnidaria at 6,985 m.

Figure 2.

Records from the NW Pacific below 2,000 m of Cnidaria and Ctenophora by lowest taxonomic rank of identification (total n=256).

Figure 3.

Records from the NW Pacific below 2,000 m of Cnidaria and Ctenophora by depth in m (total n=256).

By year, the earliest records of Cnidaria within the region were from 1906 (specimens now housed in the Smithsonian, USNM), but these were removed from our dataset as described in the methods due to their capture depths being inferred as being at the seafloor, presumably during their import into the OBIS dataset, even though they were obviously from the pelagic zone closer to the surface (DJL, pers. obs.). Thus, subsequently, the next records were from 1966 (Naumov 1971) and 1981, while the large majority of Cnidaria records from the region were from 2000 or later, from only two cruises by K. Yanagi in 2001 and 2008 and a few publications, namely Brandt et al. (2013), Sanamyan and Sanamyan (2013), Stepanjants (2013), Trebukhova et al. (2013), Brandt et al. (2015), Fischer and Brandt (2015), Schwabe et al. (2015), and Dautova (2018a,b).

4.2 Ctenophora

Within Ctenophora, there were only three records from the entire marine region, all of which were only identified to phylum level. Thus, there is no information on orders or numbers of species present. These three records were from depths of 4,859 to 5,379 m. The three records were all recorded from 2012 and reported in two papers; Brandt et al. (2015) and Fischer and Brandt (2015). Figure 11F in Brandt et al (2015), includes a photograph of a ctenophore of the Class Lobata (St. 11–9, 5,362 m depth) which, although not included in the original OBIS-derived data, would make this a fourth record for Ctenophora at abyssal depths in the study area.

4.3 Distributional patterns

Although distribution maps for various taxonomic groupings of cnidarians have been provided in this chapter (Maps 111), we consider the state of knowledge to still be too nascent to make serious hypotheses on distributional patterns of Cnidaria or Ctenophora in the NW Pacific.

Map 1.

Map of occurrence records of phylum Cnidaria from the NW Pacific below 2,000 m. Note these records are for occurrences not identified to any taxonomic level below Cnidaria.

Map 2.

Map of occurrence records of class Anthozoa from the NW Pacific below 2,000 m. Note these records are for occurrences not identified to any taxonomic level below Anthozoa.

Map 3.

Map of occurrence records of subclass Octocorallia from the NW Pacific below 2,000 m.

Map 4.

Map of occurrence records of order Scleractinia from the NW Pacific below 2,000 m.

Map 5.

Map of occurrence records of order Actiniaria from the NW Pacific below 2,000 m. Note these records are for occurrences not identified to any taxonomic level below Actiniaria.

Map 6.

Map of occurrence records of actiniarian superfamilies Actinostoloidea and Actinioidea and the family Galatheanthemidae from the NW Pacific below 2,000 m.

Map 7.

Map of occurrence records of actiniarian suborder Anenthemonae from the NW Pacific below 2,000 m.

Map 8.

Map of occurrence records of actiniarian superfamily Metridioidea from the NW Pacific below 2,000 m.

Map 9.

Map of occurrence records of class Hydrozoa from the NW Pacific below 2,000 m.

Map 10.

Map of occurrence records of class Scyphozoa from the NW Pacific below 2,000 m.

Map 11.

Map of occurrence records of class Ctenophora from the NW Pacific below 2,000 m.

5. Discussion

The area examined in this paper between 40°N to 60°N and 120°E to 180°E covers over nine million square kilometers of the Earth’s surface, with the majority being marine. Of this marine area, a large portion is below 2,000 m in depth (e.g. see maps 111), and thus it is easy to state that the deep-sea area we examined in this study is vast. Despite this, records indicate less than 250 records of cnidarians, and only three records of ctenophores from this region. These records are almost completely from within the last 20 years. It is not an overstatement to say that research on these basal metazoan groups is almost completely lacking for the region, and that this research is in its infancy.

Within the region examined in this study, there are undoubtedly more specimens and records than we have reported here. For example, other planktonic Cnidaria records from the NW Pacific include those from four deep dives by the Mir submersibles in the Kurile-Kamtchatka Trench that were analyzed by Vinogradov and Shushkina (2002), but the majority of the pelagic cnidariantaxa reported below 2,000 m depth were unidentifiable to species level, with the exception of Pantachogon haeckeli Maas, 1893 (reported as >2,500 m depth) and Botrynema brucei Browne, 1908 (deepest record at 3,400 m depth). Even generic identifications in Vinogradov and Shushkina (2002) were marked with question marks (e.g. Poralia?, Turritopsis?) or were for genera that have never previously been reported from depths below 2,000 m (e.g. Colobonema), illustrating the lack of information in general on bathyal and abyssal gelatinous zooplankton (Vinogradov and Shushkina 2002). These records have not been included in the dataset of the current study.

As well, Brandt et al. (2018) reported that there were 43 Cnidaria specimens collected in the2015 SokhoBio Expedition in the Sea of Okhotsk, but asides from 21 records mentioned in Dautova (2018a) already included in our current dataset, we could not find detailed information on these specimens.

It is well known that the marine environment becomes more similar with surrounding regions as depth increases (Vecchione et al. 2015), and looking at the deepest records worldwide of various cnidarian and ctenophore taxa may provide a guideline for what species we may expect to find in future surveys of the NW Pacific. According to Malyutin (2015), the deep-sea coral communities of the Aleutian Islands, the eastern Bering Sea and the Gulf of Alaska (northestern Pacific) are similar to the coral communities of the NW Pacific. All the occurrence records in Malyutin’s 2015 paper had depths shallower than 1,000 m. Although we might expect similar trends at deeper depths, the investigation of additional deep-water communities in those areas is crucial to further corroborate such prediction.

For example, for Anthozoa, there are records of the orders Actiniaria (sea anemones), Scleractinia (hard corals), and the subclass Octocorallia (soft corals, sea pens) from the NW Pacific area examined in this study. However, from the presence and depths of anthozoans from other regions, we may also expect to find the subclass Ceriantharia (deepest report of Cerianthus valdiviae Carlgren, 1912, from 5,248 m, Indian Ocean south of Sumatra, OBIS dataset), and the orders Corallimorpharia (Corallimorphus sp. reported from 5,274 m, South Orkney Islands, USNM catalogue number 61003), Zoantharia (Abyssoanthus convallis, 5,362 m, Japan Trench, Reimer & Sinniger, 2010), and Antipatharia (Stichopathes variabilis van Pesch, 1914, 7,000 m, Sunda Trench, ZMUC Gal-II-1248) within the NW Pacific.

Similarly, regarding planktonic data, the class Staurozoa has been reported down to 2,694 m (Lucernaria janetae Collins & Daly, 2005, East Pacific Rise). The deepest record for a cnidarian is currently a small red rhopalonematid hydromedusa (DJL, pers. obs.), observed at 9,970 m depth in the Mariana Trench by a drop camera (Gallo et al. 2015). The deepest scyphozoan record is for an ulmarid medusa at 8,200 m depthin the New Britain Trench (Gallo et al. 2015), identified at the time as tentatively belonging to the subfamily Poraliinae but now believed to warrant the erection of a new subfamily to contain it (DJL, pers. obs. based on new material collected in 2019 in the Gulf of Alaska). The deepest record for a ctenophore is 7,217 m depth in the Ryukyu Trench, for an enigmatic tentaculate ctenophore that anchors itself to the sediment by two filaments, while trailing two tentacles that lack tentillae (Lindsay and Miyake 2007). On the other hand, the cnidarian classes Cubozoa, Myxozoa, and Polypodiozoa have not been reported from depths of >2,000 m worldwide, and thus we would not expect them to be present in the NW Pacific.

Another way to predict more about the deep-sea Cnidaria and Ctenophora fauna of the NW Pacific would be to examine occurrence records and information from neighboring regions that are more well examined. For example, the waters around Japan have long been surveyed and there are comparatively many more records, other data, and specimens from the deep sea of this area (e.g. Kitamura et al. 2008a, b). There are also deep-sea records of anthozoans to the east from the Aleutian Islands of Alaska (e.g. Cairns 1994; Heifetz et al. 2005; Herrera et al. 2010; Cairns 2011; Cairns and Lindner 2011; Thoma 2013; Stone and Cairns 2017).

From marine regions to the south of the current area of interest, there are many additional Cnidaria and Ctenophora records. For benthos, in the western Pacific, Williams (2011) reported the octocoral sea pen genera Gyrophyllum at depths ≥2,000 m, and Protoptilum and Scleroptilum at depths ≥4,000 m. Among gorgonians, Swiftia pacifica (Nutting, 1912) is a western Pacific bathyal species whichhas been found at depths ≥2,000 m (Horvath 2019). Similarly, Imahara (1996) noted the gorgonian Bathygorgia profunda Wright, 1885 from 4,200 m, and the sea pen Kophobelemnon stelliferum (Müller, 1776) from down to 3,650 m in Sagami Bay. Additionally, from older records, Kölliker (1880) reported two more sea pen species from the deep sea of the North Pacific Ocean; an Umbellula (Gray, 1870) species from approximately 3,750 m, and Scleroptilum grandiflorum Kölliker, 1880 from approximately 4,200 m. Among other anthozoans, two species of the deep-sea zoantharian genus Abyssoanthus (Reimer & Fujiwara in Reimer, Sinniger, Fujiwara, Hirano & Maruyama, 2007) are known from the Japan Trench (5,347-5,360 m; Reimer andSinniger 2010) and the Nankai Trough (3,259 m; Reimer et al. 2007), respectively.

Regarding planktonic species, between 2,000-4,000 m depths in the Japan Trench, Lindsay (2005) reported the occurrence of unidentified narcomedusan species belong to the genera Solmissus (Haeckel, 1879) and Aegina (Haeckel, 1879). The most commonly observed medusa was Botrynema brucei Browne, 1908, which was most abundant in the 2,000-2,500 m layer but occurred down to 3,500 m depth (Lindsay 2005). The Bathocyroe (Madin & Harbison, 1978) species observed below 4,000 m depth was also most abundant in the 2,000-2,500 m depth layer (Lindsay 2005). The only other pelagic cnidarians identified to species level by Lindsay (2005) were: the trachymedusae Halicreas minimum Fewkes, 1882 (2,439 m depth) and Crossota aff. millsae (3,668 m depth); the physonect siphonophoresMarrus antarcticus pacificus Stepanjants, 1967 [=Marrus orthocanna (Kramp, 1942)] (2,869 m depth) and Tottonia contorta Margulis, 1976 (=Apolemia sp.) (2,810 m depth); and the ulmarid scyphomedusa Poralia rufescens Vanhöffen, 1902 (2,522 m depth). An extremely large (ca. 80 cm diameter) Aulacoctenid cydippid ctenophore was observed at 3,562 m depth (Lindsay 2005).

However, even in surrounding regions, some taxa still display an apparent lack of data. For example, very little information has been published on the abyssal planktonic cnidarian and ctenophoran fauna of the entire NW Pacific Ocean with the notable exceptions of several works by Naumov and Lindsay (e.g. Naumov 1971; Lindsay 2005). Lindsay (2005) recorded a coronate medusa belonging to the genus Periphylla (F. Müller, 1861) at 6,464 m depth in the Japan Trench, though they were hesitant to identify it as the species Periphylla periphylla (Péron & Lesueur, 1810) due to the spiralling morphology and white colour of the tentacles. Below 4,000 m depth, Lindsay (2005) recorded an undescribed lobatectenophore species belonging to the genus Bathocyroe, as well as at least two species of physonect siphonophores (as “Agalmidae”), four species of hydroidomedusae (non-Narcomedusan), one “cydippid” ctenophore species and one other lobate ctenophore species.

Formal taxonomic species descriptions can help collate past data, and thus provide important information. This can be clearly seen for the sea anemone species Edwardsia sojabio, which is by far the species with the most numerous numbers of records for both phyla examined here, directly as a result of its formal species description (Sanamyan and Sanamyan 2013). Similarly, the octocorals I. rubeus, A. rosea, and R. sakhalinensis were recently described from specimens collected in 2015 (Dautova 2018a), greatly increased our knowledge of deep-sea octocorals in the region, increasing the numbers of records by four times (7 to 28 records). Species descriptions by their nature will provide taxa identified to the species level, something that is sorely lacking from our current understanding of the gelatinous fauna of the NW Pacific. Similarly, the previously unpublished data from two cruises newly reported in this paper (KH01-2, KT08-27 datasets) almost doubled the amountof sea anemone data available, increasing the number of records of Actiniaria from 43 to 85. Thus, it can be easily concluded that even single studies can greatly increase our knowledge on Cnidaria and Ctenophora in the NW Pacific given the current state of our understanding.

Due to the paucity of data, conclusions on the patterns of distribution within the NW Pacific remain to be made. For example, there are almost no data for many Cnidaria or Ctenophora taxa for the deep sea below 2,000 m in the northern Japan Sea (e.g. Maps 414). Examining data from further south, a high diversity of deep-sea ctenophores has been reported on the Pacific side of the Japanese archipelago (Lindsay and Hunt 2005), while only the beroid ctenophore Beroe abyssicola Mortensen, 1927, the “cydippid” ctenophore Euplokamis sp. and the lobate ctenophore Bolinopsis infundibulum F.O. Müller, 1776 have been recorded in the deep Japan Sea at the present time, albeit above 1,000 m depth (Lindsay and Hunt 2005). As the water mass in the deep Japan Sea (Japan Sea Proper Water) remains homogeneous below the thermocline, with extremely low temperatures, the above three ctenophore taxa can be inferred to be secondary deep-sea species that have invaded the deep Japan Sea to take advantage of the niche space made available by primary deep-sea taxa not being able to survive at such temperature-pressure combinations (Lindsay and Hunt 2005). The Ctenophora of the deep NW Pacific Ocean would be expected to contain both primary and secondary deep-sea forms. Future work should not only focus on the NW Pacific, but particularly on areas shown by this review to be neglected thus far.

Conclusions

Due to the lack of Cnidaria and Ctenophora data in the NW Pacific, it is far too premature to make any conclusions on abundances, total diversity, endemicity, or ecology of the various cnidarian and ctenophore species in the region. One positive aspect that can be discerned from the general lack of Cnidaria and Ctenophora deep-sea data from the NW Pacific is that any future surveys or research on the region will almost assuredly gather important new information.

Although many oceanographic cruises and research expeditions have been undertaken over the last two centuries with the aim of exploring the marine diversity of the NW Pacific and Far East, such as the Pacific expedition led by Mortensen in 1914 and the Galathea Expedition organized by the Zoological Museum University of Copenhagen (ZMUC), most of these expeditions were further south from the NW Pacific region between 40°N and 60°N and 120°E to 180°E examined in the current paper. Expeditions and cruises make the collection of a variety of marine invertebrates possible, which are then deposited in museums and research institutes. However, even with extensive and massive sampling campaigns, the identification of material, especially at the species level, is often hampered by a lack of taxonomic specialists. Thus, we strongly recommend future research cruises investigating the deep sea of the NW Pacific involve relevant Cnidaria and Ctenophora taxonomy experts to help increase the current paucity of data for these two phyla (as seen in the 2015 SokhoBio survey; Brandt et al. 2018; Dautova 2018a). Due to theextreme fragility of many taxa within these two gelatinous phyla, future surveys should include a crewed submersible or remotely-operated vehicle in order to collect both in-situ photographic and video records and the physical specimens needed for a complete morphological and molecular characterization of the fauna. Once this high-quality baseline data has been collected and vetted by taxonomic experts it will become possible for future surveys to be carried out at lower cost using such tools as towed cameras and environmental DNA probing, but our present state of knowledge about these taxa in the study area prohibits such approaches at the present time.

Acknowledgements

JDR thanks Dr. Takuma Fujii (Kagoshima University) for his assistance in searching for relevant data. DJL expresses his appreciation to Ms. Kumiko Oshima for assisting with the transcription of published data into a digital, Darwin Core-compatible format. This book could not be published with a financial support of “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project“ (BENEFICIAL project)” funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany (grant number 03F0780A).

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Chapter 4. BRACHIOPODA: A REVIEW ON DEEP-SEA BRACHIOPOD PELAGODISCUS ATLANTICUS (KING, 1868) FOUND ALONG THE NW PACIFIC

Invertebrate Zoology Department, Biological Faculty, Moscow State University, 119991, Moscow, Russia
Email: kuzmina-t@yandex.ru*

1. Introduction

The brachiopods or lamp shells are a diverse group of exclusively marine invertebrates. Their bodies are enclosed in two bilaterally symmetrical valves. The ventral (pedicle) valve is usually larger than the dorsal (brachial) valve. The shell morphology, and its various skeleton structures, and its soft body impression, are well preserved in fossil states and allow tracing of the evolution of these animals. Brachiopods are known from the early Cambrian with the greatest diversity found during the Palaeozoic. The modern brachiopods comprise only 5% of the total number of species that ever existed on Earth (Carlson 2016).

The brachiopods have a pelago-benthic life cycle with larval or juvenile planktonic and benthic adult stages (Lüter 2007; Kuzmina et al. 2019). Most brachiopods are epifaunal animals with a few exceptions. The adults attach to the substrate with a pedicle, which can regulate the position of the shell relative to water currents or may cement with their ventral valves. All brachiopods are filter feeding animals and filter using a special tentacle-organ, the lophophore. The lophophore is “a tentaculated extension of the mesosoma (and its cavity, the mesocoelom) that embraces the mouth but not anus” (Hyman 1959; Emig 1976). The presence of lophophore characterizes Lophophorata, a group that includes Bryozoa, Phoronida and Brachiopoda. In brachiopods, the lophophores may vary from the simple ring shape (trocholophous) to the curved shape consisting of three arms (plectolophous) (Emig 1992; Kuzmina and Temereva 2019). The brachiopod lophophores are located within the mantle cavity, a space between the valves. Tentacles are covered by ciliary bands that create the water currents.

The phylum Brachiopoda Duméril, 1805 consists of three subphyla: Linguliformea Williams, Carlson, Brunton, Holmer & Popov, 1996, Craniiformea Popov, Basset, Holmer & Laurie, 1993, and Rhynchonelliformea Williams, Carlson, Brunton, Holmer & Popov, 1996. The shell linguliforms is organophosphatic and lacks articulatory structures. The linguliforms have a U-shaped gut with an anus that is located anterior on the right side. Recent linguliforms are represented in only two families, Lingulidae Menke, 1828, and Discinidae Gray, 1840, which strongly differ in their biology and the morphology of their shells and soft bodies (Emig 1997). The lingulides are infaunal, they have a long muscle pedicle and burrow into soft sediments. The discinides are epifaunal and live on hard substrates usually fixed by a short muscle pedicle.

The craniiforms is a minor group of brachiopods and comprise only one class with a recent family Craniidae Menke, 1828, with three extant genera. All craniiforms have organocalcitic shell without articulatory structures. The gut is open with the anus located in the posterior midline of the body. Recent craniiforms lack the pedicle to cement themselves to substrate by the ventral valve (Williams et al. 1997).

The rhynchonelliforms are the most advanced group of brachiopods. This subphylum includes five classes but only the class Rhynchonellata Williams, Carlson, Brunton, Holmer & Popov, 1996, retains extant species, which includes threeorders: Rhynchonellida Kuhn, 1949, Thecideida Elliot, 1958, and Terebratulida Waagen, 1883. The rhynchonelliform shell is calcitic and has well-developed articulation structures and the calcitic lophophore supports the brachidium. The gut of the recent rhynchonelliforms is blind, so the fecal pellets are eliminated through the mouth (Williams et al. 1997).

Recent brachiopods are found in all seas and oceans from the Arctic to the Southern Oceans (Zezina 2008). The north subtropical and tropical zones contain the largest number of species. Each of these zones includes almost a third of the entire fauna of extant brachiopods (see table 6 in Zezina 2008). The rhynchonelliforms include a large number of endemic species, while the recent linguliforms lack endemic species (Richardson 1997). This is due to the presence of planktotrophic stages of linguliformes that can float up to six weeks (Chuang 1959; Paine 1963), while the craniiform and rhynchonelliform larvae swim for only 4 days.

The extant brachiopods occur in all depths from littoral to abyssal except ultra-abyssal (Bitner et al. 2013). However, most of the recent brachiopods prefer to live on the seaward edge of the shelf and the upper part of the slope, which can be explained by the following factors (Zezina 2008):

    2. Objectives

    The current chapter is a review of published data on deep-sea brachiopod Pelagodiscus atlanticus (King, 1868) found during four Russian-German deep-sea expeditions in the NW Pacific Ocean.

    3. Material and Methods

    Two specimens of P. atlanticus were collected in the Kuril-Kamchatka Trench (45° 12 02′N, 151°60 08′E) during the German-Russian expedition Kurambio II on RV Sonne (16 August 2016–26 September 2016) (Map 1). Specimens were obtained at 5,571.6 m depth using the Agassiz Trawl at station number SO-250-86.

    Map 1.

    Distribution of Pelagodiscus atlanticus.

    3.1. Microscopy

    Two whole specimens with diameters of dorsal valves 4.0 and 4.2 mm, respectively, were fixed in 2.5% glutaraldehyde in filtered sea water. After fixation, the specimens were rinsed in 0.1 M phosphate buffer. Fixed animals were photographed in the laboratory using a Leica MZ6 stereomicroscope (Leica Microsystems GmbH, Wetzlar, Germany) equipped with a digital camera. After post-fixation, specimens were placed in a 1% osmium tetroxide in phosphate buffer for 30 min at 20°C, the specimens were rinsed in distilled water, dehydrated in ethanol and isopropanol, and embedded in Spurr Resin (Epoxy Embedding MediumKit, Fluka, Switzerland). Semi-thin and ultra-thin sections were prepared with a diamond knife on a Leica UC5 ultratome (Leica Microsystems GmbH, Wetzlar, Germany). Specimens were cut serially; ultrathin sections were taken every 10 μm. Semi-thin sections were stained with methylene blue and examined and photographed with a Zeiss Axioplan 2 imaging photomicroscope. Ultrathin sections were stained with uranyl acetate and lead citrate, and were examined with a Jeol Jem 100 V and Jeol-1,011 80 kV transmission electronmicroscopes (JEOL Ltd., Tokyo, Japan).

    3.2. Micro-CT (Micro-computed tomography)

    X-ray imaging of whole specimens embedded in Spurr Resin was performed with a SkyScan 1172 micro-CT scanner (Bruker) at the Laboratory of Natural Resources, Geological Faculty, Moscow State University. The specimens were scanned at a resolution of 1.68 μm, with a rotation step of 0.3°, without a filter, and at current conditions of 40 kV and 250 mA. The 3D reconstruction was obtained using the program NRecon. CTan and CTvol software were used for data processing.

    4. Results

    P. atlanticus is a small deep-water representative of family Discinidae, a linguliform brachiopod. Its soft body is enclosed by dorsal and ventral chitinophosphatic valves, which are very small and thin (Figure 1). The dorsal valve (about 4 mm in diameter) is much larger than the ventral valve (about 3 mm in diameter). The valves grow holoperipherally, so the apex (first-formed region) is near the center of the valve (Figure 1a). The body wall forms mantle folds that line the inner surface of both valves. Marginal long and short setae emerge from the edge of both mantles. The short muscle pedicle attaches the ventral valve to the hard substrate (Figure 1c) (Kuzmina and Temereva 2019). P. atlanticus has a small simple horseshoe-shaped lophophore with two arms directed posteriorly (Figure 1b) (Kuzmina and Temereva 2019). The lophophoral arms are located symmetrically about the mouth. The basal part of the lophophore is attached to the anterior body wall. The distal portions of the arms are separated from the body wall and are raised into the mantle cavity. The arms are fringed with a double row of tentacles. Two coelomic canals, large and small, extend inside each arm of the lophophore. Hydrostatic pressure in the large coelomiccanals supports the arms of lophophore. The small canals connect with the coelomic canals of tentacles and perform transport functions. The lophophore of P. atlanticus was regarded as a modified zygolophous type and, apparently, demonstrated the distinct part of the lophophore evolution of brachiopods (Kuzmina and Temereva 2019). This simple form of the lophophore is a transition form in the ontogenesis of other representatives of discinides (Zezina 2015).

    Figure 1.

    Dorsal and ventral chitinophosphatic valves of deep-water of Pelagodiscus atlanticus (Kuzmina & Temereva, 2019). (A) Dorsal view of the fixed animal: the dorsal valve (dv) with long setae (ls) is visible. (B) Ventral view of the fixed animal: the ventral valve (vv) is partly open, and the mantle cavity (mc) contains two lophophoral arms (lam). (C) View of the ventral valve (vv) with short setae (ss) and a round pedicle (p). first-formed region of the shell.

    We studied the spermatogenesis and ultrastructure of sperm in P. atlanticus (Temereva and Kuzmina 2018). The spermatozoon has a large acrosome, a small compact nucleus, eight mitochondria around the nucleus, two orthogonal centrioles, and a long tail. Comparative evaluation of all data on the structure of brachiopod spermatozoa indicates that P. atlanticus retains the most ancestral type of spermatozoon among all brachiopods.

    5. Discussion

    Thera are 63 species of deep-sea recent brachiopods that live at a depth of more than 2,000 meters and can be divided into two groups (Zezina 1989, 1994). The first group contains eurybathic species, the second is exclusively deep-sea animals (Zezina 1994). The most deep-sea species of recent brachiopods is P. atlanticus, whose empty shells were found at a depth of 7,460-7,600 meters in the Romanche Fracture Zone (Zezina 1994). This species is eurybathic with a range of depths for live specimens from 336-5,530 meters and is also the deepest among recent brachiopods (Zezina 1994; Emig 1997). On the marginal ridge of the Kuril-Kamchatka Trench, the density of this species is about 12 individuals per square meter (Zezina 1981). Stones of various diameters (Foster 1974), shells of brachiopods and molluscs (Cooper 1975), bones of whales and manganese nodules (Zezina 1981) can serve as a substrate for the attachment of this species in the deep sea.

    Deep-water conditions are unfavourable for brachiopods, leading to dwarfism, paedomorphosis, and homeomorphy (Zezina 2008; Bitner et al. 2013). Thus, the small size of the shell and the underdeveloped simple lophophore of P. atlanticus are interpreted as paedomorphic features (Zezina 2015), which is characteristic of the deep-sea brachiopod fauna (Zezina 1994, 2015; Bitner et al. 2013). A large number of mitochondria in the spermatozoon of P. atlanticus may also be considered as an adaptation for deep-water occurrence in this species since spermatozoon needs a lot of energy for external fertilization at extreme depths (Temereva and Kuzmina 2018).

    Acknowledgements

    This paper was part of the “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project (Beneficial project)”. Beneficial project (grant number 03F0780A) was funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany. This work was supported by a grant from the Russian Science Foundation (#18-14-00082). I would like to thank Hanieh Saeedi forcreating the distribution maps and to Rachel Downey for a language editing of the text.

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    • Zezina ON (2008) Biogeography of the Recent Brachiopod. Paleontological Journal 42(8): 830–858.
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    Chapter 5. ENTOPROCTA: A REVIEW ON THE BIOGEOGRAPHY OF THE DEEP-SEA ENTOPROCTA ALONG THE NW PACIFIC

    Faculty of Biology, Moscow State University, Moscow 119991, Russia
    Email: borisanovaao@mail.ru*

    1. Introduction

    Entoprocta , or Kamptozoa, is a phylum of invertebrate animals including about 200 species. Entoprocts are solitary or colonial animals living as epibionts of different animals (sponges, cnidarians, polychaetes, sipunculans, echiurids, bryozoans, echinoderms, and hemichordates) or as foulers of various substrates (stones, algae, mollusk shells, arthropod cuticle, tunic of ascidians) (Nielsen 1964, 2008, Soule and Soule 1965, Borisanova 2018). Two species of Entoprocta were found in fresh water (Leidy 1851, Wood 2005), all the others are marine animals. The majority of species live in the shelf zone, most often at shallow depths down to several tens of meters. Only one colonial species, Barentsia gracilis (Sars, 1835), and six solitary species of genus Loxosomella Mortensen, 1911 were described from the deep-sea floor (Borisanova 2018, Borisanova and Chernyshev 2019). All deep-sea Loxosomella species were described in recent years, and all of them were found in NW Pacific.

    2. Objectives

    This chapter represents a brief review of the biogeography of the deep-sea Entoprocta found during Russian-German deep-sea expeditions in the NW Pacific.

    3. Material and Methods

    Six deep-sea species of the genus Loxosomella (family Loxosomatidae Hincks, 1880) were found in the NW Pacific region during three German–Russian deep-sea expeditions (Map 1).

    Map 1.

    Distribution of Entoprocta species in the NW Pacific.

    Loxosomella profundorum Borisanova, Chernyshev, Neretina & Stupnikova, 2015, was collected during the German–Russian deep-sea expedition KuramBio aboard RV Sonne to the abyssal plain adjacent to the Kuril-Kamchatka Trench in the summer of 2012; Loxosomella marcusorum Borisanova, Chernyshev, 2019 was collected during the German–Russian deep-sea expedition KuramBio II aboard the RV Sonne to the Kuril-Kamchatka Trench region in August–September 2016; Loxosomella aeropsis Borisanova, Chernyshev & Ekimova, 2018, L. cyatiformis Borisanova, Chernyshev & Ekimova, 2018, L. malakhovi Borisanova, Chernyshev & Ekimova, 2018, L. sextentaculata Borisanova, Chernyshev & Ekimova, 2018 were collected during the German-Russian deep-sea expedition SokhoBio aboard RV Akademik Lavrentyev to the Kuril Basin of the Sea of Okhotsk, Bussol Strait, and the adjacent open Pacific abyssal area in July - August 2015. Five species were found in abyssal area (L. aeropsis, L. cyatiformis, L. malakhovi, L. profundorum, L. sextentaculata) at depths ranging from 3,206 to 5,223 m, one species in hadal zone at depth 6,202-6,204 m (L. marcusorum) (Table 1). The samples containing entoprocts were collected with a box corer (BC) (L. malakhovi) or dredged with a modified camera-epibenthic sledge (EBS) (L. cyatiformis, L. malakhovi, L. profundorum), and Agassiz trawl (AGT) (L. aeropsis, L. marcusorum, L. sextentaculata).

    List of deep-sea loxosomatid entoprocts from the NW Pacific.

    Species Point of species detection Coordinates Depth, (m) Locality Host species References
    Loxosomella profundorum 43.029667 N 152.976833 E 5,222–5,223 NW Pacific, east of the Kuril Islands Corallimorpharia Carlgren, 1943 Borisanova et al. 2015
    Loxosomella aeropsis 1 48.05 N 150.005 E 3,348 Kuril Basin, Sea of Okhotsk Aeropsis fulva (Agassiz, 1898) (Aeropsidae Lambert, 1896, Echinoidea) Borisanova et al. 2018
    2 46.261667 N 152.051667 E 3,580 Open Pacific abyssal area between the Bussol Strait and the Kuril-Kamchatka Trench.
    Loxosomella cyatiformis 1 45.588333 N 146.411667 E 3,206 Kuril Basin, Sea of Okhotsk Catillopecten squamiformis (Bernard, 1978) (Propeamussiidae Abbott, 1954, Bivalvia) Borisanova et al. 2018
    2 46.91 N 151.088333 E 3,296
    Loxosomella malakhovi 1 45.625 N 146.373333 E 3,216 Kuril Basin, Sea of Okhotsk Aglaophamus sp. (Nephtyidae Grube, 1850, Polychaeta) Borisanova et al. 2018
    2 46.91 N 151.088333 E 3,296
    3 46.95 N 151.083333 E 3,300
    4 48.09 N 150.026667 E 3,347
    5 47.203332 N 149.611666 E 3,366
    Loxosomella sextentaculata 48.05 N 150.005 E 3,348 Kuril Basin, Sea of Okhotsk Laonice sp. (Spionidae Grube, 1850, Polychaeta) Borisanova et al. 2018
    Loxosomella marcusorum 1 45.942883 N 152.904267 E 6,201.7 Kuril-Kamchatka Trench Thalassema sp. (Thallassematidae Forbes & Goodsir, 1841 (Echiura) Borisanova and Chernyshev 2019
    2 45.943117 N 152.904183 E 6,203.9

    All species were fixed in 95% ethanol (for light microscopy, scanning electron microscopy, and for molecular analyses). Several specimens of two species (L. aeropsis, L. malakhovi) were also fixed in 4% paraformaldehyde solution in 0.1 M phosphate-buffered saline (for confocal laser scanning microscopy).

    4. Results

    The brief descriptions of the deep-sea entoproct species of the NW Pacific are given below. The main morphological characteristics are listed in Table 2.

    Main morphological characteristics of deep-sea Entoprocta.

    Species Average body length, μm Tentacle number Sensitive papilla Shape of stomach Foot Budding area
    Loxosomella cyatiformis 498 14 One unpaired triangular No latero-frontal, lower level of stomach
    Loxosomella malakhovi 190 8 No roundish No; stalk ends with concaved disk frontal, middle level of stomach
    Loxosomella sextentaculata 834 6 No roundish Present latero-frontal, upper level of stomach
    Loxosomella aeropsis 558 9-10 No roundish or slightly triangular No latero-frontal, middle level of stomach
    Loxosomella profundorum 3,200 10-12 1 pair heart-shaped No latero-frontal, upper level of stomach
    Loxosomella marcusorum 596 10-12 No roundish-triangular No; stalk ends with star-shape plate latero-frontal, bottom of stomach

    Loxosomella cyatiformis Borisanova, Chernyshev, Ekimova, 2018

    (Figure 1A)

    Figure 1.

    Deep-sea entoprocts of the NW Pacific. (A) Loxosomella cyatiformes, lateral view, (B, C) Loxosomella malakhovi: (B) two specimens on a gill of parapodia, (C) specimen with a bud, lateral view, (D) Loxosomella sextentaculata, frontal view, (E, F) Loxosomella aeropsis: (E) two specimens on a spine of sea urchin, (F) lateral view of specimen, (G, H) Loxosomella profundorum: (G) frontal view of specimen, (H) lateral view of calyx with a bud, (I) Loxosomella marcusorum, lateral view. Abbreviations: b, bud; e, embryo; f, foot; g, gill of parapodia; ht, host tissue; pl, star-shaped plate; sp, spine of sea urchin; st, stalk; t, tentacles. Scale bars: (A, B, D–I) 200 µm, (C) 100 µm.

    Loxosomella cyatiformis was found in the Kuril Basin of the Sea of Okhotsk, at depths 3,206 m and 3,296 m. Specimens were found living on scallop valves. L. cyatiformis is a medium-sized species. The total body length is from 383 μm to 596 μm. The stalk is longer than the calyx. Foot is absent in adults. Calyx bears 14 tentacles. One unpaired papilla is present on the abfrontal side of calyx. Stomach is triangular. Buds originate from the latero-frontal areas located at the lower level of the stomach. Full-developed buds with a conspicuous foot. Species was collected in late July-early August 2015, and some specimens were found with developing embryos, up to seven embryos in the calyx.

    Loxosomella malakhovi Borisanova, Chernyshev, Ekimova, 2018

    (Figure 1B, 1C)

    Loxosomella malakhovi was found in the Kuril Basin of the Sea of Okhotsk, at depths 3,216–3,366 m. Specimens were attached to the gills of parapodia of nephtyid polychaetes. L. malakhovi is a small-sized species. The total body length is from 160 μm to 225 μm. The stalk is very short. Foot is reduced, and the stalk is ended with a roundish concaved disk which grasps part of the host tissue. The calyx bears eight tentacles. Sensitive papillae are not found. The stomach is roundish. Buds originate from the frontal area located at the middle level of the stomach. Full-developed buds with a prominent foot. Specimens were collected from mid-July to early August 2015, and many specimens were found with developing embryos, usually with two large embryos in the calyx.

    Loxosomella sextentaculata Borisanova, Chernyshev, Ekimova, 2018

    (Figure 1D)

    Loxosomella sextentaculata was found in the Kuril Basin of the Sea of Okhotsk, at a depth of 3,348 m. Specimens were found attached to parapodia of spionid polychaetes. L. sextentaculata is a large-sized species. The total body length is from 705 µm to 938 µm. The stalk is long, and ends with a large foot. Calyx bears six tentacles. Sensitive papillae are not found. The stomach is roundish. Buds originate from the latero-frontal areas located at the upper level of the stomach. Full-developed buds were not observed. Species was collected in late July 2015, and no embryos were observed.

    Loxosomella aeropsis Borisanova, Chernyshev, Ekimova, 2018

    (Figure 1E, 1F)

    Specimens of Loxosomella aeropsis were collected in the Kuril Basin of the Sea of Okhotsk at a depth of 3,348 m and in open Pacific abyssal area between the Bussol Strait and the Kuril-Kamchatka Trench at a depth of 3,580 m. Specimens were found living attached to the anterior spines of sea urchins. L. aeropsis is a medium-sized species. Total body length is from 417 µm to 925 µm, the stalk is longer than the calyx. The foot is absent in adults. Calyx bears 10 or, more rarely, nine tentacles. Sensitive papillae are not found. The stomach is roundish or slightly triangular. Buds originate from the latero-frontal areas located at the middle level of stomach. Full-developed buds bear eight tentacles and have a short foot. Species was collected in late July 2015, and no embryos were observed in the calyxes of any specimens.

    Loxosomella profundorum Borisanova, Chernyshev, Neretina & Stupnikova, 2015

    (Figure 1G, 1H)

    Loxosomella profundorum was found in the abyssal plain adjacent to the Kuril-Kamchatka Trench, at depths of 5,222–5,223 m. Specimens were attached to the oral disc of the corallimorpharian polyp. L. profundorum is one of the largest species among entoprocts. The total body length is from 1.3 mm to 4 mm, the stalk is long, up to 3.5 mm. Foot is reduced in adults. Calyx bears 10–12 tentacles. One pair of sensitive papillae is present. Stomach is heart-shaped. Buds originate from the latero-frontal areas located at the upper level of the stomach. Full-developed buds were not observed. Species was collected in mid-August 2012, and no embryos were observed.

    Loxosomella marcusorum Borisanova, Chernyshev, 2019

    (Figure 1I)

    Loxosomella marcusorum was found in the Kuril-Kamchatka Trench, in the hadal zone, at depths of 6,202-6,204 m. L. marcusorum is an epibiont of echiurids. It is a medium-sized species. Total body length is from 449 µm to 685 µm, the stalk is shorter than the calyx. Foot is absent, the stalk is ended with an expanded star-shaped plate immersed in the host body. Calyx bears 10–12 tentacles. Sensitive papillae were not found. Stomach is roundish-triangular. Buds originate from the latero-frontal areas located at lower level of stomach. Full-developed buds were not observed. The species was collected in late August 2016, and many specimens had embryos developing in the calyx, usually with four embryos at a time.

    5. Discussion

    Eight new species of Entoprocta were found in the NW Pacific region during three deep-sea expeditions in recent years: Loxosomella aeropsis, L. cyatiformis, L. malakhovi, L. marcusorum, L. profundorum, L. sextentaculata, and two species, that have not yet been described (one species is an epibiont of polychaetes from the family Scalibregmatidae Malmgren, 1867, another species is associated with Sipuncula (Borisanova et al. 2018)). The discovery of eight new species in three expeditions suggests that the biodiversity of Entoprocta in the abyssal and hadal zone may be quite high in this region, and future investigations will contribute to our knowledge of the deep-sea entoproct species diversity.

    Deep-sea Entoprocta are associated with different deep-sea animals, including those that are not characteristic for shallow-water entoproct species: corallimorpharians, sea urchins, and bivalve molluscs. The new symbiotic associations in the abyssal zone could have evolved due to the shortage of firm substrata and the low density of benthic animals, which results in an extremely limited choice of available hosts for epibiotic species. Although five species (Loxosomella malakhovi, L. marcusorum, L. sextentaculata, and two undescribed Loxosomella species) were found in association with annelids, the most typical hosts for Entoprocta (Nielsen 1964, Borisanova 2018).

    Molecular genetics analysis of four species of deep-sea Entoprocta indicates that these species are not close to each other and cluster with different species of shallow-water entoprocts from different habitats. L. cyatiformis forms a single clade with L. vancouverensis Rundell & Leander, 2012 from the western coast of the Pacific Ocean (Vancouver Island in British Columbia, Canada). L. malakhovi clustered together with L. varians Nielsen, 1964 which was found in the Atlantic Ocean, and L. murmanica (Nilus, 1909) which was found in the Atlantic, Antarctic and Arctic Ocean, but not in the Pacific (Nielsen 1989, Emschermann 1993). L. aeropsis forms a sister clade to L. malakhovi, L. murmanica, and L. varians. L. profundorum is genetically different from all solitary entoproct species and forms a sister clade to all Loxosomatidae.

    Acknowledgements

    This paper was part of the “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project (Beneficial project)”. Beneficial project (grant number 03F0780A) was funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany. The author is deeply thankful to Hanieh Saeedi for her help with the preparing of the manuscript. The author is grateful to Rachel Downey for reviewing and English proofreading this chapter. This work was financially supported by the Russian Science Foundation (grant 18–14–00082) and Moscow State University Grant for Leading Scientific Schools “Depository of the Living Systems” in frame of the MSU Development Program.

    References

    • Borisanova AO (2018) Entoprocta (Kamptozoa). In: Schmidt-Rhaesa A, ed, Handbook of Zoology. Miscellaneous Invertebrates. De Gruyter, Berlin, Boston, 111–162.
    • Borisanova AO, Chernyshev AV (2019) A new loxosomatid species from the Kuril-Kamchatka trench area: Loxosomella marcusorum sp. n., the first record of hadal Entoprocta. Progress in Oceanography 178: 102146.
    • Borisanova AO, Chernyshev AV, Ekimova IA (2018) Deep-sea Entoprocta from the Sea of Okhotsk and the adjacent open Pacific abyssal area: new species and new taxa of host animals. Deep Sea Research Part II: Topical Studies in Oceanography: 87–98.
    • Borisanova AO, Chernyshev AV, Neretina TV, Stupnikova AN (2015) Description and phylogenetic position of the first abyssal solitary kamptozoan species from the Kuril-Kamchatka trench area: Loxosomella profundorum sp. nov. (Kamptozoa: Loxosomatidae). Deep-Sea Research Part II: Topical Studies in Oceanography 111: 351–356.
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    • Nielsen C (2008) A review of the solitary entoprocts reported from sponges from Napoli (Italy), with designation of a neotype of Loxosoma pes Schmidt, 1878. Journal of Natural History 42: 1573–1579.
    • Rundell RJ, Leander BS (2012) Description and phylogenetic position of the first sand-dwelling entoproct from the western coast of North America: Loxosomella vancouverensis sp. nov. Marine Biology Research 8: 284–291.
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    CHAPTER 6. NEMERTEA: A REVIEW ON DEEP-SEA BENTHIC NEMERTEANS ALONG THE NW PACIFIC

    A.V. Zhirmunsky National Scientific Center of Marine Biology, Far East Branch of the Russian Academy of Sciences, Vladivostok, Russia
    Email: chernyshev.av@dvfu.ru*

    1. Introduction

    Nemertea is a phylum of the invertebrates known as nemerteans, or ribbon worms, which includes about 1300 valid species (Kajihara et al. 2008). These worms are found from the supralittoral to the abyssal zone on different bottoms, including silt, sand, algae, sponges, and dead corrals. Nemerteans are predators and scavengers feeding on small crustaceans, annelids, and molluscs. About 50 species are symbionts of decapods, barnacles, bivalve mollusks, ascidians, star-fishes, sea urchins, sea anemones, and echiurids. Most of the bathypelagic nemerteans (about 100 species) known to date are commonly found within a depth range of a few hundred to a few thousand meters, reaching their highest abundance at 600–3,000 m. To date, 22 species of fresh-water nemerteans and 13 species of land nemerteans living have been described (Gibson 1995; Sundberg and Gibson 2008).

    Available information on deep-sea benthic nemerteans is even less compared to the shallower waters. By 2013, only seven of the described species of benthic nemerteans have been collected from depths exceeding 2,000 m, with none truly abyssal among them. In the last five years, we have had the opportunity to create a diverse and abundant collection of benthic nemerteans from abyssal and hadal depths. The data obtained indicate a high species diversity of benthic nemerteans inhabiting depths greater than 3,000 m. Nine species of the abyssal, pseudoabyssal and hadal nemerteans have been described quite recently (Chernyshev 2013; Chernyshev et al. 2015; Chernyshev and Polyakova 2018a; Chernyshev and Polyakova 2018b, Chernyshev and Polyakova 2019).

    2. Objectives

    The present chapter summarizes published data on deep-sea benthic nemerteans found during four Russian-German deep-sea expeditions in the NW Pacific.

    3. Material and Methods

    During four Russian-German deep-sea expeditions (SoJaBio 2010, KuramBioI 2012, SokhoBio 2015, and KuramBioII 2016) benthic nemerteans were collected at depths from 470 to 9,577 m. Specimens were sampled using a camera epibenthic sledge (EBS), Agassiz trawl (AGT), and giant box-corer (BK). We divided the collected nemerteans into two groups. The first one included nemerteans studied live and fixed for both morphological (in 4% paraform) and genetic (in 96% ethanol) analyses. Due to the rapid technique for examination of the internal structure using confocal laser scanning microscopy, the taxonomic affiliation of these nemerteans was determined, and some specimens were identified to the genus or species level. However, these nemerteans in each sample were represented by one, rarely two specimens. The second group includes individuals collected using EBS and fixed in chilled (−20°C) 96% ethanol and kept in a −20°C freezer. They are of little use for morphological studies, and thus their systematic position has not been determined as accurately as for individuals studied live.

    Deep-sea benthic nemerteans are frequently found damaged in hydrobiological samples: in most cases, with the epidermis and the posterior or anterior parts of the body missing, making them unsuitable for description. Most of collected specimens could be identified down to the family or order level only. Animals collected using EBS are best preserved for genetic studies (Chernyshev and Polyakova 2018a), but a quick fixation in cold 95% ethanol makes specimen less suitable for histological studies; a fixation in formol does not allow genetic analysis of material. The optimum way is fixation of a largest portion of living nemertean’s body in 4% formalin for morphological investigation and a small portion in 95% ethanol for genetic studies. This approach was applied in description of the first abyssal heteronemertean Sonnenemertes cantelli (Chernyshev et al. 2015).

    4. Results

    In samples from the abyssal and hadal zones, a vast majority of nemerteans belonged to four groups: (1) carininid palaeonemerteans (Carininidae); (2) tubulanid palaeonemerteans (Tubulanidae s. str.); (3) heteronemerteans; (4) eumonostiliferous hoplonemerteans. Archinemerteans (cephalotrichid palaeonemerteans) and reptantian hoplonemerteans occurred much more rarely; carinomid palaeonemerteans and cratenemertid hoplonemerteans were not found in the samples from the abyssal and hadal zones (Chernyshev 2013, 2015; Chernyshev and Polyakova 2018a, Chernyshev and Polyakova 2018b, 2019; Chernyshev et al. 2015) (Figure 1 and Map 1). Deep-sea palaeonemerteans are represented by new species from known genera (Carinina, Cephalothrix, and Tubulanus s.l.).

    Figure 1.

    NW Pacific nemerteans. (A) Cephalothrix iwatai; (B) Sonnenemertes cantelli; (C) Proamphiporus crandalli.

    Map 1.

    Distribution of NW Pacific nemertean species.

    All deep-sea Carinina collected in the NW Pacific form a highly supported clade, which is sister group to a clade of the shallow-water species (Chernyshev and Polyakova 2019). The most basal position in this clade is occupied by Carininidae KuramBio II 103, collected in the Kuril-Kamchatka Trench at a depth of 9,301 m. A preliminary study of the internal structure of some of the hadal carininids showed their structure typical of Carininidae: they had intraepidermal lateral nerve cords, well-developed inner circular musculature of the body wall, rhynchocoel wall with thick circular muscle layer, and inner position of the lateral blood vessels. A distinguishing feature of the collected deep-sea Carinina (except for Carininidae KuramBio II 103) is that they had relatively large body sizes (with the length of the anterior fragment of the body being 4–5 cm; the total body length was apparently 1.5–2 times larger). It should specially be noted that, according to DNA analysis, the specimens collected at the hadal stations, did not belong to the same species as those collected at abyssal depths in the Kuril-Kamchatka Trench, near the Kuril Islands, and from the abyssal plain near the Kuril-Kamchatka Trench.

    Cephalothrix iwatai Chernyshev, 2013 (Figure 1a) is a single known deep-sea archinemertean and obviously common species in depth of 1,500–3,300 m in the Sea of Japan (Chernyshev 2013). Most nemerteans of genus Cephalothrix occur in the intertidal zone; whereas, only few have been found in depths from 20 to 40 m. In the Sea of Japan, several shallow-water Cephalothrix species have been recorded, but they all differ from C. iwatai and do not live in soft bottoms. Other deep-sea species for the Sea of Japan, Micrura bathyalis Chernyshev, 2013 from depths 2,670–3,426 m, is closely related to the sublittoral Cerebratulus species. The lack of typical abyssal species of nemerteans in the deep Sea of Japan is connected with isolation of this basin from the Pacific abyssal depths.

    Basal heteronemertean Sonnenemertes cantelli Chernyshev, Abukawa & Kajihara, 2015 (Figure 1b) was collected in samples from four stations in the Sea of Okhotsk and on both sides of the Kuril-Kamchatka Trench. Sonnenemertes cantelli has not been found in samples from depths shallower than 3,000 m and deeper than 6,000 m. For this reason, the species can be considered a marker of abyssal fauna. Our records of S. cantelli, originally described from a single abyssal station adjacent to the Kuril-Kamchatka Trench (Chernyshev et al. 2015) and reported from the Sea of Okhotsk (Chernyshev and Polyakova 2018b), further support relationships between the abyssal fauna of the Kuril Basin and parts of the NW Pacific fauna via straits between the Kuril Islands. Sonnenemertes cantelli apparently feeds on small sipunculid worms (Chernyshev and Polyakova 2018b).

    Abyssal Proamphiporus crandalli Chernyshev & Polyakova, 2019 (Figure 1c) found in the Kuril-Kamchatka Trench from depth of 5,496 m is very similar in external traits and internal morphology to Amphiporus rectangulus Strand et al., 2014, described from the coastal waters of Norway from a depth of 220 m. Deep-sea benthic nemerteans do not have any specific color pattern, and live worms are unicoloured: mostly in whitish, pinkish, yellowish or, rarely, reddish tones. It is noteworthy that P. crandalli is the only abyssal nemertean with specific color pattern on the head, much resembling that in A. rectangulus.

    Uniporus alisae Chernyshev & Polyakova, 2018 collected in the Sea of Okhotsk from depth of 3,301 m is morphologically close to Uniporus hyalinus Brinkmann, 1914–1915 described from the bathyal (depth 1,000–1,200 m) of the Norwegian Sea. Externally both species are very similar and have gelatinous translucent body.

    The Nemertovema is a single known hadal genus with two described species: Nevertovema hadalis Chernyshev & Polyakova, 2018, collected in the Puerto Rico Trench from a depth of 8336–8,339 m (Chernyshev and Polyakova 2018a), and Nemertovema norenburgi Chernyshev & Polyakova, 2019, found in the Kuril-Kamchatka Trench from depths of 8,220 and 8,271 m (Chernyshev and Polyakova 2019). The pairwise COI-gene sequence distances between N. hadalis and N. norenburgi are 8.1–8.5%, which seems unusual because of the huge geographic gap between the Puerto Rico Trench and the NW Pacific localities. For comparison, the p-distances between COI-gene sequences of the sympatric cryptic species of the shallow water nemerteans are 8–14%.

    Galathenemertes giribeti Chernyshev & Polyakova, 2019, found in the tube of sea anemone Galatheanthemum sp. in the Kuril-Kamchatka Trench from depth of 7,256 m, is the deepest known symbiotic nemertean and the second known species associated with Actinia. This species is closely related to ascidian-associated nemertean Gononemertes parasita Bergendal, 1900 (Chernyshev and Polyakova 2019). Deep-sea symbiotic nemerteans comprise species from the genera Ovicides and Gononemertes s.l. At least four undescribed species of Gononemertes-like nemerteans have been obtained from the peribranchial cavity of deep-sea carnivorous ascidians of the genus Culeolus (Herdman, 1881): (1) “Gononemertes” sp.1 from Culeolus nadejdi found in the Sea of Okhotsk (depth 1,040–1,050 m) (Sanamyan 1992); (2) “Gononemertes” sp. 2 from Culeolus sp. found in the abyssal plain adjacent to the Kuril–Kamchatka Trench (depth 4,869 m) (Chernyshev et al. 2015); (3) “Gononemertes” sp. 3 from Culeolus sp. found in the Kuril Basin of the Sea of Okhotsk (depths 3,301-3,347 m) (Chernyshev and Polyakova 2018b); (4) “Gononemertes” sp. 4 from Culeolus barryi, off the coast of California (depth 1,200 m) (Sanamyan et al. 2018). The phylogenetic analysis has confirmed the previously stated assumption that deep-sea Gononemertes-like nemerteans associated with Culeolus cannot be attributed to the genus Gononemertes with the type species G. parasita associated with the shallow-water ascidian Phallusia (Chernyshev and Polyakova 2018b).

    5. Discussion

    The taxonomic diversity of the abyssal and hadal nemerteans is quite high, though sequences have been obtained for less than a third of the species collected during deep-sea expeditions in the NW Pacific. Of particular interest is the finding of genetically close species (Nemertovema hadalis and N. norenburgi) in the Puerto Rico and Kuril-Kamchatka Trenches, which may indicate the relationships in the hadal nemertean fauna from different regions of the World Ocean. Among the deep-sea heteronemerteans and hoplonemerteans, species that could not be assigned to any of the known genera seem to be predominant. The genetic and morphological similarity between Amphiporus rectangulus and Proamphiporus crandalli is the first proven case of close phylogenetic relationships between sublittoral and real abyssal nemertean species (Chernyshev and Polyakova 2019).

    The species diversity of nemerteans in the samples from the abyssal zone is usually quite high (about 50–60 species in the NW Pacific Ocean); however, in the Sea of Japan only two nemertean species, Cephalothrix iwatai (Chernyshev, 2013) and Micrura bathyalis, were found at a depth of over 3 km. With the rare exceptions, abyssal and hadal nemerteans are genetically well distinguished from shallow-water species. The p-distances between the COI sequences of the C. iwatai and shallow-water Cephalothrix sp. 4 TCH-2015 from northeast Pacific are 6.4–6.5%, indicating their close relationship. Accordingly, this fact indicates that C. iwatai is a ‘young’ eurybathic species.

    Another interesting finding of our research was the different species compositions of nemerteans in the abyssal and hadal zones of the Kuril-Kamchatka Trench and adjacent abyssal depths. Moreover, we found no species present in the samples from both the abyssal and bathyal zones. The exceptions were Cephalothrix iwatai and Micrura bathyalis, but it should be taken into account that both species live in the Sea of Japan, which lacks real abyssal fauna (Andriashev 1979). Apparently, among nemerteans eurybathic species with a wide range of habitat depths are not as common. There is no doubt that the abyssal and hadal zones of the World Oceans are inhabited by a large number of species and genera of nemerteans new to science.

    Acknowledgements

    This paper was part of the “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project (Beneficial project)”. Beneficial project (grant number 03F0780A) was funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany. I am grateful to Hanieh Saeedi for help with the map and the English proofread.

    References

    • Andriashev AP (1979) About some questions of the marine bottom fauna vertical zonations. In Studenetskiy SA (Ed.), Biological Resources of the World Ocean. Nauka, Moscow: 17–138.
    • Chernyshev AV (2013) Two new species of deep-sea nemerteans from the SoJaBio expedition in the Sea of Japn. Deep Sea Research II 86–87: 148–155.
    • Chernyshev AV, Abukawa S, Kajihara H (2015) Sonnenemertes cantelli gen. et sp. nov. (Heteronemertea)—A new Oxypolella-like nemertean from the abyssal plain adjacent to the Kuril–Kamchatka Trench. Deep Sea Research II 111: 119–127.
    • Chernyshev AV, Polyakova NE (2018a) Nemerteans of the Vema-TRANSIT expedition: First data on diversity with description of two new genera and species. Deep Sea Research II 148: 64–73.
    • Chernyshev AV, Polyakova NE (2018b) Nemerteans from deep-sea expedition SokhoBio with description of Uniporus alisae sp. nov. (Hoplonemertea: Reptantia s.l.) from the Sea of Okhotsk. Deep-Sea Research II 154: 121–139.
    • Chernyshev AV, Polyakova NE (2019) Nemerteans from the deep-sea expedition KuramBio II with descriptions of three new hoplonemerteans from the Kuril-Kamchatka Trench. Progress in Oceanography 178. https://doi.org/ 10.1016/j.pocean.2019.102148
    • Gibson R (1995) Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution. Journal of Natural History 29(2): 271–561.
    • Kajihara H, Chernyshev AV, Sun S-C, Sundberg P, Crandall FB (2008) Checklist of nemertean genera and species published between 1995 and 2007. Species Diversity 13: 45–274.
    • Sanamyan K (1992) Ascidians from the Sea of Okhotsk collected by R.V. Novoulyanovsk. Ophelia 36: 187–197.
    • Sanamyan K, Sanamyan N, Kuhnz L (2018) A new Culeolus species (Ascidiacea) from the NE Pacific, California. Zootaxa 4420(2): 270–278.
    • Sundberg P, Gibson R (2008) Global diversity of nemerteans (Nemertea) in freshwater. Hydrobiologia 595: 61–66.

    Chapter 7. SOLENOGASTRES: DIVERSITY AND DISTRIBUTION OF SOLNOGASTRES (MOLLUSCA) ALONG THE NW PACIFIC

    aLudwig-Maximilians-Universität (LMU Munich), Department II Biologie, Großhaderner Str. 2, 82152 Planegg-Martinsried, Germany.
    bSNSB-Zoologische Staatssammlung München (ZSM), Section Mollusca, Münchhausenstraße 21, 81247 München, Germany
    Email: franzi.bergmeier@googlemail.com*

    1. Introduction

    Solenogastres (= Neomeniomorpha) are exclusively marine, vermiform molluscs. Together with Caudofoveata (= Chaetodermomorpha), they form the clade Aplacophora, a name referring to their body, which lacks a shell. Solenogastres is a comparatively species poor and understudied class of Mollusca with currently 293 described species organized in 24 families and four orders. Most Solenogastres are minute and reach only a few millimeters in body length and are thus usually collected with sampling gear designed for benthic meiofauna (only few giant species reach exceptional body lengths of up to 30 cm, and can be retrieved through macrobenthic sampling).

    In Solenogastres, the molluscan foot is reduced to a narrow ciliary gliding sole, usually visible as a fine median line running along the ventral side of the animal and they lack a head shield (both characters help to distinguish them from equally worm-shaped Caudofoveates). Aragonitic sclerites protrude from the chitinous cuticle surrounding the entire body. These sclerites (comprising the so-called scleritome) are highly diverse, ranging from solid or hollow needles to solid scale-like elements. Depending on the composition of the scleritome, Solenogastres often appear smooth and shiny, shaggy, or very spiny. Together with the organization and histology of the digestive and reproductive system, the scleritome serves as one of the main taxonomic characters required to differentiate and identify solenogaster species. Most scientific work conducted on this group focuses on traditional taxonomy, but recent phylogenomic studies have begun investigating internal evolutionary relationships and rendered several parts of the current classificatory system (i.e. the order Cavibelonia Salvini-Plawen, 1978) paraphyletic (Kocot et al. 2019). Solenogastres systematics will thus likely receive major revisions in the near future.

    1.1. Biology and Ecology

    Solenogastres are commonly found among benthic fauna, even though they are seldom encountered in high individual numbers. They prey on marine invertebrates, mainly cnidarians (preferably hydrozoans) and polychaetes.

    Little is known about the biology and ecology of Solenogastres, and observations are restricted to a few well-studied taxa. They are hermaphrodites and after copulation most species are assumed to deposit small batches of fertilized eggs from which lecitotrophic swimming larvae hatch (Todt and Wanninger 2010). A few species of Solenogastres brood and retain the encapsulated larvae within their pallial cavity until juveniles emerge, altogether suggesting limited dispersal abilities (Todt and Kocot 2014).

    1.2. Habitat

    Solenogastres inhabit a wide range of sediments from coarse shell gravel and volcanic sands to fine, silty sediments. Several species have been found living epizoically on cnidarians (Figure 1) or in association with sponges (Kocot et al. 2019).

    Figure 1.

    Dondersiidae sp. SB-2 (Pholidoskepia), from the Kuril Basin of the Sea of Okhotsk. Found wrapped around a cnidarian. Head to the right. Scale bar: 1 mm.

    While a few species can be collected in knee-deep waters of the shallow intertidal zone, the lower continental shelf is currently assumed to harbor the highest species diversity (Todt 2013). The solenogaster fauna of the world’s vast abyssal plains and the hadal zone of oceanic trenches still remain largely unexplored.

    1.3. Geographical Distribution

    Solenogastres are known from all oceans, sampled from the Arctic to the Antarctic. Most taxonomic work has focused on historical samples from Antarctica (see monographs by Salvini-Plawen 1978a; 1978b) and the North Atlantic along the western European coast, thus the majority of species has been described from these regions. To date, out of 293 recognized solenogaster species on a global-scale, 56 species are known from the entire Pacific Ocean and only 17 have been recorded from the NW Pacific. They occur mostly in the shallow bathyal around the Japanese coast (11 species, 27-600 m), the Sea of Japan (one species, 200-600 m), the Sea of Okhotsk (2 species, 200-400 m), and the Bering Sea (1 species, 880 m) (García-Álvarez and Salvini-Plawen 2007; Sirenko 2013).

    2. Objectives

    The present chapter aims to compile the current knowledge on the diversity and distribution of Solenogastres in the investigated area of the NW Pacific, recorded from the deep sea below 2,000 m. Based on this data, we explore putative patterns of species richness and distribution comparing the open NW Pacific and the semi-isolated adjacent Sea of Okhotsk.

    3. Material and Methods

    3.1. Coverage Area

    The KuramBio I and II (Kuril-Kamchatka Biodiversity Studies I and II, see Brandt et al. 2015, 2020) and SokhoBio (Sea of Okhotsk Biodiversity Studies, Brandt et al. 2018) Expeditions between 2012 and 2016 explored the benthic deep-sea fauna of the open NW Pacific and its adjacent regions. Solenogastres were collected during these expeditions using Agassiz trawls and epibenthic sledges. Overall, the investigated area ranges from 120-180°E and 40-60°N. It partially covers the open NW Pacific abyssal plain and the semi-isolated Kuril Basin of the Sea of Okhotsk, which is connected to the open NW Pacific via two deep straits. East of the Kuril Islands, the Kuril-Kamchatka Trench extends southwards reaching hadal depths of almost 9,600 m.

    3.2. Depth Gradient

    We have compiled data on Solenogastres occurring in the coverage area from bathyal (2,000-3,000 m), upper (3,000-4,000 m) and lower abyssal (4,000-6,000 m), and hadal depths (6,000 m and below).

    3.3. Latitudinal Gradient

    This chapter covers the deep-sea Solenogastres found in the temperate open NW Pacific and the Sea of Okhotsk with a latitudinal gradient of 40-60°N. Sampling sites correspond to the stations investigated during the recent KuramBio I (2012) and II (2016) (Brandt et al. 2015, 2020) and the SokhoBio (2015) (Brandt et al. 2018) expeditions.

    4. Results

    4.1. Richness Patterns

    Prior to this recent expedition series to the deep NW Pacific no Solenogastres were described from the investigated area of the NW Pacific below 2,000 m. However, these expeditions revealed a unique solenogaster diversity: 66 candidate species were collected between the Kuril Basin of the Sea of Okhotsk, the open NW Pacific Plain, and the Japanese and Kuril-Kamchatka Trench, spanning a depth range from 3,000 to more than 9,500 m (see Bergmeier et al. 2017, 2019; Ostermair et al. 2018).

    Following the currently recognized classificatory system of Solenogastres (García-Álvarez and Salvini-Plawen 2007), these 66 species cover all four traditional solenogaster orders and represent at least 10 families (see the Species Check-List in Chapter 1, Table 1). The two orders Cavibelonia Salvini-Plawen, 1978 and Pholidoskepia Salvini-Plawen, 1978 constitute in mostly equal parts for 98% of all collected Solenogastres in the area, and are both distributed from the upper abyssal down to the hadal zone. These two most common groups can be usually differentiated directly in the field under a stereomicroscope, as Cavibelonia are in general characterized by a spinier and rough appearance due to a scleritome largely composed of needle shaped elements, whereas Pholidoskepia are rather smooth and shiny, predominantly covered in scale-like elements).

    Species numbers (on familial level) in the investigated Northwest Pacific regions.

    Family Kuril Basin, Sea of Okhotsk (ca. 3,300 m) Slopes and bottom of the Kuril-Kamchatka-Trench (ca. 5,200-9,577 m) Open Northwest Pacific (abyssal plain) (ca. 4,800-5,400 m)
    Acanthomeniidae 2 4 8
    Amphimeniidae - 2 -
    Proneomeniidae 1 - 2
    Pruvotinidae 1 2 6
    Simrothiellidae 1 2 12
    Dondersiidae 4 4 6
    Gymnomeniidae 1 - 3
    Macellomeniidae - - 1
    Neomeniidae - - 1
    Phyllomeniidae - - 1

    The five cavibelonian families are represented by 44 species, and while species of Acanthomeniidae, Amphimeniidae, Pruvotinidae, and Simrothiellidae all have been reported from the abyssal zone before (in the Atlantic, Indian, South Pacific and Southern Ocean), abyssal Proneomeniidae are currently only known from the NW Pacific (Map 1). Three families of Pholidoskepia (20 species) are present in the investigated regions and are among the first records of this order below 2,500 m (Map 2), apart for a single dondersiid species from the abyssal Atlantic (Cobo et al. 2020).

    Map 1.

    Records of cavibelonian solenogaster families (Acanthomeniidae, Amphimeniidae, Pruvotinidae, and Simrothiellidae) in the Northwest Pacific.

    Map 2.

    Records of pholidoskepian (Dondersiidae, Gymnomeniidae, Macellomeniidae), neomeniomorph (Neomeniidae), and sterrofustian (Phyllomeniidae) solenogaster families.

    The remaining orders Neomeniamorpha and Sterrofustia are both rare and only account for one (Neomeniamorpha) and two (Sterrofustia) species, and while neomeniamorph Solenogastres are known from the bathyal NW Pacific, Sterrofustia have only been found once outside of the Southern Ocean before.

    Species diversity varies along a depth gradient: 15 species are present in the upper abyss (3,000-4,000 m), 43 species in the lower abyssal (4,000-6,000 m), and 11 species in the hadal zone (6,000-9,577 m). Most of the upper abyssal species are recorded at around 3,300 m throughout the Kuril Basin in the Sea of Okhotsk (12 species) and the Bussol Strait (3 species) between the Sea of Okhotsk and the open sea (Table 1, Map 3 and 4). Nevertheless, the lower diversity of Solenogastres in the semi-isolated Kuril Basin when compared to the open NW Pacific plain might be a result of oxygen-depleted bottom waters, formed during interglacial periods (Liu et al. 2006). 41 species are currently known from the open NW Pacific and its abyssal plain, while the slopes of the Kuril-Kamchatka Trench harbor nine species (5,200-7,200 m). Overall six species were sampled at four localities along the bottom of the trench, for the first time demonstrating the presence of Solenogastres in the hadal zone of oceanic trenches.

    Map 3.

    Distribution of dondersiid species recorded at three or more localities in the Sea of Okhotsk.

    Map 4.

    Distribution of pholidoskepian (Gymnomeniidae sp.SB-2) and cavibelonian solenogaster species recorded at three or more localities in the Northwest Pacific.

    4.2. Biogeographic Patterns

    Overall, the known solenogaster fauna of the abyssal and hadal zone of the NW Pacific is characterized by a high rate of singletons (i.e. species collected as single individuals only). Currently, within the investigated region, 45 out 66 species are collected only as singletons, and eight additional species were found only at a single location. This suggests that they might generally occur at low densities and/or with patchy distribution and consequently render potential hypotheses on their biogeographic and bathymetric distributions difficult based on the current state of knowledge.

    Out of 10 families, four (Acanthomeniidae, Pruvotinidae, Simrothiellidae, Dondersiidae) are widely distributed across the Sea of Okhotsk, the Kuril-Kamchatka Trench and the open NW Pacific. Two families (Proneomeniidae, Gymnomeniidae) are present on both sides of the Kuril-Kamchatka Trench (albeit not recorded from the slopes or bottom), and four have only been recorded with restricted distribution, e.g. the large-sized Amphimeniidae (Figure 2) are currently only known from the lower slope and bottom of the Kuril-Kamchatka Trench (Table 1, Map 1 and 2).

    Figure 2.

    A large-sized Amphimeniidae sp.2 (Cavibelonia), found between 7,100 and 8,200 m at the bottom of the Kuril-Kamchatka Trench. Head to the left. Scale bar: 1 cm.

    In the Sea of Okhotsk, 55% of the species are comparatively common, i.e. present at three or more localities (Map 3 and 4). Dondersiidae sp. SB-4 (Figure 3) is one of three common dondersiid species in the Kuril Basin (Map 3), and accounts for 40% of the local solenogaster fauna. The families Acanthomeniidae, Gymnomeniidae, and Simrothiellidae are each represented by single species, albeit collected at several locations within the Kuril Basin (Map 4). 98% of species from the NW Pacific abyssal plain are highly restricted in their occurrence, and only a single species (Pruvotinidae sp.KBI-2) was found at three different localities, all in close vicinity (Map 4).

    Figure 3.

    Dondersiidae sp.SB-4 (Pholidoskepia), a common species found in the Sea of Okhotsk. Note the shiny, smooth appearance due to the flatly arranged scales. Head to the left. Scale bar: 1 mm.

    Figure 4.

    Holotype of Kruppomenia genslerae Ostermair, Brandt, Haszprunar, Jörger & Bergmeier, 2018 (Cavibelonia). Note the spiny outer appearance (needle-like, püreojectinv spicules). Head to the left. Scale bar: 1 mm.

    Overall there is only little faunal overlap on species level between the Sea of Okhotsk and the open NW Pacific: Kruppomenia genslerae Ostermair, Brandt, Haszprunar, Jörger & Bergmeier, 2018 (Figure 4) is so far the only solenogaster species reported from both sides of the Kuril-Kamchatka Trench (Map 4), as confirmed via molecular barcoding, suggesting a connection between the abyssal NW Pacific Plain and the semi-isolated Kuril Basin of the Sea of Okhotsk.

    Most deep-sea Solenogastres known from the NW Pacific all show restricted depth ranges of max. 1,800 m. However, Acanthomeniidae sp. 6 exhibits an astonishing vertical distribution of more than 6,000 m, as conspecifity between five individuals recorded from the bottom of the Kuril-Kamchatka Trench and a single individual from the Sea of Okhotsk was confirmed via molecular barcoding (Bergmeier et al., in press).

    5. Discussion

    Within the last couple of years, the number of deep-sea species of Solenogastres (below 2,000 m) recorded from the NW Pacific has risen from zero to 66 candidate species, with the majority new to science and still pending formal descriptions.

    It is generally assumed that solenogaster diversity is the highest on the continental shelf (Todt 2013) and decreases with increasing depth, which is a general trend in benthic deep-sea diversity (Rex et al. 1990). The comparably high number of abyssal species in the NW Pacific is most likely result from sampling bias, as the solenogaster fauna of the adjacent bathyal zone currently remains largely unexplored.

    The currently known species recorded in the NW Pacific and summarized in this chapter present only a fraction of the actual diversity of deep-sea Solenogastres in the region, and we expect them to continuously rise with increasing sampling efforts.

    Acknowledgements

    We wish to express our gratitude to the editors, Hanieh Saeedi and Angelika Brandt, for the opportunity to join this compilation on benthic NW Pacific deep-sea fauna. Thanks to Hanieh Saeedi for creating the maps of the present chapter and the proofread of the manuscript, Peter C. Kohnert (ZSM Munich) for providing pictures of the amphimeniid Solenogastres, and Bastian Brenzinger (ZSM Munich) for suggestions on the manuscript. We also wish to thank all crew members and scientists participating in the SokhoBio, KuramBio I and II expeditions for their support during the cruises and their sampling efforts. This chapter was part of the “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project (Beneficial project)”. The Beneficial project (grant number 03F0780A) was funded by Federal Ministry for Education and Research (BMBF – Bundesministerium für Bildung und Forschung) in Germany.

    References

    • Bergmeier FS, Brandt A, Schwabe E, Jörger KM (2017) Abyssal Solenogastres (Mollusca, Aplacophora) from the NW Pacific: Scratching the surface of deep-sea diversity using integrative taxonomy. Frontiers in Marine Science 4: 1–22.
    • Bergmeier FS, Haszprunar G, Brandt A, Saito H, Kano Y, Jörger KM (2019) Of basins, plains and trenches: systematics and distribution of Solenogastres (Mollusca, Aplacophora) in the NW Pacific. Progress in Oceanography, Volume 178, 102187.
    • Brandt A, Alalykina I, Fukumori H, Golovan O, Kniesz K, Lavrenteva A, Lörz A-N, Malyutina M, Philipps-Bussau K, Stransky B (2018) First insights into macrofaunal composition from the SokhoBio expedition (Sea of Okhotsk, Bussol Strait and northern slope of the Kuril-Kamchatka Trench). Deep-Sea Research Part II: Topical Studies in Oceanography 154: 106–120.
    • Brandt A, Brix S, Riehl T, Malyutina M (2020) Biodiversity and biogeography of the abyssal and hadal Kuril-Kamchatka trench and adjacent NW Pacific deep-sea regions. Progress in Oceanography, Volume 178: 102232.
    • Brandt A, Elsner NO, Malyutina MV, Brenke N, Golovan OA, Lavrenteva AV, Riehl T (2015) Abyssal macrofauna of the Kuril–Kamchatka Trench area (NW Pacific) collected by means of a camera–epibenthic sledge. Deep-Sea Research Part II: Topical Studies in Oceanography 111: 175–187.
    • Cobo MC, Kocot KM (in press). Micromenia amphiatlantica sp. nov.: first Solenogastres (Mollusca, Aplacophora) with an amphi-Atlantic distribution and insight into abyssal solenogaster diversity. Deep Sea Research Part I: Oceanographic Research Papers, Volume 175, 103189
    • García-Álvarez O, Salvini-Plawen Lv, 2007. Species and diagnosis of the families and genera of Solenogastres (Mollusca). Iberus, 25: 73-143.
    • Liu Y-J, Song S-R, Lee T-Q, Lee M-Y, Chen Y-L, Chen H-F (2006) Mineralogical and geochemical changes in the sediments of the Okhotsk Sea during deglacial periods in the past 500 kyrs. Global and Planetary Change 53: 47–57.
    • Ostermair L, Brandt A, Haszprunar G, Jörger KM, Bergmeier FS (2018) First insights into the solenogaster diversity of the Sea of Okhotsk with the description of a new species of Kruppomenia (Simrothiellidae, Cavibelonia). Deep-Sea Research Part II: Topical Studies in Oceanography 154: 214–229.
    • Salvini-Plawen Lv (1978a) Antarktische und subantarktische Solenogastres. Eine Monographie: 1898-1974 (Part I). Zoologica 128: 1–155.
    • Salvini-Plawen Lv (1978b) Antarktische und subantarktische Solenogastres. Eine Monographie: 1898-1974 (Part II). Zoologica 128: 157–315.
    • Sirenko BI (2013) Check-list of species of free living invertebrates of the Russian Far Eastern Seas. Russian Academy of Sciences, Zoological Institute (St. Petersburg, Russia): 1-258.
    • Todt C (2013) Aplacophoran mollusks - still obscure and difficult? American Malacological Bulletin 31: 181-187.
    • Todt C, Kocot KM (2014) New records for the solenogaster Proneomenia sluiteri (Mollusca) from Icelandic waters and description of Proneomenia custodiens sp. n.. Polish Polar Research 35: 291–310.
    • Todt C, Wanninger A (2010) Of tests, trochs, shells, and spicules: development of the basal mollusk Wirenia argentea (Solenogastres) and its bearing on the evolution of trochozoan larval key features. Frontiers in Zoology 7: 1–17.

    Chapter 8. BIVALVIA: SPECIES COMPOSITION AND RICHNESS OF BIVALVE FAUNA ALONG THE NW PACIFIC

    A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch of Russian Academy of Sciences, Vladivostok 690041, Russia
    Email: gennady.kamenev@mail.ru*

    1. Introduction

    Bivalve mollusks occur from the intertidal zone to the greatest depths of the World Ocean (Filatova 1968, 1971; Knudsen 1970; Scarlato 1981; Belyaev 1989; Coan et al. 2000; Jamieson 2015). Along with peracarid crustaceans, polychaetes and echinoderms, they are the most common and widespread animals in the abyssal zone and have played a key role as a model group in deep-sea biology research (Filatova 1958, 1971, 1976, 1982; Knudsen 1970; Brandt et al. 2005, 2007; Allen 2008; Tittensor et al. 2011). Bivalves are also found in the hadal zone of all investigated deep-water trenches at all depths down to the maximum depth in the Mariana Trench (Filatova 1960; Knudsen 1970; Belyaev and Mironov 1977; Filatova 1985; Belyaev 1989; Ramirez-Llodra et al. 2010; Jamieson 2015; Kamenev 2019). In the hadal zone, they are one of the richest groups of animals, after polychaetes and isopods, in terms of the number of species (Jamieson 2015), and rank second to holothurians in terms of average abundance on the bottom of various trenches, forming sometimes populations with very high densities (Zenkevitch et al. 1955; Filatova 1971; Belyaev 1989). Bivalves are currently one of the best-known animal groups in the northern Pacific (Scarlato 1981; Higo et al. 1999; Coan et al. 2000; Okutani 2000). However, the species composition and distribution of bivalves in the NW Pacific (north of 40°N) at depths in excess of 2,000 m remain insufficiently studied thus far. The NW Pacific is one of the most productive regions of the Pacific Ocean (Sokolova 1981) with high diversity of its benthic fauna (Zenkevitch and Filatova 1958; Filatova 1960, 1968; Belyaev 1989). In this regard, the study of the composition and distribution patterns of the deep-sea fauna in this region of the Pacific Ocean is of particular interest.

    The investigated region of the NW Pacific includes several deep-water ecosystems that are connected with one another to a varying degree: deep-sea basins (maximum depths greater than 3,000 m) in the Sea of Japan, the Sea of Okhotsk, and the Bering Sea; oceanic slopes of the Kuril, Commander, and Aleutian Islands, as well as eastern coast of Kamchatka Peninsula (2,000-6,000 m); abyssal oceanic plain (5,000-6,000 m) adjacent to the Kuril-Kamchatka and Aleutian trenches; the northernmost part of the Japan Trench, the Kuril-Kamchatka Trench, and the deepest western part of the Aleutian Trench (depths in excess of 6,000 m). These deep-sea regions differ in the time of origin, geomorphology, depth, hydrological and hydrochemical regimes, bottom sediment structure, and consequently, the habitat conditions of benthic animals. In addition, they differ in the state of study of the deep-sea bivalve fauna.

    1.1. Sea of Japan

    The Sea of Japan with a maximum depth of 3,670 m (Mel’nichenko 2007), unlike other marginal seas of the NW Pacific, is rather isolated and communicates with the neighboring seas and the Pacific Ocean only via shallow straits (15-130 m deep) (Tada 1994; Tyler 2002; Kitamura et al. 2011). The deep-sea basin of the Sea of Japan includes 3 basins: Tsushima, Central, and Honshu. The Central Basin located north of the 40°N latitude is the largest. Its area is approximately equal to the total area of other deep-sea basins of this sea. The bottom of the Central Basin is an almost flattened slightly sloping plain. The depths of the bottom gradually increase from west to east from 3,200 to 3,450-3,650 m. The maximum depth, which is the greatest for the Sea of Japan, reaches 3,670 m. On the plain surface of the hollow, there are several underwater elevations, which are mainly located in the western and northern parts of the basin. The maximum depths of the elevations are 1,064-1,326 m (Mel’nichenko 2007).

    The first data on the quantitative and bathymetric distribution patterns of dominant species of macrobenthos, including several species of bivalves, in the bathyal and abyssal zones of the Sea of Japan appeared in works of Derjugin (1939) and Derjugin and Somova (1941). Only after the expeditions of the P. P. Shirshov Institute of Oceanology of the Russian Academy of Sciences (Moscow) (IO RAS) (1950, 1972, 1976) undertaken to study the deep-sea bottom fauna of the Sea of Japan, a number of papers dealing with quantitative distribution of macrobenthos in the bathyal and abyssal zones of that sea was published (Mokyevsky 1954; Zenkevitch and Filatova 1958; Zenkevitch 1963; Levenstein and Pasternak 1973, 1976; Pasternak and Levenstein 1978). A total of four species of bivalves were recorded in the Sea of Japan at depths below 2,000 m. Later, Scarlato (1981) examined the bivalves of the Zoological Institute of the Russian Academy of Sciences (Saint-Petersburg) collected in the NW Pacific over 150 years and gave descriptions and illustrations of 279 species and subspecies, of which 6 species were found in the Sea of Japan at depths in excess of 2,000 m. This monograph has long been the most complete Russian-language source of information on the deep-water bivalve fauna of the Sea of Japan. Japanese malacologists also described several species found at the bathyal slope of the Sea of Japan (Kuroda 1929; Okutani and Izumidate 1992) and published surveys of the bivalve fauna of Japan with brief notes on the finding of some species in the deep Sea of Japan (Habe 1977; Higo et al. 1999; Okutani 2000; Okutani and Saito 2014, 2017). During the period from 1972 to 2010, the IO RAS and A.V. Zhirmunsky Institute of Marine Biology of the Far Eastern Branch of the Russian Academy of Sciences (Vladivostok) organized five expeditions (4 expeditions of the IO RAS and SoJaBio (Sea of Japan Biodiversity Studies) Russian-German expedition on the RV Akademik M.A. Lavrentyev), which investigated the bottom fauna in the bathyal and abyssal zones of the Sea of Japan. As a result of examination of this extensive material, the most complete data were obtained on the composition and distributions of bivalves in deep-water basins of the Sea of Japan at depths of 465-3,435 m (Kamenev 2013).

    1.2. Sea of Okhotsk

    The Sea of Okhotsk is a deep-water sea (maximum depth 3,374 m) separated from the Pacific Ocean by a chain of the Kuril Islands (Udintsev 1981). The Pacific waters enter the sea through 17 straits between the Kuril Islands; the Bussol Strait (maximum width 83.3 km; maximum depth 2,318 m) and the Kruzenstern Strait (maximum width 66.7 km; maximum depth 1,920 m) (Glukhovsky et al. 1998) are the widest and deepest. The south-eastern part of the Sea of Okhotsk adjacent to the Kuril Islands is the deepest. The Kuril Basin bounded by the 3,000 m isobath is located here (Ushakov 1953; Glukhovsky et al. 1998). The Kuril Basin narrows in the east and gradually passes into a narrow depression. The abyssal zone (depths in excess of 3,000 m) occupies 123,400 km2, 7.7% of the total area of the sea (Glukhovsky et al. 1998). The northern, continental side of the basin is relatively sloping (5°). The south-eastern slope on the side of the Kuril Islands is steep (20-25°). The floor of the basin has gently sloping, flat or slightly undulating valleys in the west, which gradually give way to flat, horizontal valleys in the east. The sea floor is covered with thick finely-grained sediments, the bulk of which are diatom remains (Tsoy 2007, 2011).

    As a result of extensive biological investigations during the last 70 years, the bivalve fauna of the subtidal and bathyal zones of the Sea of Okhotsk, which occupy 92.3% of the sea floor area, is fairly well known (Scarlato 1981; Kamenev 1996, 2002, 2008, 2009; Kamenev and Nadtochy 1998, 1999, 2000; Kamenev et al. 2001; Kamenev and Nekrasov 2012; Kharlamenko et al. 2016). Nevertheless, despite the intensive investigations of the deep-sea fauna of the NW Pacific and the Russian Pacific seas, very little was known about the species composition of bivalves that inhabit the abyssal zone of the Sea of Okhotsk (Ushakov 1953; Savilov 1961; Scarlato 1981).

    Benthic animals from the abyssal zone of the Sea of Okhotsk were sampled, for the first time, by an expedition with the RV Albatross (1906), which made 1 haul at a depth of 3,375 m (Ushakov 1953). Later, in the course of intensive hydrological and hydrobiological investigations in the Sea of Okhotsk, an expedition on the RV Gagara (1932) collected one more sample from the bottom of the Kuril Basin from 3,350 m depth using a dredge (Ushakov 1953). In both deep-sea samples, a rich benthic fauna was found that contained many taxonomic groups, with the exception of live bivalves. Moreover, an integrated Kuril-Sakhalin expedition on the RV Toporok (1947-1949) investigated the fish fauna and valuable invertebrates off the southern Kuril Islands and the southern part of Sakhalin Island and collected one trawl sample from the 2,850 m depth in the south-western Sea of Okhotsk. In the subsequent years (1949–1990), the IO RAS expeditions have conducted only four deep-sea stations (RV Vityaz, cruise no. 2, 1949) in the Kuril Basin of the Sea of Okhotsk at depths below 2,900 m, including altogether seven samples. The bivalves from the samples were not identified to species. Ushakov (1953) and Savilov (1961) who reviewed the results of all investigations of benthic animals of the Sea of Okhotsk listed only specimens of the genera Thyasira and Cardiomya among the bivalve fauna of the sea floor of the Kuril Basin. Later, Scarlato (1972) described a new bivalve species Cardiomya filatovae Scarlato, 1972 on the basis of an empty shell that was found in a deep-water sample collected by the Gagara expedition in the Kuril Basin of the Sea of Okhotsk. Thus, only 10 samples were collected in the abyssal zone of the Sea of Okhotsk during all the years of investigations. Cardiomya filatovae and a small number of specimens of the genus Thyasira were found in the samples, the rest of the bivalve material remained unidentified.

    In 2015, a SokhoBio (Sea of Okhotsk Biodiversity Studies) Russian-German expedition on the RV Akademik M.A. Lavrentyev investigated the benthic fauna of abyssal depths (greater than 3,000 m) in the Kuril Basin of the Sea of Okhotsk and collected macrobenthos in the deepest Bussol Strait, which connects the Sea of Okhotsk and the Pacific Ocean, as well as at abyssal depths of the Pacific slope of the Kuril Islands that is adjacent to the strait. Investigation of the materials collected by the SokhoBio expedition and two Russian expeditions (RV Toporok, 1948; RV Vityaz, 1949) from the bottom of the Kuril Basin of the Sea of Okhotsk (2,850–3,366 m depth) revealed a rich fauna of bivalves including 25 species (Kamenev 2018c).

    1.3. Bering Sea

    Deep-sea Commander, Aleutian, and Bowers basins of the Bering Sea with a maximum depth of about 4,300 m are located in its western part and are least isolated from the Pacific Ocean (Belous and Svarichevsky 2007). The Bering Sea communicates with the Pacific Ocean through the wide and deep Kamchatka Strait (depth about 4,500 m) and the Blizhniy Strait and numerous relatively shallow straits between the Aleutian Islands.

    The benthic fauna at depths of more than 2,000 m in the western Bering Sea was explored by an expedition with the RV Dalnevostochnik (1932) and four expeditions of the IO RAS (RV Vityaz, 1950, 1951, 1952; RV Akademik Mstislav Keldysh, 1990) (Scarlato 1981; Monin 1983). As a result of these expeditions, extensive material of benthic animals, including bivalves, was collected from depths of more than 2,000 m. However, most of the material of bivalves is not yet examined. To date, only 14 species of bivalves are listed for the deep-water bivalve fauna of the western Bering Sea (Scarlato 1981; Filatova and Schileyko 1984; Krylova 1997; Kamenev 2014, ; 2018а, b ; 2019). However, according to preliminary data (Kamenev, unpublished data), a much richer bivalve fauna occurs in the western part of the Bering Sea at depths greater than 2,000 m.

    1.4. Abyssal plain of the NW Pacific and the Kuril-Kamchatka and Aleutian trenches

    The first studies of the bivalve fauna of the abyssal plain of the central and NW Pacific were performed based on examination of collections made by the famous round-the-world expedition of HMS Challenger in 1872-1876 (Smith 1885). Unfortunately, all samples of benthic animals in the NW Pacific were collected by this expedition from south of 40°N. Intensive studies of the deep-sea fauna of the NW Pacific north of 40°N were begun in 1949 by expeditions of the IO RAS. During the period from 1949 to 1990, the IO RAS organized 13 expeditions, which explored the benthic fauna of the abyssal plain of the NW Pacific Ocean, and the Kuril-Kamchatka and Aleutian trenches. These expeditions collected tremendous material of benthic animals of different taxonomic groups from the entire region. As a result of examination of this material, a large number of new species of bivalves found in the abyssal and hadal zones of the NW Pacific were described, and the distribution of many species in the Pacific was investigated (Filatova 1958, 1960, 1971, 1976; Ivanova 1977; Filatova and Schileyko 1984, 1985; Krylova 1993, 1995, 1997). However, Russian scientists concentrated primarily on the study of benthic animals collected in oceanic trenches, and hence, much of the material sampled from the Pacific abyssal plain remained unexamined.

    The Kuril-Kamchatka and Aleutian trenches are narrow V-shaped depressions of the oceanic floor along the Kuril and respectively Aleutian chains of islands, which are separated by a relatively small area of the ocean floor with depths of less than 6,000 m off the south-eastern coast of Kamchatka. The Kuril-Kamchatka Trench with a maximum depth of 9,600 m (Vasiliev et al. 1978; Kamenev 2019) is among 9 deepest trenches of our planet (Belyaev 1989). The shallower Aleutian Trench (maximum depth 7,822 m) is one of the longest (3,700 km) (Jamieson 2015). The fauna of the Kuril-Kamchatka and Aleutian trenches was explored almost exclusively by expeditions of the RV Vityaz (1949-1969). Only one quantitative sample was taken from the bottom of the eastern part of the Aleutian Trench in 1970 by the U.S. RV Thomas Washington (Belyaev 1989). On the whole, during all the years of study, 26 trawl hauls were made and five quantitative samples were collected using an Okean grab in the Kuril-Kamchatka Trench; eight trawl hauls and five quantitative samples, one of which was taken with a box-corer, in the Aleutian Trench.

    During deep-sea research expeditions, a very rich material of bivalves was collected in the Kuril-Kamchatka and Aleutian trenches. No less than 18 species of bivalves were found in the hadal zone of the Kuril-Kamchatka Trench, which was much better studied, compared to the Aleutian Trench (Belyaev 1989); 11 of them were described as new to science. In the Aleutian Trench, only 10 species were recorded, three species remained unidentified (Filatova 1971, 1976; Ivanova 1977; Filatova and Schileyko 1984, 1985; Belyaev 1989; Krylova 1993, 1997; Kamenev 2018a, 2019).

    Likewise, Japanese researchers were conducting intensive studies of the deep-sea bivalve fauna in the NW Pacific. However, most of their research was performed in the Pacific Ocean south of the 40°N latitude. Okutani (1974) listed 44 species of bivalves found around Japan at depths greater than 2,000 m. Later, after studying the abyssal plain and oceanic trenches in this NW Pacific region, the list was extended significantly (Оkutani and Kawamura 2002; Sasaki et al. 2005; Okutani et al. 2009).

    In recent years, two joint German-Russian expeditions KuramBio (Kuril-Kamchatka Biodiversity Studies) (2012) and KuramBio II (2016) performed complex studies of the benthic fauna of the Pacific abyssal plain adjacent to the Kuril-Kamchatka Trench and the hadal zone of the Kuril-Kamchatka Trench (Brandt and Malyutina 2015; Brandt et al. 2019). After examination of the materials of these expeditions, as well as some of the materials collected by previous expeditions of the IO RAS, nine new species were described and bivalve species composition and distribution in these regions were investigated (Kamenev 2014, 2015, 2018a, b, 2019; Krylova et al. 2015). Moreover, Japanese researchers described 9 species found in the abyssal and hadal zones of the Japan Trench north of 40°N and in the southernmost part of the Kuril-Kamchatka Trench (Okutani and Fujiwara 2005; Sasaki et al. 2005; Okutani et al. 2009). As a result of these studies, data on the species richness of the deep-sea bivalve fauna of the NW Pacific are extended significantly.

    2. Objectives

    The main objectives of this work are (1) to investigate the species composition and richness of bivalve fauna of the deep NW Pacific areas (north of 40°N) at depths in excess of 2,000 m; (2) to analyze the geographic distribution of species founded in these areas; (3) to study the change in the species composition and richness of bivalves in relation to depth.

    3. Material and Methods

    For this study I designated 8 deep-sea areas within the NW Pacific, differing in the time of origin, geomorphology, depth, hydrological and hydrochemical regimes, bottom sediment structure: the Central Basin of the Sea of Japan; the Kuril Basin of the Sea of Okhotsk; the Commander, Aleutian, and Bowers basins of the Bering Sea; oceanic slopes of the Kuril, Commander, and Aleutian Islands, as well as the eastern coast of Kamchatka Peninsula; the abyssal oceanic plain adjacent to the Kuril-Kamchatka and Aleutian trenches; the northernmost part of the Japan Trench; the Kuril-Kamchatka Trench; the western part of the Aleutian Trench (Map 1). For the analysis of species composition and distribution of bivalve molluscs in these areas I used all available data from relevant literature sources (Table 1).

    List of species and the depth range (in meters) of finding of bivalves recorded at depths greater than 2000 m in different deep NW Pacific areas (north of 40°N) and in eastern Pacific.

    Family Species Sea of Japan Sea of Okhotsk Bering Sea Oceanic slopes of the Kuril, Commander, and Aleutian islands Oceanic plain Northernmost part of the Japan Trench Kuril- Kamchatka Trench Western part of the Aleutian Trench Eastern Pacific References
    Nuculidae Gray, 1824 Nucula profundorum Smith, 1885 4,861-5,406 734-4,134 Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2015, 2019
    Pristiglomidae Sanders & Allen, 1973 Pristigloma cf. alba Sanders and Allen, 1973 5,112-5,427 Kamenev 2015
    Setigloma japonica (Smith, 1885) 4,861-5,427 3,000-5,240 Schileyko 1983; Coan et al. 2000; Kamenev 2015
    Nuculanidae H. Adams & A. Adams, 1858 Ledellina convexirostrata Filatova & Schileyko, 1984 4,861-5,427 6,441-6,710 4,860 Filatova and Schileyko 1984; Kamenev 2015, 2019
    Ledellina formabile Filatova & Schileyko, 1984 3,661-4,294 2,800 Filatova and Schileyko 1984; Kamenev 2019
    Microgloma sp. 3,342-3,432 4,861-5,427 Kamenev 2015
    Nuculana leonina (Dall, 1896) 307-2,850 2,622-3,034 1,690-2,500 Kamenev 2018c; Coan et al. 2000
    Parayoldiella ultraabyssalis (Filatova, 1971) 8,355-9,583 Filatova 1971; Filatova and Schileyko 1985; Belyaev 1989; Kamenev 2019
    Parayoldiella mediana (Filatova & Schileyko, 1984) 7,265-8,740 Filatova and Schileyko 1984, 1985; Belyaev 1989; Kamenev 2015
    Poroleda extenuata (Dall, 1897) 2,850 2,992-3,432 2,000-2,900 Coan et al. 2000; Kamenev 2018c
    Robaia robai (Kuroda, 1929) 83-2,900 Scarlato 1981; Okutani 2000; Kamenev 2013
    Bathyspinulidae Coan & Scott, 1997 Bathyspinula calcarella (Dall, 1908) 5,220-5,572 4,861-5,752 6,000-6,860 6296-6328 4,200-5,830 Filatova 1958, 1976; Filatova and Schileyko 1984; Belyaev 1989; Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2019
    Bathyspinula calcar (Dall, 1908) 5,379-5,743 4,000-5,000 Filatova 1958; Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2015
    Bathyspinula vityazi (Filatova, 1964) 6,475-7,587 6,435-9,335 6,965-7,250 Filatova 1964, 1971, 1976; Belyaev 1989; Kamenev 2019
    Malletiidae H. Adams & A. Adams, 1858 Katadesmia vincula (Dall, 1908) 3,206-3,366 1,490-4,382 1,260-5,572 4,861-5,427 7,320 6,400-7,256 6,856-7,250 590-3,585 Coan et al. 2000; Okutani and Fujiwara 2005; Coan and Valentich-Scott 2012; Kamenev 2015, 2018c, 2019
    Neilonellidae Schileyko, 1989 Neilonella politissima Okutani & Kawamura, 2002 4,861-5,787 Kamenev 2015, 2019
    Neilonella profunda Okutani & Fujiwara, 2005 7,320 Okutani and Fujiwara 2005
    Neilonella sp. 1 5,216-5,427 Kamenev 2015
    Neilonella sp. 2 4,679-5,572 4,861-5,752 6,047-6,561 Kamenev 2015, 2019
    Neilonella sp. 3 7,055-7,256 7,246 Belyaev 1989; Kamenev 2019
    Neilonella sp. 4 7,055-8,740 Kamenev 2019
    Siliculidae Allen & Sanders, 1973 Silicula beringiana Kamenev, 2014 4,89-4,811 4,890-4,984 Kamenev 2014
    Silicula okutanii Kamenev, 2014 5,013-5,572 5,101-5,497 6,441-6,561 Kamenev 2014, 2015, 2018c, 2019
    Tindariidae Verrill & Bush, 1897 Tindaria antarctica Thiele & Jaeckel, 1931 5,220-5,572 4,861-5,427 6,441-6,561 Kamenev 2015, 2019
    Tindaria sp. 1 4,861-5,352 Kamenev 2015, 2019
    Tindaria sp. 2 4,679-5,572 4,861-5,427 Kamenev 2015, 2018c, 2019
    Tindaria sp. 3 4,861-5,427 Kamenev 2015, 2019
    Tindaria sp. 4 4,861-5,427 Kamenev 2015
    Tindaria sp. 5 4,977-4,998 Kamenev 2015
    Tindaria sp. 6 2,327-3,366 Kamenev 2018c
    Tindaria sp. 7 6,441-6,561 6,296-7,286 Belyaev 1989; Kamenev 2019
    Yoldiidae Dall, 1908 Megayoldia sp. 2,850 Kamenev 2018c
    Yoldiella derjugini Scarlato, 1981 22-2,520 520-800 Scarlato 1981; Coan et al. 2000; Kamenev 2013
    Yoldiella cf. jeffreysi (Hidalgo, 1877) 4,861-5,497 Kamenev 2015, 2019
    Yoldiella kaikonis Okutani & Fujiwara, 2005 7,299-7,333 Okutani and Fujiwara 2005
    Yoldiella olutoroensis Scarlato, 1981 3,000 Scarlato 1981
    Yoldiella orbicularis Scarlato, 1981 53-2,300 Scarlato 1981; Kamenev 2013
    Yoldiella sp. 1 3,206-3,307 3,342-3,432 Kamenev 2018c
    Yoldiella sp. 2 6,441-7,256 Kamenev 2019
    Mytilidae Rafinesque, 1815 Dacrydium rostriferum Bernard, 1978 3,206-3,366 3,313-4,294 4,679-5,013 4,690-5,787 6,090-6,561 2,350-2,870 Coan et al. 2000; Kamenev 2015, 2018c, 2019
    Dacrydium vitreum (Møller, 1842) 40-3,347 500-3,170 depth not specified Scarlato 1981; Coan et al. 2000; Kamenev 2013
    Arcidae Lamarck, 1809 Bathyarca imitata (Smith, 1885) 3,206-3,307 4,861-5,497 1,463-4,000 Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2015, 2018c, 2019
    Bentharca asperula (Dall, 1881 4,861-5,223 3,100-4,900 Coan et al, 2000; Coan and Valentich-Scott 2012; Kamenev 2007, 2015
    Pectinidae Rafinesque, 1815 Delectopecten vancouverensis (Whiteaves, 1893) 730-3,435 27-4,100 Scarlato 1981; Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2013
    Hyalopecten abyssalis Kamenev, 2018 4,550-5,020 Kamenev 2018a
    Hyalopecten kurilensis Kamenev, 2018 4,995-5,045 Kamenev 2018a
    Hyalopecten vityazi Kamenev, 2018 6,090-8,100 6,410-7,246 Kamenev 2018a, 2019
    Propeamussiidae Abbott, 1954 Catillopecten brandtae Kamenev, 2018 4,860-5,423 Kamenev 2015, 2018b
    Catillopecten malyutinae Kamenev, 2018 4,988-5,418 6,090-6,135 4,081 Kamenev 2015, 2018b, 2019
    Catillopecten natalyae Kamenev, 2018 3,342-3,432 5,112-5,497 Kamenev 2015, 2018b, 2019
    Catillopecten squamiformis (Bernard, 1978) 2,901-3,366 3,957-4,382 3,342-4,990 4,391-4,990 2,000-5,020 Coan et al. 2000; Kamenev 2015, 2018b, 2019
    Parvamussium pacificum Kamenev, 2018 4,860-5,497 5,180 Kamenev 2015, 2018b, 2019; P. Valentich-Scott, personal communication
    Limidae Rafinesque, 1815 Limatula sp. 1 5,220-5,572 4,861-5,497 Kamenev 2015, 2019
    Limatula sp. 2 4,997-5,406 Kamenev 2015
    Thyasiridae Dall, 1900 Adontorhina cyclia S.S. Berry, 1947 308-3,366 3,342-3,432 12-3,000 Kamenev 1995, 1996, 2013, 2018c; Coan et al. 2000; Coan and Valentich-Scott 2012
    Adontorhina sp. 1 4,679-5,013 Kamenev 2018c
    Axinodon sp. 2 1,694-3,366 4,679-5,013 Kamenev 2018c
    Axinopsida subquadrata (A. Adams, 1862) 5- 2,550 Scarlato 1981; Kamenev 2013
    Axinulus sp. 1 3,342-3,432 4,861-5,787 Kamenev 2015, 2018c
    Axinulus sp. 2 9,301-9,583 Kamenev 2019
    Axinulus sp. 3 5,220-5,572 6,047-6,221 Kamenev 2019
    Axinulus sp. 4 6,460-7,285 Belyaev 1989
    Axinulus hadalis (Okutani, Fujikura & Kojima, 1999) 6,326-7,434 Okutani et al. 1999; Sasaki et al. 2005
    Channelaxinus excavata (Dall, 1901) 2,901-3,218 2,359 800-2,520 Kamenev 2018c; Coan et al. 2000; Coan and Valentich-Scott 2012
    Genaxinus” sp. 1 5,220-5,572 5,101-5,752 6,047-9,583 Kamenev 2019
    Genaxinus” sp. 2 5,220-5,572 5,726-5,752 6,441-7,256 Kamenev 2019
    Mendicula sp. 1 1,694-3,366 3,342-5,572 4,861-5,787 6,047-7,256 Kamenev 2015, 2018c, 2019
    Mendicula sp. 2 2,327-3,366 3,342-5,572 4,997-5,752 6,047-6,221 Kamenev 2015, 2018c, 2019
    Mendicula sp. 3 1,694-3,366 3,342-3,432 Kamenev 2018c
    Parathyasira sp. 1 3,206-3,366 3,342-5,013 4,977-5,406 Kamenev 2015, 2018c
    Parathyasira sp. 2 4,679-5,013 5,217-5,406 Kamenev 2015, 2018c
    Parathyasira sp. 3 6,047-6,561 Kamenev 2019
    Thyasira kaireiae (Okutani, Fujikura & Kojima, 1999) 5,791-6,390 Okutani et al. 1999; Sasaki et al. 2005
    Thyasira sp. 1 4,861-5,787 Kamenev 2015
    Thyasira sp. 2 900-3,102 Kamenev 2013
    Thyasiridae gen. sp. 7,055-8,740 Kamenev 2019
    Tellinidae Blainville, 1814 Macoma shiashkotanika (Scarlato, 1981) 465-4,984 Kamenev and Nadtochy 1999; Kamenev 2018c
    Montacutidae Clark, 1855 Montacutidae gen. sp. 5,101-5,497 6,441-6,561 Kamenev 2015, 2019
    Mysella sp. 1,694-3,351 Kamenev 2018c
    Syssitomya cf. pourtalesiana Oliver, 2012 5,347-5,427 Kamenev 2015
    Vesicomyidae Dall & Simpson, 1901 Abyssogena phaseoliformis (Métivier, Okutani & Ohta, 1986) 5,400-6,400 4,700-6,200 4,550-6,400 4,190-4,982 Métivier et al. 1986; Fujikura et al. 2002; Kojima et al. 2004; Sasaki 2005; Okutani et al. 2009; Krylova et al. 2010
    Calyptogena extenta (Krylova & Moskalev, 1996) 3,512 3,000-4,445 Okutani et al. 2009; Coan and Valentich-Scott 2012
    Calyptogena sp. 4,819 Okutani et al. 2009
    Ectenagena laubieri kurilensis (Okutani & Kato, 2009) 3,512-3,560 Okutani et al. 2009
    Isorropodon fossajaponicum (Okutani, Fujikura & Kojima, 2000) 6,248-6,809 Okutani et al. 2000; Fujikara et al. 2002; Sasaki et al. 2005
    Vesicomyafilatovae Krylova & Kamenev, 2015 4,861-5,497 Kamenev 2015, 2019; Krylova et al. 2015
    Vesicomya pacifica (Smith, 1885) 3,299-3,366 3,957-3,978 3,342-5,572 4,861-5,787 1,200-6,200 Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2015, 2018c, 2019; Krylova et al. 2015, 2018
    Vesicomya profundi Filatova, 1971 6,047-9,050 7,246 Filatov 1971; Belyaev 1989; Krylova et al. 2015, 2018; Kamenev 2019
    Vesicomya sergeevi Filatova, 1971 6,090-9,530 Filatova 1971; Belyaev 1989; Krylova et al. 2015, 2018; Kamenev 2019
    Xylophagidae Purchon, 1941 Xylophaga sp. 1 5,216-5,223 Kamenev 2015
    Xylophaga sp. 2 5,347-5,379 Kamenev 2015
    Xylophaga sp. 3 5,217-5,243 Kamenev 2015
    Xylophaga sp. 4 5,217-5,243 Kamenev 2015
    Xylophaga sp. 5 5,347-5,352 Kamenev 2015
    Protocuspidariidae Scarlato & Starobogatov, 1983 Protocuspidaria sp. 5,236-5,406 Kamenev 2015
    Cuspidariidae Dall, 1886 Bathyneaera hadalis (Knudsen, 1970) 3,957-3,978 4,418-5,752 6,047-8,740 Krylova 1993, 1997; Kamenev 2015, 2019
    Cardiomya behringensis (Leche, 1883) 31-2,900 Scarlato 1981; Kamenev 2013
    Cardiomya filatovae Scarlato, 1972 3,299-3,366 3,260-3,875 3,880-3,900 Scarlato 1972, 1981; Krylova 1997; Kamenev 2018с
    Cardiomya sp. 1 3,342-3,432 Kamenev 2018c
    Cardiomya sp. 2 3,351-3,353 Kamenev 2018c
    Cuspidaria cf. abyssopacifica Okutani, 1975 3,299-3,353 3,342-3,432 Kamenev 2018c
    Cuspidaria cf. arcoida (Okutani & Kawamura, 2002) 5,112-5,130 Kamenev 2015
    Cuspidaria buccina Bernard, 1989 5,112-5,130 3,585 Coan et al., 2000; Kamenev 2015
    Cuspidaria sp. 1 5,101-5,497 Kamenev 2019
    Cuspidaria sp. 2 3,206-3,307 Kamenev 2018c
    Cuspidaria sp. 3 3,305-3,366 Kamenev 2018c
    Cuspidaria sp. 4 2,430-2,670 Krylova 1997
    Cuspidaria sp. 5 3,875 Krylova 1997; Coan et al. 2000;
    Myonera garretti Dall, 1908 3,299-3,366 3,260-4,294 1,645-4,294 Krylova 1997; Coan et al. 2000; Coan and Valentich-Scott 2012; Kamenev 2018c
    Myonera paucistriata Dall, 1886 4,550-5,427 1,000-3,806 Krylova 1997; Coan et al. 2000; Kamenev 2015
    Octoporia sp. 5,379-5,427 Kamenev 2015
    Rengea murrayi (Smith, 1885) 4,861-5,427 Kamenev 2015
    Rhinoclama filatovae (Bernard, 1979) 4,550-5,497 3,315-5,140 Krylova 1997; Coan et al. 2000; Kamenev 2015, 2019
    Poromyidae Dall, 1886 Cetoconcha sp. 3,342-3,432 5,236-5,379 Kamenev 2015, 2018c
    Poromya sp. 5,347-5,352 Kamenev 2015
    Lyonsiellidae Dall, 1895 Dallicordia cf. alaskana (Dall, 1895) 5,347-5,352 450-3,570 Coan et al. 2000; Coan and Valentich-Scott 2012
    Policordia extenta Ivanova, 1977 8,185-8,400 Ivanova 1977; Belyaev 1989; Kamenev 2019
    Policordia laevigata Ivanova, 1977 8,185-8,740 Ivanova 1977; Belyaev 1989; Kamenev 2019
    Policordia maculata Ivanova, 1977 9,000-9,050 Ivanova 1977; Belyaev 1989; Kamenev 2019
    Policordia ovata Ivanova, 1977 5,740 6,040 Ivanova 1977
    Policordia rectangulata Ivanova, 1977 8,175-9,583 Ivanova 1977; Belyaev 1989; Kamenev 2019
    Policordia sp. 1 3,206-3,366 Kamenev 2018c
    Policordia sp. 2 6,047-6,221 Kamenev 2019
    Map 1.

    Deep NW Pacific areas (north of 40°N): CeB – Central Basin of the Sea of Japan; KuB – Kuril Basin of the Sea of Okhotsk; DeB – deep-sea Commander, Aleutian, and Bowers basins of the Bering Sea; OcS – oceanic slopes of the Kuril, Commander, Aleutian Islands, and eastern coast of Kamchatka Peninsula; JT – Japan Trench; KKT – Kuril-Kamchatka Trench; AT – Aleutian Trench; AbP – abyssal plain of the Pacific Ocean.

    4. Results

    4.1. Composition of the bivalve fauna of deep NW Pacific areas

    To date, 123 species (including morphospecies) that belong to 56 genera and 23 families have been recorded for the NW Pacific north of 40°N at depths greater than 2,000 m (Table 1, Figures 1 and 2). About one third of them (39 species, 31.7%) belong to the subclass Protobranchia. Out of the 123 species, 68 species (55.3%) were identified to the species level. Other 55 species (44.7%) need additional research, and very probably, most of them are new to science. The richest families in terms of number of species were the Thyasiridae (22 species) and Cuspidaridae (18 species). Other families were represented by no more than nine species, and four families (Nuculidae, Malletidae, Tellinidae, and Protocuspidariidae) were represented by merely one species. The abyssal plain adjacent to the Kuril-Kamchatka and Aleutian trenches had the greatest number of species (60) among all the deep NW Pacific areas studied (Table 2). In deep-sea basins of the Sea of Japan, Sea of Okhotsk, and Bering Sea, the richest bivalve fauna was recorded for the Kuril Basin in the Sea of Okhotsk. The smallest number of species (8) at depths of more than 2,000 m was found in the Sea of Japan. Almost four times more species were found in the hadal zone (at depths greater than 6,000 m) of the Kuril-Kamchatka Trench than in the hadal zone of the Aleutian Trench. At the present time, the bivalve fauna of the Kuril-Kamchatka Trench is the richest, after the bivalve fauna of the abyssal plain, in number of species among the deep NW Pacific areas compared.

    Widely distributed deep-sea bivalve species of the North Pacific: (A–B) Ledellina convexirostrata, Kuril-Kamchatka Trench, 6,551–6,560 m; (C–D) Nuculana leonina, Bering Sea, 2,622–3,034 m, 23.6 mm shell length; (E–F) Poroleda extenuata, Kuril Islands, Pacific Ocean, 3,342–3,432 m, 24.0 mm shell length; (G–H) Katadesmia vincula, Sea of Okhotsk, 3,351–3,353 m, 14.9 mm shell length; (I–J) Parayoldiella ultraabyssalis, Kuril-Kamchatka Trench, 9,294–9,431 m; (K) Bathyspinula calcarella, abyssal plain adjacent to Kuril-Kamchatka Trench, Pacific Ocean, 5,417–5,422 m, 15.4 mm shell length; (L) Bathyspinula vityazi, Kuril-Kamchatka Trench, 7,955–8,015 m, 15.0 mm shell length; (M–N) Dacrydium rostriferum, abyssal plain adjacent to Kuril-Kamchatka Trench, Pacific Ocean, 5,290–5,427 m; (O–P) Dacrydium vitreum, Sea of Japan, 970–1,075 m; (Q–R) Bathyarca imitata, Sea of Okhotsk, 3,305–3,307 m, 6.8 mm shell length. Scale bars: (A–B, I–J, M–N) = 500 µm; (O–P) = 200 μm.

    Figure 2.

    Widely distributed deep-sea bivalve species of the North Pacific: (A–B) Delectopecten vancouverensis, Sea of Japan, 2,700–3,100 m, 15.7 mm shell length; (C–D) Catillopecten squamiformis, Bering Sea, 3,957–3,978 m, 10.1.mm shell length; (E–F) Parvamussium pacificum, abyssal plain adjacent to Kuril-Kamchatka Trench, Pacific Ocean, 5,398–5,389 m, 8.5 mm shell length; (G) Vesicomya pacifica, Sea of Okhotsk, 3,351–3,353 m, 5.2 mm shell length; (H) Vesicomya profundi, Kuril-Kamchatka Trench, 8,240–8,345 m; (I) Vesicomya sergeevi, Kuril-Kamchatka Trench, 9,170–9,335 m; (J–K) Bathyneaera hadalis, Kuril-Kamchatka Trench, 8,740–8,735 m, 10.0 mm shell length; (L–M) Macoma shiashkotanika, Bering Island, Commander Islands, Bering Sea, 1,490 m, 9.3 mm shell length; (N) Adontorhina cyclia, Sea of Japan, 970–1,075 m, Scale bars: (H) = 500 µm; (I) = 1 mm; (N) = 200 μm.

    The number of bivalve families, genera, and species recorded at depths greater than 2,000 m in different deep-sea areas of the NW Pacific (north of 40°N).

    Taxon Sea of Japan Sea of Okhotsk Bering Sea Oceanic slopes of the Kuril, Commander, and Aleutian islands Oceanic plain Northernmost part of the Japan Trench Kuril-Kamchatka Trench Western part of the Aleutian Trench
    Family 6 12 9 15 22 6 15 8
    Genus 7 21 13 24 37 8 22 9
    Species 8 26 14 34 60 8 35 10

    4.2. Geographic distribution of species

    On the whole, almost half of the 68 identified species (29 species, 42.6%) are widespread in the northern Pacific and were recorded in the eastern Pacific off the coasts of America. In its turn, out of the remaining 39 species, most species (23) are widespread in the NW Pacific. These species were found in the shelf, bathyal, and abyssal zones of the NW Pacific marginal seas or in different areas of the vast abyssal plain adjacent to the Kuril-Kamchatka and Aleutian trenches. Likewise, a considerable part of hadal species was found in more than one trench of the NW Pacific. It should be noted that a significant part of morphospecies is also widespread in this Pacific region. Now, merely 15 identified species were recorded only in one of the deep NW Pacific areas compared and can be considered endemic to the areas. Almost all species are fairly widespread in their areas and some of them form extensive populations and occur in large numbers. Thus, Robaia robai (Kuroda, 1929) and Yoldiella orbicularis Scarlato, 1981 are widespread only in the Sea of Japan, while Parayoldiella ultraabyssalis (Filatova, 1971), Vesicomya sergeevi Filatova, 1971, Policordia laevigata Ivanova, 1977, and Policordia rectangulata Ivanova, 1977 occur widely in the hadal zone of the Kuril-Kamchatka Trench, where P. ultraabyssalis and V. sergeevi are the dominant species of macrobenthos on the lower slopes and bottom of the trench, forming very abundant populations. Out of all identified species, only four (Yoldiella olutoriensis Scarlato, 1981, Policordia extenta Ivanova, 1977, Policordia maculata Ivanova, 1977, and Hyalopecten kurilensis Kamenev, 2018) were described from specimens found only in one sample. This, in part, may be due to that the deep-sea area of finding of species is poorly studied. For example, Y. olutoriensis was found in a very poorly studied deep-sea basin of the Bering Sea. It is also possible that the species are in the category of rare species and may be found in other Pacific regions after more intensive studies in the NW Pacific. For example, H. kurilensis was so far found only in one sample collected from the abyssal plain adjacent to the Kuril-Kamchatka Trench.

    4.3. Vertical distribution of species

    The analyzed deep NW Pacific areas included partially or fully three vertical zones of the World Ocean: the lower bathyal zone (2,000-2,999 m); the abyssal zone (3,000-5,999 m); almost the entire hadal zone (6,000-9,600 m). Analysis of the bivalve species richness within 1,000 m depth ranges showed that the number of species and, correspondingly, genera and families markedly increases with increasing depth from 2,000 to 5,999 m (Table 3). The greatest number of species (60) was found in the lower abyssal zone at depths of 5,000-5,999 m, on the oceanic plain adjacent to the trenches. At depths of more than 6,000 m, in the hadal zone of the trenches, the bivalve species richness sharply decreases with depth, reaching the minimum (8 species) at the maximum depth (more than 9,000 m). In the hadal zone of the NW Pacific region studied, the highest number of species (38 species) was found in its uppermost depth range (6,000-6,999 m). The proportion of members of the subclass Protobranchia in the bivalve fauna of the hadal zone increases to 39.5%, compared to the species-richest abyssal depth range of 5,000-5,999 m where it is 30%.

    A small portion of all deep-sea species of the NW Pacific (28 species, 22.8%) were not encountered at depths greater than 4,000 m and occurred in the subtidal, bathyal, and upper abyssal zones. Most of these relatively shallow-water species were recorded in deep-sea basins of the NW Pacific marginal seas. Only a small portion of these species was found on the oceanic slopes of the Japanese, Kuril, and Aleutian Islands and eastern Kamchatka Peninsula. Most species (69 species, 56.1%) were only recorded at depths of more than 4,000 m in the lower abyssal zone and in the hadal zone. About one third of them (22 species, 31.9%) were exclusively found in the hadal zone of the Japan, Kuril-Kamchatka, and Aleutian trenches at depths of more than 6,000 m. Hence, at the present time, they can be considered endemic to this zone.

    The vertical distribution of the number of bivalve families, genera, and species recorded at depths of more than 3,000 m in the NW Pacific (north of 40°N).

    Taxon Depth range (m)
    2,000-2,999 3,000-3,999 4,000-4,999 5,000-5,999 6,000-6,999 7,000-7,999 8,000-8,999 9,000+
    Family 12 16 18 22 15 10 8 5
    Genus 20 30 33 41 21 13 9 6
    Species 24 41 47 60 38 18 13 8

    For most of deep-sea bivalve species found in the studied NW Pacific region, the vertical distribution range does not exceed 3,000 m. Only 17 species (13.8%) were found in the depth range greater than 3,000 m. For 10 out of the 17 species (Katadesmia vincula (Dall, 1908), Silicula beringiana Kamenev, 2014, Dacrydium rostriferum Bernard, 1978, Delectopecten vancouverensis (Whiteaves, 1893), “Genaxinus” sp. 1, Macoma shiashkotanika (Scarlato, 1981), Vesicomya pacifica (Smith 1885), Bathyneaera hadalis (Knudsen, 1970), Myonera paucistriata Dall, 1886, Dallicordia alaskana (Dall 1895)), the vertical distribution range exceeds 4,000 m. All the species are widespread in the northern Pacific, except Silicula beringiana Kamenev, 2014, which was predominantly recorded in the Bering Sea.

    5. Discussion

    The first surveys of the species richness of the deep-sea bivalve fauna of the World Ocean (Clarke 1962; Knudsen 1970), as well as the Pacific (Filatova 1968) listed only 6 species for the NW Pacific north of the 40°N latitude at depths of more than 2,000 m. This is not surprising because these studies reported results obtained from the very first deep-sea expeditions, and a significant portion of bivalve materials collected north of 40°N by mainly Russian researchers was to be examined (Filatova 1968). Subsequent analogous reviews of the deep-sea bivalve species composition of the NW Pacific south of 40°N, already listed no less than 50 species found off Japan at depths below 2,000 m (Okutani 1974, 1975). In the following years, Russian and Japanese researchers described a large number of new species of bivalves found in the Sea of Japan, the Sea of Okhotsk, and the Bering Sea, as well as in the abyssal and hadal zones of the Pacific. As a result, the list of species inhabiting depths of more than 2,000 m to the north of 40°N was extended to 42 species (Filatova 1971, 1976; Scarlato 1972, 1981; Ivanova 1977; Filatova and Schileyko 1984, 1985; Belyaev 1989; Krylova 1993, 1997; Kamenev and Nadtochy 1999; Okutani et al. 1999, 2009; Okutani and Fujiwara 2005; Sasaki et al. 2005).

    In recent years, examination of materials collected by Russian-German (2010 and 2015) and German-Russian (2012 and 2016) expeditions in the deep-sea basins of the Sea of Japan and the Sea of Okhotsk, as well as on the abyssal plain adjacent to the Kuril-Kamchatka Trench and in the hadal zone of the trench down to its maximum depth made a significant contribution deep-sea bivalve fauna research (Kamenev 2013, 2014, 2015, 2018a, b, c, 2019; Krylova et al. 2015). Thus, all these studies in the NW Pacific north of the 40°N latitude revealed a very rich and diverse deep-sea bivalve fauna (123 species). For comparison, Knudsen (1970) listed 193 species belonging to 20 families for the deep-sea bivalve fauna of the whole World Ocean. Taking into account more recent data, Allen (2008) listed 14 living bivalve families present at the 5,000 m depth in the Atlantic, while in the studied Pacific region members of 22 bivalve families were recorded for the abyssal plain (5,000-6,000 m). As an example, we also note that in such a large region as Great Australian Bight (southern coast of Australia) merely 43 species of bivalves from 18 families were recorded at depths of 200 to 5,000 m (MacIntosh et al. 2018). In reality, the deep-sea bivalve fauna of the NW Pacific is even richer, and further research will significantly increase the number of species inhabiting depths below 2,000 m. To date, fairly well-studied bivalve faunas are those of the deep-sea basin of the Sea of Japan, the bottom of the Kuril Basin (depths of more than 3,000 m) of the Sea of Okhotsk, the oceanic abyssal plain near the Kuril-Kamchatka Trench, and the Kuril-Kamchatka Trench. So far, the rich faunas of the lower slopes of the Kuril Basin (2,000-3,000 m) in the Sea of Okhotsk, oceanic slopes (2,000-5,000 m) of the Kuril, Commander, Aleutian Islands, and eastern Kamchatka, deep-sea basins of the Bering Sea (2,000-4,000 m), and the hadal zone of the Aleutian Trench are still very poorly studied (Scarlato 1981; Kamenev 2018c). As an example, according to preliminary data, the deep-sea fauna of the Bering Sea harbors no less than 40 species (Kamenev, unpublished results), while only at two stations performed on the oceanic slope of the Kuril Islands 23 species of bivalves were found at depths of 3,000-5,000 m (Kamenev 2018с).

    The high species richness and diversity of the deep-sea bivalve fauna of this northern Pacific region are probably due to the abundant organic matter fluxes to the bottom. Many researchers showed that one of the main factors limiting the diversity and abundance of deep-sea fauna is food availability to bottom animals (Rex et al. 2005; Rex and Etter 2010). The NW Pacific is one of the most productive regions of the World Ocean with high level of primary production in the marginal seas and around the Kuril-Kamchatka Trench (Sokolova 1976, 1981). Hence, organic matter abundantly supplied to the bottom creates favorable feeding conditions for the diverse and plentiful bottom fauna in the abyssal and hadal zones of this Pacific region (Filatova 1960, 1968; Belyaev and Mironov 1977; Belyaev 1989).

    The deep-sea fauna of the Sea of Japan is the poorest (in number of species) among all deep NW Pacific areas. Only three species were recorded at maximum depths (more than 3,000 m) of that sea. No characteristic species of the Pacific abyssal zone were found in the deep-sea basins of the Sea of Japan. The deep-water bivalve fauna of the Sea of Japan is an impoverished shelf fauna comprised of eurybathic species that extend from the shelf to the bathyal and abyssal zones. Most of them have a wide geographic distribution. The lack of typical abyssal species of bivalves in the deep Sea of Japan is probably connected with the isolation of this body of water from the Pacific abyssal depths (Kamenev 2013).

    In the Sea of Okhotsk, only the fauna of the bottom of the Kuril Basin at depths below 3,000 m was studied in detail (Kamenev 2018c). In contrast to the Sea of Japan, in the abyssal zone of the Sea of Okhotsk there is a species-rich fauna of bivalves with many Pacific eurybathic bathyal-abyssal species, which could penetrate into the Sea of Okhotsk through deep-sea straits between the Kuril Islands.

    The greatest number of species was recorded for the abyssal plan adjacent to the trenches. Most species were found in this region during the KuramBio German-Russian expedition (2012). This expedition sampled many small species with a fragile shell which were difficult to collect in previous expeditions using such sampling gear as trawls and dredges. Knudsen (1970) noted that “there is little doubt; however, that the abyssal zone harbors numerous minute species which, owing to too crude sampling methods, have remained unknown”. The finding of these minute species much increased the bivalve species richness of this region (Kamenev 2015). A rich, in number of species, fauna was also recorded for the Kuril-Kamchatka Trench. The bottom fauna of this trench is the best studied as a result of numerous expeditions of Russian researchers (Belyaev 1989). Nevertheless, using modern sampling methods and gear, studies of the KuramBio II German-Russian expedition (2016) significantly increased data on the bivalve species richness of this trench owing to the finding of minute species (Kamenev 2019).

    The relatively low species richness of the deep-sea bivalve fauna of the Bering Sea, oceanic slopes of the Kuril, Commander and Aleutian Islands, and the eastern coast of Kamchatka, as well as the Aleutian Trench, are exclusively connected with insufficient study of these deep-sea regions. Overall, about half of species comprising the deep-sea fauna of this NW Pacific region were not determined to the species level. Many of the species will probably be described as new to science and the systematic position of many will be ascertained as a result of further research.

    Allen (2008) noted that in the abyssal zone there is a large increase in the number of deposit feeding species to which protobranchs belong. In the Atlantic Ocean, at depths greater than 4,500 m, the proportion of protobranch species is 57.3%. In the studied sector of the NW Pacific, at similar abyssal depths (5,000-5,999 m), the proportion of protobranch species is almost two times lower (30%) than in the Atlantic and increases to 39.5% in the hadal zone at depths of more than 6,000 m. The relatively low share of protobranch species in the abyssal and hadal zones of this region is probably connected with recent records of many species of the Pectinidae, Propeamussidae, Thyasiridae, Vesicomyidae, Cuspidariidae, and Lyonsiellidae. More than half of deep-sea species (64 species, 52%) of this NW Pacific region belong to these families. The richest, in number of species, families were the Cuspidariidae and Thyasiridae, with thyasirids being the least studied (77.3% of the total number of species of this family were not identified to species level). Previously, this family was only represented by a few species in the NW Pacific deep-sea fauna (Scarlato 1981; Belyaev 1989; Sasaki et al. 2005). Only recent studies using epibenthic sledge have allowed collecting a large number of minute thyasirids having a very fragile shell, which is easily destroyed by sampling with trawls and dredges (Kamenev 2015, 2018c, 2019). In the Atlantic Ocean, this family is also the richest in number of deep-sea species, of which a great many remain to be described (Allen 2008). An important contribution to the knowledge of the species richness of the family Vesicomyidae was made by Japanese researchers who found many specialized species in chemosynthesis-based biological communities in this region (Sasaki et al. 2005).

    With increase in depth, the number of species increases, reaching the maximum at 5,000-5,999 m depth. Such a change in the bivalve species richness in the depth range of 2,000-5,999 m primarily reflects the level of knowledge of faunas of different deep-sea regions of the NW Pacific. The least studied regions such as the slopes of the Kuril Basin, oceanic slopes of the Kuril, Commander and Aleutian Islands, and Kamchatka, as well as the deep-sea basins of the Bering Sea have depths of 2,000 to 5,000 m. Preliminary researches revealed a very rich bivalve fauna in these vast regions (Kamenev 2018c; unpublished results). Thorough studies of these deep NW Pacific regions will increase the number of bivalve species and, correspondingly, change the picture of the vertical distribution of species in the whole region. At the 5,000-5,999 m depth, there is a relatively well-studied vast area of the oceanic abyssal plain near the trenches. Therefore, to date the richest bivalve fauna is known at these depths. Many researchers have also shown that the ecosystem of the abyssal plain of the World Ocean is one of the richest and diverse on the planet (Etter and Mullineaux 2001; Snelgrove and Smith 2002; Stuart et al. 2003). It is very likely that this vast plain is the species-richest among all deep NW Pacific regions to the north of 40°N. Depths of greater than 6,000 m correspond to the hadal zone of oceanic trenches, in which the bottom fauna becomes much impoverished with increasing depth (Belyaev 1989; Jamiesson 2015). Future detailed studies of the bottom fauna of the Aleutian Trench will probably change the species ratio within different depth ranges of the hadal zone of the region of the NW Pacific but will not influence the general pattern of vertical distribution of species at depths below 6,000 m.

    Acknowledgments

    I am very grateful to Drs. A.V. Gebruk, E.M. Krylova, T.N. Molodtsova, A.N. Mironov, A.V. Kremenckaya, K.V. Minin, all collaborators of the Laboratory of Ocean Bottom Fauna (IO RAS), as well as to Drs. H. Saito (National Museum of Nature and Science, Tsukuba, Japan), L.T. Groves (Natural History Museum of Los Angeles County, Los Angeles, USA), E. Kools (California Academy of Sciences, San Francisco, USA), P. Valentich-Scott (Barbara Museum of Natural History, Santa Barbara, USA), M.A. Frey, H. Gartner (Royal BC Museum, Victoria, Canada), B. Hausdorf (Zoological Museum, Hamburg, Germany) for arrangement of my work with the bivalve mollusk collections and great help during this work; to Dr. E.M. Krylova for identification of bivalves of the families Vesicomyidae and Cuspidariidae; to Drs. E.V. Coan (Department of Invertebrate Zoology, California Academy of Sciences, San Francisco, USA), E.M. Krylova, and P. Valentich-Scott for the sending copies of scientific papers necessary for this work; to Dr. M.V. Malyutina (National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia), chief scientist of the SokhoBio expedition and coordinator of the Russian team of the KuramBio and KuramBio II expeditions, and to Prof. Dr. A. Brandt (Senckenberg Research Institute and Natural History Museum, and Goethe University Frankfurt, Frankfurt, Germany), chief scientist of the KuramBio and KuramBio II expeditions and coordinator of the German team of the SokhoBio expedition, for invitation to join the deep-sea expeditions KuramBio (RV Sonne 2012), SokhoBio (RV Akademik M.A. Lavrentyev 2015), KuramBio II (RV Sonne 2016) and to the scientific stuff of the expeditions and the ship crews for their assistance during the expeditions; to Prof. Dr. A. Brandt and Dr. H. Saeedi (Senckenberg Research Institute and Natural History Museum, and Goethe University Frankfurt, Frankfurt, Germany) for great help during this work; to Ms. T.N. Koznova (National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, Russia) for help with the translation of the manuscript into English. The present research was performed within the project (grant number 03F0780A) “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean (Beneficial Project)”, which was funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany. This research was also supported by the Russian Foundation for Basic Research (Grant no. 19-04-00281-а).

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    Chapter 9. SIPUNCULA: A REVIEW ON BIOGEOGRAPHY OF THE DEEP-SEA SIPUNCULA ALONG THE NW PACIFIC

    aA.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch of Russian Academy of Sciences, Palchevskogo str. 17, Vladivostok 690041, Russia
    bFar Eastern Federal University, Sukhanova str. 8, Vladivostok 690091, Russia
    E-mail: anastasia.mayorova@gmail.com*

    1. Introduction

    Sipunculans are a well-separated monophyletic group of marine coelomic worms with a small number of external characters (Cutler 1994; Rice 1993). These non-segmented worms have a sac-like trunk and a retractable introvert. Their taxonomic rank is still controversial, and recent phylogenomic analyses recognized Sipuncula as an early branch within the annelid radiation (Weigert et al. 2014, 2016).

    From the other side, sipunculans occur widely along oceans, from polar to the tropical seas. Their bathymetric range is also extensive from the intertidal flats down to the abyssal depth. The world’s deep-sea sipunculan fauna has been studied insufficiently. The most recent revision listed only 22 species of sipunculans from depths greater than 500 m (Saiz et al. 2018). This also largely applies to the NW Pacific (NWP) (Maiorova and Adrianov 2017). Most of the available collections, including those from the Kuril–Kamchatka Trench (KKT) area, were made by trawling during a series of expeditions on the renowned RV Vityaz in the 1950s–1960s (Murina 1957, 1958, 1961, 1964, 1971). Only five records of sipunculans had been sampled from depths exceeding 2,000 m before the RV Vityaz expeditions. Among these are Nephasoma (Nephasoma) flagriferum (Selenka, 1885) was sampled by Challenger in 1875, two records were sampled by the Siboga Expedition in the Indo-Malayan Archipelago (Sluiter 1902) and the eurybathic N. (N.). eremita (Sars, 1851) was obtained by RV Gagara in the Bering Sea at the depth of 3,867 m (Makarov 1950).

    Recently, more species were collected by several further expeditions, with the most extensive collections made during scientific cruises of several Russian and German research vessels in the NWP (Maiorova and Adrianov 2013, 2015, 2017, 2018). The greatest contribution to the description of museum material and the inventory of the NWP sipunculan fauna was made by V.V. Murina, who published a reasonably detailed key to sipunculans of the arctic and boreal waters of Eurasia (Murina 1977). All data on the world’s sipunculan fauna available at that time were reviewed by Stephen and Edmonds (1972) who recognized 320 sipunculan species. Despite the efforts of researchers, detailed descriptions of live worms are absent because of the poor condition of the bottom-trawl material. Moreover, the degree of intactness and the quality of the preserved material do not allow genetic methods to be used for ascertaining the taxonomic status of some closely related species, which is important in the case of the variability of many morphological characters even within one species. Many revisions of the individual taxa of sipunculans undertaken in the 1980s have substantially hampered the use of the previously published taxonomic keys (Cutler and Cutler 1982, 1985, 1986; Cutler et al. 1983). In 1994, Cutler published a new overall review of this group and a new key to sipunculans of the world, in which he reduced many species, among them those described by Fisher, Murina and Sato from the North Pacific, to synonymy and the total number of species from 320 to roughly 150 (Cutler 1994). Unfortunately, this very valuable and important book lacks illustrations of most species, thus hindering its use as a field guide. Nevertheless, well-illustrated papers on the sipunculan fauna of some areas of the western Pacific appeared later, which substantially helped the identification of common species of sipunculans (Adrianov and Maiorova 2010; Morozov and Adrianov 2001; Cutler 1994; Cutler et al. 2004; Maiorova and Adrianov 2013, 2015; Pagola-Carte and Saiz-Salinas 2000). In recent years, interest in the NWP sipunculan fauna has increased in connection with a series of deep-sea expeditions that have been conducted in this region using state-of-the-art technology for the collection of biological material, including underwater robotic vehicles (Adrianov et al. 2013, 2016). These investigations showed that even at relatively low species richness, the sipunculans are an abundant group of deep-sea benthos in all seas of the Russian Far East, including abyssal and ultra-abyssal depths (Maiorova and Adrianov 2013, 2015, 2018). Analysis of previously published, museum and our own material from deep-water samples showed that 11 valid species of sipunculans are reliable records from depths below 2,000 m in the NWP. Some species were also known from less deep waters of the Pacific Ocean.

    Several species have only been reported from their type localities. Some of these have been synonymized with other, more widespread, species or are now regarded Incertae sedis or species inquirenda (Cutler 1994). The majority of sipunculan species have large reported distribution ranges. This view of generally wide geographic distributions is supported by the presence of free-swimming and long-lived planktotrophic larvae able to travel huge distances via oceanic currents and could have allowed some sipunculan species to colonize the entire depth range from the intertidal zone to the abyssal plains and deep-sea trenches (Hall and Scheltema 1975). Recently, molecular data has challenged the notion of widely distributed sipunculan species by revealing significant genetic differences among geographically separated populations, leading to the detection of “cryptic” (i.e., morphologically unrecognizable but genetically distinct) or “pseudo-cryptic” (i.e., morphologically and genetically distinct but lumped together in the taxonomic literature) species (Schulze et al. 2019). These include Apionsoma misakianum Ikeda, 1904 (see Staton and Rice 1999), Sipunculus nudus Linnaeus, 1766 (see Kawauchi and Giribet 2014), Phascolosoma perlucens Baird, 1868 (see Kawauchi and Giribet 2010), Phascolosoma agassizii Keferstein, 1866 (see Schulze et al. 2012, Johnson et al. 2016, Johnson and Schulze 2016), Themiste pyroides (Chamberlin, 1919) (see Schulze et al. 2012), and Thysanocarida nigra (Ikeda, 1904) (see Schulze et al. 2012). Species newly recognized on a molecular level are not formally described yet. The populations of previously largely synonymized sipunculans G. (Golfingia) margaritacea (Sars, 1851), N. (N.) minutum (Keferstein, 1862) and N. (N.) diaphanes (Gerould, 1913), as well as some others, can also be revised in future.

    2. Objectives

    In this chapter we are providing a review of the biogeography of the deep-sea Sipuncula of the NW Pacific Ocean (NWP).

    3. Material and Methods

    The data used herein represents a final compilation of all the works published previously by Murina (1964, 1971, 1977) and Maiorova and Adrianov (2013, 2015, 2017, 2018) on the Sipuncula group. Distribution of all sipunculan species recorded in the NWP at a depth below 2,000 m from 40 to 60°N and between 120 and 180°E are displayed in Map 1.

    Map 1.

    Distribution of deep-sea sipunculans in NWP.

    4. Results

    4.1. Family Golfingiidae Stephen & Edmonds, 1972

    Genus Golfingia Lankester, 1885

    Golfingia (Golfingia) anderssoni (Théel, 1911)

    (Figure 1 A)

    Figure 1.

    (A) Golfingia anderssoni Bar, 10 mm., (B) Golfingia margaritacea margaritacea Bar, 10 mm., (C) Golfingia muricaudata Bar, 10 mm., (D) Nephasoma abyssorum abyssorum Bar, 10 mm., (E) Nephasoma diaphanes diaphanes Bar, 10 mm., (F) Nephasoma diaphanes corrugatum Bar, 10 mm., (G) Nephasoma sp1 Bar, 10 mm., (H) Nephasoma sp2 Bar, 10 mm., (I) Phascolion lutense Bar, 10 mm, (J) Phascolion pacificum Bar, 10 mm.

    Diagnosis. Medium sized sipunculans (trunk no longer than 85 mm). Only juveniles may have hooks on introvert. Tentacular crown around mouth with an array of digitiform tentacles. External midregion of trunk wall smooth with minute papillae. Worms have а caudal appendage and distinctive wart-like papillae covering an area about 65-90% of the distance toward the posterior end of the trunk. In this they are strikingly similar to N. (N.) flagriferum. Nephridia opening anterior to the anus.

    Biogeographical remarks. Most species of subgenus Golfingia inhabit cold waters at depths of 2-6,800 m. Exceptions are also known, so G. (Spinata) pectinatoides Cutler & Cutler, 1979 lives in tropical coral sands in the Indo-West Pacific (IWP). A similar habitat is occupied by G. (G.) vulgaris herdmani (Shipley, 1903) in shallow Indian Ocean waters and around Australia, as well as some populations of G. (G.) elongata (Keferstein, 1862) are recorded in intertidal warm-temperate waters. Two endemic species are scattered over the NW Atlantic (G. (G.) iniqua (Sluiter, 1912)) and South Africa (G. (G.) capensis (Teuscher, 1874)). Two species described by Murina based on single records come from East Africa (G. (G.) mirabilis Murina, 1969)) and the NW Pacific (G. (G.) birsteini Murina, 1973)) (Murina 1969, 1973).

    The deep-water species, G. (G.) anderssoni commonly occur in the Atlantic and Pacific oceans. This species has been collected from almost all Antarctic waters except the Bellingshausen and Amundsen Seas and the distribution of the species is mainly restricted to the southern hemisphere at depths of 75-1,880 m (Cutler 1994; Saiz Salinas 1995). Although some other isolated records exist and in NWP, it is found in the Philippine Sea (3,150 m) and near KKT at depths of 5,739 and 6,135 m. This species belongs to the large sipunculan family Golfingiidae, which has many cold deep-water representatives in the world oceans (Murina 1975; Cutler 1994; Saiz Salinas 2014, 2018). Presence of a long caudal appendage may be a physiological pre-adaptation to the deep-water habitat.

    Golfingia (Golfingia) margaritacea (Sars, 1851) (Figure 1 B)

    Diagnosis. Medium sized smooth-skinned sipunculans, commonly 30-90 mm long, but may be up to 150 mm long. Small hooks have been seen only in a few small shallow-water individuals and juveniles. The number of unpigmented tentacles (15-30) varies with the size of the worm. The contractile vessel without swellings and branches, but may have villi in some shallow-water populations.

    Biogeographical remarks. This very widely distributed species is found in the Atlantic, Arctic, Southern and Pacific oceans. The species is unknown from the Indian Ocean and Mediterranean Sea. In the Sea of Okhotsk, this species is the most abundant found and has a high biomass (Maiorova and Adrianov 2013). In the Sea of Japan, this species was previously known from the Tatar Strait and Sakhalin Island, north to Tsushima Strait in the south, alongside the Korean, Japanese and Russian coasta as well as in the middle part of the Sea of Japan. The depth range is 1–5,300 m, but most specimens have been collected from depths of less than 300 m (see Cutler 1994). Furthermore G. (G.) margaritacea has a confusing nomenclatural history after Cutler and Cutler (1987) synonymized several varieties, forms, or subspecies to only two subspecies. Now rather abundant populations of G. (G.) margaritacea across the world oceans, are representing a suitable material for exploring further the cosmopolitan concept on sipunculans.

    Golfingia (Golfingia) muricaudata (Southern, 1913)

    (Figure 1 C)

    Diagnosis. Small- to medium-sized elongated, cylindrical, with nipple-like tail, worms (up to 70 mm in length). Tentacular crown with an array of 8–10 short transparent non-pigmented tentacles, arranged in a single row around the mouth. Two reddish eyespots visible. Anterior introvert with highly packed large papillae. Small hooks (20 μm) observed only in juveniles. Papillae on trunk are randomly distributed, tail covered by minute tall papillae. The nerve cord ends anterior to the tail. Specimens from the Kuril Basin differ from specimens from the abyssal plain near the Kuril-Kamchatka Trench by the length of tail (8% vs 15%) (Maiorova and Adrianov 2015).

    Biogeographical remarks. This mainly deep water species is found in the Atlantic, Indian and Pacific oceans. The depth range is 60–6,860 m, but most specimens have been collected from depths of more than 2,000 m (see Cutler 1994). In the North Pacific, it has been reported from British Columbia, around the Bering Sea, and from the Bering Sea to Japan (including the Kuril Basin of the Sea of Okhotsk) (Maiorova and Adrianov 2018). In the North Atlantic (near Ireland) and Southern Ocean (Bouvet Island), it occurs at depths of 150–1,081 m, while in the NW Pacific this species is noted at depths of 2,959–6,860 m (Murina 1964; Maiorova and Adrianov 2015).

    Golfingia (Golfingia) vulgaris vulgaris (de Blainville, 1827)

    Diagnosis. Small- to medium-sized worms (very few exceed 30 mm in length). Tentacular crown around mouth with an array of digitiform tentacles, whose number and complexity increase with age within species of this genus. Hooks (up to 150 μm) irregularly arranged. Both ends of the trunk are distinct – dark brown or black and heavily papillated – while the mid-trunk is smooth and whitish. The nephridia open anterior to the anus. Although four retractors are the norm, worms with only three have been noted (Cutler et al. 1984 and own observation).

    Biogeographical remarks. This aptly named cosmopolitan species is found in the NE Atlantic Ocean including Greenland, Scandinavia, and the British Isles, and into the Mediterranean, Adriatic, and Red seas; south to the Azores, Canary Islands, Cape Verde Islands, and West Africa; the Indian Ocean off South Africa and Zanzibar; the Pacific Ocean in the Kuril-Kamchatka Trench, Japan, Malaya, Singapore, and one record (Frank 1983) off British Columbia (the only one from the eastern Pacific). The depth range is 5-2,000 m, but specimens from depths greater than 500 m are rare (Cutler 1994). There is one very deep record: from 5,853 m in the KKT (Murina 1977).

    Genus Nephasoma Pergament, 1940

    Nephasoma (Nephasoma) abyssorum abyssorum (Koren and Danielssen, 1875)

    (Figure 1 D)

    Diagnosis. Small- to medium-sized worms, with trunk 10-30 mm in length. Tentacular crown around mouth with one row of digitate tentacles. Dark hooks (50–150 µm) may be spirally arranged, or scattered at distal part of introvert. Two nephridia open at the level of the anus.

    Biogeographical remarks. With nine species occurring at depths greater than 4,000 m and 21 at depths greater than 1,000 m, Nephasoma is clearly deep water genus. Of the six remaining intertidal and shelf species, three have been collected often ( N. (N.) minutum, N. (N.) rimicola (Gibbs, 1973), and N. (N.) schuttei (Augener, 1903)), with the remaining three only collected once. A few eurybathyal species fit both categories: N. (Cutlerensis) rutilofuscum (Fischer, 1916), 1–1,500 m; N. pellucidum, 1–1,600 m; N. (N.) confusum (Sluiter, 1902), 4–4,300 m; and N. (N.) eremita (Sars, 1851), 20–2,000 m (Cutler 1994).

    The richest fauna of Nephasoma inhabit the Atlantic Ocean (16 species). Five species N. (N.) abyssorum abyssorum, N. (N.) capilleforme (Murina, 1973), N. (N.) diaphanes corrugatum Cutler & Cutler, 1986, and N. (N.) eremita live throughout the Atlantic and in the Pacific, and three N. (N.) confusum, N. (N.) diaphanes diaphanes and N. (N.) pellucidum pellucidum (Keferstein, 1865) are found in these two oceans plus the Indian Ocean (Murina 1977; Cutler 1994).

    Of the 13 species living in the Pacific Ocean, two (N. laetmophilum (Fischer, 1952) and N. vitjazi (Murina 1964) are known only from the original descriptions (Fisher 1952; Murina 1964). Of the seven species that have been collected in the Indian Ocean, two ( N. filiforme (Sluiter, 1902) and N. tasmaniense (Murina, 1964) are known only from the original descriptions (Sluiter 1902; Murina 1964). Ten Nephasoma species live in the Southern Ocean (Edmonds 1969; Saiz Salinas 1995, 2014; Cutler et al. 2001). The Arctic Ocean is only inhabited by five species of Nephasoma, but all are common in the North Atlantic and the North Pacific, and elsewhere as well (Pergament 1946; Murina 1977; Kędra and Murina 2007; Kędra and Włodarska-Kowalczuk 2008; Kędra et al. 2018).

    The deep-water species N. (N.) abyssorum abyssorum is found in the NE Atlantic and Arctic oceans, and with single records in the SE and NW Atlantic. In the NW Pacific, and the Mediterranean Sea, it is found at bathyal to abyssal depths (500–5,300 m).

    Nephasoma (Nephasoma) diaphanes diaphanes (Gerould, 1913)

    (Figure 1 E)

    Diagnosis. Small-sized worms, with trunk 2–9 mm in length. Trunk whitish, opaque or golden brown, smooth, with hyaline cuticle and flattened papillae. Smooth thickened cuticular collar like pseudoshield encircle anterior trunk, and posterior pseudoshield surrounding posterior extremity of trunk. Tentacular crown composed of two primary tentacles and non-pigmented tentacular lobes around mouth present. Small scattered hooks (30–40 μm) on distal introvert. Cupola-shaped papillae located between hooks. Short nephridia open at anus level. This species often lives in foraminiferan tests, small polychaete tubes, or scaphopod shells.

    Distribution. Considered a cosmopolitan species in cold water, most often found at bathyal and abyssal depths (down to 6,860 m). In the NW Pacific the species occurs in the Kuril Basin and along the Pacific side of the Kuril Islands with high abundance at most localities.

    Together with G. (G.) margaritacea, this species has a confusing taxonomic story after many species across the world ocean were transferred by Cutler and Cutler (1986) to N. (N.) diaphanes. Immature members of other species are easily mistaken for N. (N.) diaphanes diaphanes, so the literature has some unfortunate but unavoidable zoogeographical “noise”.

    Nephasoma (Nephasoma) diaphanes corrugatum (E. B. Cutler and N.J. Cutler, 1985)

    (Figure 1 F)

    Diagnosis. Pear shaped to cylindrical; trunk usually 5–10 mm long (occasionally 20–30 mm). The skin is tan to grayish brown, translucent to opaque, with irregular, wavy, zigzag longitudinal epidermal ridges on the introvert base and the anterior part of the trunk. Often the papillae on the posterior end are darker than the surrounding skin. Hooks small (20– 30 µm), scattered, pale, triangular hooks. The tentacular crown consists of six to eight short lobes plus two longer dorsal tentacles. This species often lives in foraminiferan tests, and small polychaete tubes.

    Biogeographical remarks. Broad latitudinal range from the Atlantic and Pacific oceans, plus the Mediterranean and Red seas. Collected at depths ranging from 80 to 7,123 m, most occur >1,000 m. This species was found together with N. (N.) d. diaphanes along both slopes of the Kuril-Kamchatka Trench and adjacent abyssal (Maiorova and Adrianov 2015, 2015; Murina 1958).

    Nephasoma sp1 in Maiorova & Adrianov, 2018 (Figure 1 G)

    Diagnosis. Medium-sized worms 80 mm in length. Tentacular crown is around mouth with 30 non-pigmented tentacles. Introvert behind tentacular apparatus is covered by irregular shaped oval papillae, hooks absent. Trunk whitish or yellowish, lustrous; flattened papillae randomly distributed; some areas covered with black particles. Nephridia open minute posterior to anus.

    Biogeographical remarks. Known from a single locality in the Sea of Okhotsk at 3,200 m depth (site #11 of SokhoBio expedition).

    Nephasoma sp2 in Maiorova & Adrianov, 2018 (Figure 1 H)

    Diagnosis. Small-sized worms, with pyriform trunk 9 mm in length. Trunk with irregular, zigzag, longitudinal epidermal ridges on introvert base, anterior and posterior parts of the trunk. Two tentacles and short nonpigmented tentacular lobes around mouth present. No hooks found behind tentacular apparatus, this area only covered with highly cuticularized tall papillae with radiating ridges in cortical layers of cuticle. Nephridia open minute anterior of anus level.

    Biogeographical remarks. Known from single locality at the landward slope of KKT at 4,700 m depth.

    Genus Phascolion Théel, 1875

    Subgenus Phascolion (Montuga) Gibbs, 1985

    Phascolion (Montuga) lutense Selenka, 1885

    (Figure 1 I)

    Diagnosis. Medium-sized worms (up 50 mm in length). Inhabitants tubes composed of sediment, mucous and own descended cuticle. Tentacular crown around mouth with only short non-pigmented folds (lobes). Hooks present in narrow zone behind the tentacles on distal part of introvert, but ill-defined in rough cuticle (50–70 µm in height). Dark cap on the front trunk end consists of densely arranged tall finger-shaped brownish papillae. The trunk is smooth with flat rounded or elliptical papillae without hardened edge randomly distributed around trunk (400 µm outer border, inner part 140 µm), but not holdfast papillae. Tall and brown papillae present at anterior and posterior ends of trunk. Body wall musculature continuous. Ventral nerve cord ends before posterior end (retractor roots origin) (3/4 of trunk length) separates into two fine branches. Single large left brown-purple nephridium opens at anus level and not attached to body wall. Retractor muscles originate at 95% to posterior end of trunk, fused in column with three or four separate unequal origins.

    Biogeographical remarks. Together with Nephasoma, the genus Phascolion are amongst the most well distributed and most species-rich genera of sipunculans. With almost equal numbers of species (14 and 12, respectively), they inhabit both shelf waters (1–300 m) and deeper waters, Phascolion is the deep-water genus. Six species are known from both shelf and continental slope depths (300–3,000 m), including P. (Isomya) hedraeum Selenka & de Man, 1883 (7–4,600 m) and the eurytopic P. (Phascolion) strombus strombus (Montagu, 1804) (1–4,030 m). Six taxa are known only from slope and deeper waters (300–6,900 m), but only P. (M.) lutense and P. (M.) pacificum Murina, 1957, occur in significant numbers at abyssal depths (>4,000 m) as well as on the continental slope (Murina 1971, 1977). Three species of Phascolion have significant populations in all three of the world’s oceans, P. (I.) strombus strombus being the most widely distributed and eurytopic. Two deep-water species, P. (M.) lutense and P. (M.) pacificum, are close seconds throughout the northern and southern Atlantic and Pacific. Aside from the three widespread eurytopic deep-water species noted above, the eastern half of the Pacific Ocean is almost devoid of Phascolion. A single specimen of P. (P.) bogorovi Murina, 1973, was collected from the Peru-Chile Trench, and is the only one known from this part of the ocean (Murina 1973).

    The deep-water species P. (M.) lutense is common in the Atlantic, Indian and the Pacific oceans; found at depths from 1,800 to 6,860 m (Cutler 1994). In the NWP it was collected at depths ranging from 4,690 to 6,860 m (Murina 1961, 1969, 1971).

    Phascolion (Montaga) pacificum Murina, 1957 (Figure 1 J)

    Diagnosis. Small to medium-sized worms (5–25 mm in length). Tall conical brown papillae present at anterior and posterior ends of trunk. Introvert with dark conical papillae in proximal part. Often inhabit foraminifera tubes. Rounded or elliptical (holdfast) papillae with hardened edge randomly distributed over trunk (50–60 mm in diameter and 45–50 mm in height). Tentacles present only as short non-pigmented folds around mouth. Hooks present (30–35 mm). Ventral nerve cord ends at the ¾ of trunk length. Single (left) medium sized brown-purple nephridium opens at the anus level. Retractor muscles originate at 95% to the posterior end of the trunk, fused in column with one, two or three separate unequal origins.

    Biogeographical remarks. This species is described from both the Japanese and Kuril-Kamchatka Trench and is particularly distinguished from the only other representative of this subgenus P. (M.) lutense by the presence of holdfast papillae. This bathyal and abyssal species (300–6,860 m) is widespread in the NW and SW Pacific and also in the northeastern (up to 57˚N), southeastern, and South Atlantic, and the sub-Antarctic Indian Ocean. The only records at lower latitudes are from the Peru-Chile Trench (5,760–6,860 m) and 28˚N (1,760 m) in the eastern Atlantic (Cutler 1994; Murina 1957, 1961; Saiz Salinas 1993). Also recently described subspecies of Phascolion (M.) pacificum denticulatum Saiz et al., 2015) is recorded from shallow waters (15–20 m deep) off Malvan and Ratnagiri in India. This is the first record of any Phascolion species for all the Indian coasts (Saiz et al. 2015).

    4.2. Family Phascolosomatidae Stephen & Edmonds, 1972

    Genus Apionsoma Sluiter, 1902

    Apionsoma (Apionsoma) murinae murinae (Cutler, 1969)

    Diagnosis. Small-sized sipunculans less than 10 mm in trunk length. Introvert 10–15 times longer than trunk. Hooks recurved and with series of basal spinelets, organized in rings Distinctive mammiform papillae at the posterior end of the trunk. Contractile vessel without true villi and any swellings. Spindle muscle attached posteriorly. A pair of unilobed nephridia.

    Biogeographical remarks. Two of four valid species of Apionsoma species are deep water taxa (Apionsoma (Apionsoma) murinae murinae and A. murinae bilobatae (Cutler, 1969)) occur in the Atlantic and Pacific oceans at bathyal to abyssal depths (300–5,200 m). According to Murina (1964), in the Pacific, this species occurs in the Bering Sea and the Peru-Chile Trench, and in other deep waters of the southern Pacific. The second taxon is also found in the Mediterranean Sea and on both sides of the Indian Ocean at shallow to continental slope depths (200–1,200 m) (Cutler, 1994). The three remaining species (A. (A.) misakianum (Ikeda, 1904), A. (A.) trichocephalus Sluiter, 1902, and A. (Edmondsius) pectinatum (Keferstein, 1867)) are also widespread, but in shallow, warm waters. The first is known from the Indian Ocean and both sides of the Pacific, but only the western Atlantic, including the Gulf of Mexico. The second co-occurs in warm-water sandy habitats over most of this range plus the eastern Atlantic Ocean. The third is less common but circumtropical and has been collected on both sides of all three oceans (Cutler 1994).

    5. Discussion

    The most ubiquitous NWP sipunculan species is N. (N.) diaphanes corrugatum. Other widespread sipunculan species are N. (N.) diaphanes diaphanes, G. (G.) muricaudata and Also, P. (M.) lutense Also, N. (N.) d. corrugatum and N. (N.) d. diaphanes comprise 30% and 25%, respectively, of the total records of sipunculans in the deep area of the NW Pacific. Both species are present along almost the entire Kuril-Kamchatka Trench, at the adjacent abyssal plain, in the Kuril Basin of the Sea of Okhotsk and the Bering Sea, and only in the Sea of Japan, they have not been recorded. Several other common species (G. (G.) muricaudata, G. (G.) margariatcea margaritacea, P. (M.) lutense and P. (M.) pacificum) were sampled from widely scattered locations with a high number of specimens per sample. The remaining species (N. (N.) abyssorum, G. (G.) anderssoni, G. (G.) vulgaris vulgaris, Nephasoma sp1, Nephasoma sp2 and Apionsoma (Apionsoma) murinae murinae) are represented by few specimens, and mostly from single locations. Concerning the vertical distribution, most specimens of G. (G.) m. margaritacea were found at depth range 1,700–3,990 m; other abundant deep-sea sipunculan species (N. (N.) d. diaphanes, G. (G.) muricaudata, G. (G.) margaritacea, P. (M.) lutense and P. (M.) pacificum) were found at abyssal depths up to 6,800 m. The most dense sipunculan populations (N. (N.) d. corrugatum, P. (M.) lutense and P. (M.) pacificum) were found at depths of 6,800 m on the eastern slope of KKT. The deepest record of sipunculans in the selected area belongs to N. (N.) d. corrugatum from 7,123 m in the KKT.

    Acknowledgments

    Hanieh Saeedi is kindly acknowledged for her efforts in bringing scientists together to discuss the deep-sea NWP biogeography, and for the inviting us to this publication and mapping the sipunculan records. This paper was published with a financial support of the “Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean project (Beneficial project)”. Beneficial project (grant number 03F0780A) was funded by Federal Ministry for Education and Research (BMBF: Bundesministerium für Bildung und Forschung) in Germany. The authors gratefully acknowledge the financial support of the National Scientific Center of Marine Biology FEBRAS and Russian Foundation of Basic Researches (Grant 18-04-00973), which has made this work possible. We are grateful to Prof. Angelika Brandt and Dr. Marina Malyutina for the coordination of deep-sea projects in the NWP. We would also like to thank Rachel Downey for reviewing and English proofreading this chapter.

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    Chapter 10. POLYCHAETA: A REVIEW ON THE DEEP-SEA BENTHIC POLYCHAETES ALONG THE NW PACIFIC

    A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch of Russian Academy of Sciences, Vladivostok 690041, Russia

    1. Introduction

    Generally, polychaetes are the most abundant and diverse invertebrate group in marine environments worldwide. They occur in all substrates from the intertidal to hadal depths, displaying a wide variety of life forms, and constitute an important food base for many other animals. Of the macrofaunal taxa, polychaetes are often known to be dominant in deep-sea environments, including hydrothermal vents and cold seeps (Hessler and Jumars 1974; Rouse and Pleijel 2001; Paterson et al. 2009; Reuscher et al. 2009; Kongsrud et al. 2017).

    The deep-sea Japan Basin, with a maximum depth of around 3,700 m, is located in the north-western part of the Sea of Japan and is isolated from the adjacent deep-sea areas by shallow straits (La Perouse Strait and Tatarsky Strait) (Talley et al. 2004). The deep-sea fauna of the Sea of Japan is considered to be rather poor and composed of eurybathic species found in adjacent high-boreal regions (Derjugin 1939; Zenkevitch 1963). The earliest investigations of the deep-sea fauna of the Sea of Japan found only eight polychaete species from depths of 1,000–3,900 m (Annenkova 1937, 1938), including the polynoid species Harmothoe derjugini (Annenkova, 1937), which was considered a truly endemic deep-sea species of the Sea of Japan (Mokievsky 1954). Later, Levenstein (1969) reviewed the data on deep-water polychaete fauna of the Pacific Ocean and listed about 25 polychaete species inhabiting depths greater than 2,000 m in the Sea of Japan.

    The deep-water Kuril Basin, bounded by 3,000 m isobaths, is located in the deepest southwestern part of the Sea of Okhotsk, and is characterized by a low oxygen concentration. It is separated from the Pacific Ocean by the Kuril Island archipelago and is connected to the ocean through several straits of bathyal depths (Bussol Strait, max. depth of 2,318 m, and Kruzenstern Strait, max. depth of 1,920 m) (Zenkevitch 1963; Shuntov 2001; Tyler 2002). During the 20th century, in the course of extensive biological surveys, the polychaete fauna of the northern and central parts of the Sea of Okhotsk was relatively well studied (Usсhakov 1950, 1953), while the deepest southwestern part of the Sea of Okhotsk remained practically unstudied, since only five abyssal stations were sampled from the Kuril Basin. Among invertebrates collected from the abyssal depths of the Kuril Basin deeper 3,000 m only three polychaete species (Notomastus latericeus Sars, 1851 and Maldane sarsi Malmgren, 1865 considered to be eurybathic and distributed worldwide, and Lumbrineris abyssicola Uschakov, 1950 considered to be truly abyssal and endemic to the Sea of Okhotsk) were recorded (Usсhakov 1950, 1953).

    The Kuril-Kamchatka Trench (KKT) extends from the southeast coast of Kamchatka to the Japan Trench, east of Hokkaido, and separates the abyssal seafloor of the NW Pacific Basin from the Kuril Islands slope and from the Kuril Basin in the Sea of Okhotsk. The abyssal KKT area is considered one of the most productive regions in the World Ocean (Sokolova 1976, 1981). The earliest investigations of benthic fauna of the KKT performed during six biological Vityazs' expeditions revealed high diversity and species richness of the deep-sea macrobenthos in the North Pacific (Levenstein 1961, 1969; Zenkevitch 1963; Belyaev 1983; 1989). Polychaeta, Bivalvia and Isopoda were known to be dominant taxa in deep-sea samples (Hessler and Jumars 1974). For the Pacific Ocean, Levenstein (1969) listed 204 bathyal and abyssal species of polychaetes, including 13 species from the KKT at depths of 5,070–9,950 m (RV Vityaz collections). But many samples collected by the RV Vityaz and other Russian research vessels are still unstudied and apparently many bathyal and abyssal polychaete species new to science remain undescribed (Kupriyanova et al. 2011).

    2. Objectives

    The present chapter summarizes published data on deep-sea benthic polychaetes found during the Russian-German deep-sea expeditions, and reviews literature data on polychaete species occurring deeper 2,000 m in the NW Pacific area.

    3. Material and Methods

    The four deep-sea areas of the NW Pacific: Sea of Japan, Sea of Okhotsk, abyssal plain adjacent to the Kuril-Kamchatka Trench (KKT area), and Kuril-Kamchatka Trench (KKT), were studied during the Russian-German and German-Russian sampling campaigns from 2010 to 2016. During the SoJaBio (Sea of Japan Biodiversity Studies) expedition 13 stations along four transects were taken in the northwestern sector of the Sea of Japan (Japan Basin) at depths of 455–3,666 m. During the SokhoBio (Sea of Okhotsk Biodiversity Studies) expedition eight stations were sampled across the Kuril Basin of the Sea of Okhotsk at depths of 1,676–3,366 m, one station in the Bussol Strait at depths of 2,327–2,358 m, and two stations at the western abyssal slope of the KKT at depths of 3,347–5,009 m. From the abyssal plain of the KKT area (4,830–5,780m) and from the abyssal and hadal depths of the KKT (5,120–9,584 m) twelve and eleven stations, respectively, were sampled during the expeditions KuramBio I and KuramBio II (Kuril-Kamchatka Biodiversity Studies).

    Different types of modern gears were used during the expeditions: an epibenthic sledge (EBS), an Agassiz trawl (AGT), and a Box-Corer (BC, sampling area of 0.25 m2). Sledge operation procedure is described in Brandt et al. (2019). On deck, the samples were washed with ice-cold water and sieved through 300-µm mesh screens. Samples from the first deployment of each station were fixed with pre-cooled 96% ethanol. Samples from the second deployment were fixed with 4% formaldehyde and later transferred to 75% ethanol. Collected samples were sorted either on board or later in the laboratory.

    In this article, we also consider literature data on polychaete species occurring below 2,000 m in the NW Pacific area, limited between approximately 40 and 60 degrees North latitude and 120–180 degrees East longitude. The abyssal zone is generally defined as lying between 2,000 m and 6,000 m depth, and waters deeper than 6,000 m are treated as the hadal zone. Both zones are described mainly by their extremely uniform environmental conditions, as reflected in the distinct life forms inhabiting it.

    4. Results

    During the SoJaBio expedition more than 11300 polychaete specimens of 90 species belonging to 70 genera and 28 families were collected in the Japan Basin at depths of 470–3,431 m (Alalykina 2013). However, most specimens (5,406) and species (84) were sampled from the shallow station positioned on the continental slope of the Japan Basin at depths of 450–550 m. Species richness and polychaete diversity rapidly decreased with depth. At depths between 1,000–1,500 m 36 species were found, between abyssal depths of 2,500–2,700 m 14 species, and at depths greater than 3,300 m only eight species were registered. In total, only 18 polychaete species (5,928 specimens) were accounted in depths below 2,000 m in the Japan Basin (see abb. X in Table 1, own data).

    List of polychaetes recorded in the studied NW Pacific region at depths below 2,000 m (X – own data, L – literature records).

    Species Japan Sea Okhotsk Sea Bering Sea NW Pacific abyssal plain KKT Distribution Reference
    Phyllodocidae
    Austrophyllum sphaerocephalum (Levenstein, 1961) X L X, L Kuril Basin of the Okhotsk Sea, Kuril-Kamchatka Trench, Bering Sea, Pacific; 2,440–4,130 m Levenstein 1961; Uschakov 1972; Alalykina 2018
    Eteone sp. X
    Eteone vitiazi Uschakov, 1972 L Japan (off east of Honshu), Pacific; 5,475 m Uschakov 1972
    Eulalia cf. pacifica (Imajima, 1964) X L Kuril Basin of the Okhotsk Sea, off east of Japan, Pacific; 2,230–2,350 m Uschakov 1972; Alalykina 2018
    Eulalia gravieri Uschakov, 1972 L Japan (off east of Honshu), off Kamchatka Peninsula, Pacific; 1,641–3,265 m Uschakov 1972
    Eulalia sp. X X
    Eumida cf. angolensis Böggemann, 2009 X Angola Basin, Atlantic; 3,950–5,443 m Böggemann 2009
    Eumida nuchala (Uschakov, 1972) X L X Angola and Cape Basins, Atlantic; Japan (east of Honshu), Pacific; 3,704–5,475 m Uschakov 1972; Böggemann 2009
    Eumida sp. X
    Lugia abyssicola Uschakov, 1972 X L South-Sandwich Trench, Antarctic; Japan (Hokkaido), California, Pacific; 4,200–5,475 m Uschakov 1972; Levenstein 1975
    Mystides caeca Langerhans, 1880 X Off north Carolina, Angola,Cape and Guinea Basins, Atlantic; off California, Pacific; 102–5,496 m Blake 1994a; Böggemann 2009
    Mystides schoderae Uschakov, 1972 L Japan (off Hokkaido), Pacific; 3,095–5,800 m Uschakov 1972
    Mystides sp.nov. X X X
    Paranaitis bowersi (Benham, 1927) X Ross Sea, Antarctic; 219–1,837 m Uschakov 1962; Kato and Pleijel 2003
    Paranaitis sp. X
    Paranaitis uschakovi Eibye-Jacobsen, 1991 X Japan (east of Honshu), Pacific; 45–598 m Kato and Pleijel 2003
    Protomystides levensteinae Uschakov, 1972 X L Kuril Basin of the Okhotsk Sea, Aleutian and Mariana Trenches, Pacific; 4,549–5,740 m Uschakov 1972
    Protomystides orientalis Uschakov, 1972 X X Japan (east of Honshu), north New Zealand, Pacific; 598–1,225 m Uschakov 1972
    Pseudomystides rarica (Uschakov, 1958) X X, L X, L South-Sandwich Trench, Atlantic; Japan (off Hokkaido), Bonin Islands, Kuril-Kamchatka Trench, Kermadec Trench, Pacific; 1,125–5,070 m Uschakov 1972; Levenstein 1975
    Pseudomystides sp.nov. X
    Sige cf. brunnea (Fauchald, 1972) X X North California, Pacific; 1,110–3,000 m Blake 1994a; Pleijel 1990