Review of Ostracoda (Crustacea) living below the Carbonate Compensation Depth and the deepest record of a calcified ostracod

Progress in Oceanography 178 (2019) 102144

Contents lists available at ScienceDirect

Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean

Review

Review of Ostracoda (Crustacea) living below the Carbonate Compensation Depth and the deepest record of a calcified ostracod

T

Simone N. Brandãoa,b,c, , Mario Hoppemad, Gennady M. Kameneve, Ivana Karanovicf,g, Torben Riehlh, Hayato Tanakai, Helenice Vitalb, Hyunsu Yoof, Angelika Brandth,j ⁎

a

Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal Rural do Semi-Árido, Centro de Ciências Biológicas, Av. Francisco Mota, 572, Bairro Costa e Silva, Mossoró, RN CEP 59.625-900, Brazil b Programa de Pós-Graduação em Geodinâmica e Geofísica, Laboratório de Geologia e Geofísica Marinha e Monitoramento Ambiental (GGEMMA), Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, Postbox: 1596, Natal, RN CEP 59072-970, Brazil c Programa de Pós-Graduação em Sistemática e Evolução, Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, Natal, RN CEP 59072-970, Brazil d Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Climate Sciences Department, Postfach 120161, 27515 Bremerhaven, Germany e National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Palchevskogo Street, 17, Vladivostok 690041, Russia f Department of Life Science, College of Natural Science, Hanyang University, Seoul 133-791, South Korea g Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, 7001 Hobart, Tasmania, Australia h Senckenberg Research Institute and Natural History Museum, Senckenberganlage 25, 60325 Frankfurt am Main, Germany i Tokyo Sea Life Park, 6-2-3 Rinkai-cho, Edogawa-ku, Tokyo 134-8587, Japan j Institute for Ecology, Evolution and Diversity, Goethe-University of Frankfurt, FB 15, Max-von-Laue-Str. 13, 60439 Frankfurt am Main, Germany

ARTICLE INFO

ABSTRACT

Keywords: Hadal Ostracoda Kuril-Kamchatka Trench Northwestern Pacific

Ostracods are small-sized crustaceans, which inhabit all aquatic ecosystems and, because they have a comprehensive fossil record, are important environmental and paleoenvironmental indicators. However several aspects of the ecology of modern species (the basis for the paleontological investigations) are still controversial. Previous authors have raised the hypothesis that benthic ostracods, because of their calcified carapaces, are unable to survive below the Carbonate Compensation Depth (CCD). Herein we test this hypothesis based on (1) ostracods newly collected from the Kuril-Kamchatka Trench at depths far below the CCD during the KuramBio II expedition; and (2) a compilation of all previously published records of (geologically) Recent deep-sea Ostracoda in regions deeper than 3500 m. The KuramBio II expedition provided hundreds of living, hadal ostracods from at least 30 species and 21 genera from thousands of meters deeper than the CCD in the Kuril-Kamchatka Trench region. Additionally, the KuramBio II expedition provided the deepest record (9307 m) of a living ostracod with calcified carapaces: specimens of the genus Krithe. Finally, the compilation of all published information on living ostracods show that a highly diverse assemblage both at high and low taxonomic levels (2 subclasses, 4 suborders, 25 families, 89 genera and at least 206 species) occur below 3500 m. Therefore, we conclude that contrary to previous beliefs, the new data from the Kuril-Kamchatka Trench and the compilation of the literature show that ostracods do live and are even sometimes abundant below the CCD.

1. Introduction 1.1. The Carbonate Compensation Depth in the world’s oceans Benthic Ostracoda are organisms with calcite valves that live on the seafloor and in the sediment. When considering the occurrence and distribution of ostracods, the state of calcite saturation on and near the seafloor is thought to be of utmost importance (e.g., Whatley, 1996;

Yasuhara et al., 2008; see discussion below). Generally, in upper water layers the ocean is supersaturated with respect to the carbonate (CO32–) and bicarbonate ion (HCO3−) and thus to calcite (and to other solid carbonates such as aragonite). Because of an increase of calcite solubility with pressure, the calcite saturation decreases almost monotonically with depth and at some depth (the calcite saturation depth) the ocean becomes undersaturated. At somewhat greater depths, calcite (e.g., from ostracod valve remains) starts to dissolve; the depth where

⁎ Corresponding author at: Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal Rural do Semi-Árido, Centro de Ciências Biológicas, Av. Francisco Mota, 572, Bairro Costa e Silva, Mossoró, RN CEP 59.625-900, Brazil. E-mail address: [email protected] (S.N. Brandão).

https://doi.org/10.1016/j.pocean.2019.102144

Available online 08 August 2019 0079-6611/ © 2019 Published by Elsevier Ltd.

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

the dissolution increases dramatically is called the lysocline. At the sea floor, in the sediments, calcite remains are deposited, but on the other hand this calcite (CaCO3) is dissolved due to the reaction CaCO3 + CO2 + H2O → Ca

2+

+

1.2. Life below the CCD The idea of a lifeless zone in deep oceans (including the ocean trenches, +6000m) prevailed in marine biology until the middle of the 20th century (Petterson, 1948; Belyaev, 1989). This idea was based on the assumption that the main factors limiting the distribution of life to depths greater than 6000 m is not only the extremely high pressure, but also the extremely low concentration of calcium carbonate (CaCO3) in the near-bottom water layer and sediments, which in turn should prevent many marine animals from building their skeletal structures (such as spicules, shells, or carapace). Furthermore, such animals should face problems associated with not only constructing, but also active maintaining and renewal of skeletons contrary to the CaCO3 concentration gradient, which tends to dissolve them (Belyaev, 1989). Thus, the phenomenon of “deep-sea rickets”, manifested as thinning and reduction in the degree of skeleton calcification, is known for many deep-sea dwelling organisms (Belyaev, 1989). However, a Swedish expedition aboard the Research Vessel Albatross in 1948 took a sample with benthic animals in the Puerto Rico Trench, from a depth of 7625–7900 m (Nybelin, 1951). In addition, a Russian expedition aboard Research Vessel Vityaz in 1949 sampled many species of benthic animals in the Kuril-Kamchatka Trench, from a depth of 8100 m (Ushakov, 1952). Both investigations proved that life exists in the oceans at depths greater than 6000 m. In their samples, various groups of animals, including those with strongly calcified shells, were present in abundance. For example, the largest hadal species of bivalves – Hyalopecten vityazi Kamenev, 2018, with its shell height of up to 40 mm – was found in a sample from a depth of 8100 m in the Kuril-Kamchatka Trench (Kamenev, 2018a). In subsequent deep-sea expeditions, benthic animals with both external and internal skeletons (crustaceans, echinoderms, and mollusks) were observed much deeper than the CCD in all the investigated oceanic trenches, up to the maximum depth of the World Ocean (Belyaev, 1989; Jamieson, 2015).

HCO3–

The Carbonate Compensation Depth or Calcite Compensation Depth (CCD) is defined as the depth horizon at which the calcite deposition rate equals the rate of dissolution. Consequently, because the dissolution impedes major accumulation on the seafloor, the content of solid carbonates at or below the CCD is very low, depending on the definition zero (Bickert, 2009), from 2 to 10 wt% (Emelyanov, 2005) or 20 wt% (Lee et al., 2000). Calcite can still exist below the calcite saturation depth and also below the CCD because its dissolution kinetics are relatively slow (Berner and Morse, 1974). Already in the 19th century, researchers noted the sharp depth boundary between calcareous and other kinds of sediments on the seafloor (e.g., Ben-Yaakov et al., 1974). In practice, the CCD separates pelagic red clays from carbonatic oozes (Emelyanov, 2005). In regions with sea floor depths of 6000–8000 m, the CaCO3 content in the upper layer of the sediments is usually less than 10% (Emelyanov, 2005). The position of the CCD depends on many factors, such as pressure, temperature, organic matter content in the sediment and consequently biological activity (which generates CO2 and favors the dissolution of CaCO3; see above reaction), the level of supply of CaCO3 to the sea floor (which is related to the primary productivity in the photic zone), closeness to the formation areas of deep-water masses (further away from the source region the water is richer in CO2, which favors the dissolution of CaCO3), shape and size of the calcite valves, and coatings. Due to the variability on biotic and abiotic factors, the CCD also varies worldwide by more than 5000 m, for example, in some regions of the Southern Ocean where the CCD lies close to the surface layer to some basins in the Atlantic, where it lies at 6000 m (Table 1 and references therein). In general, the CCD is deeper in the Atlantic (i.e., 4700–6000 m) than in the Pacific (3000–5500 m), Indian (3500–4500 m) and Southern oceans (0–4000 m). The CCD may lie on the continental shelf, -slope and -rise, in the abyss or, in deep oceanic trenches. Generally, however, the CCD mostly lies in the abyss and also in hadal environments. The hadal zone ranges from 6000 to +11,000 m depth and encompasses merely 2% (in area) of the benthic oceanic ecosystems, but includes the deepest 45% of the oceanic vertical depth range (Jamieson et al., 2010). In the southern hemisphere, the CCDs in the Atlantic, Indian and Pacific oceans are similar, because of the inflow and recirculation via the Antarctic Circumpolar Current of deep and bottom waters with relatively low CO2 content into all ocean basins. On the other hand, in the northern hemisphere the supply of low-CO2 deep waters (which are formed in the North Atlantic and Arctic oceans) to the Atlantic causes the CCD to be deeper in the Atlantic than in the other two oceans, where this supply is absent and the bottom waters are much higher in CO2 (Emelyanov, 2005). Adjacent to the coasts, the CCD tends to be shallower because of the higher primary productivity and consequently higher organic matter supply to the sediments and its remineralization there, which releases CO2, and in turn favors CaCO3 dissolution. Carbonatic deposition on the seafloor is a non-negligible carbon sink (e.g., in the Southern Ocean, Hauck et al., 2012), playing an important role in the carbon cycle on long geological time scales (e.g., Ben-Yaakov et al., 1974). In the current climate change debate, the carbonaceous sediments play an important role as well: the final sink for anthropogenic CO2 is the sedimentary carbonates. Sulpis et al. (2018) found that carbonate dissolution has already occurred in all ocean basins, particularly at places where bottom waters are enriched with anthropogenic CO2, like the North Atlantic and close to the Southern Ocean. Such processes also relate to ostracod remains on the seafloor.

1.3. Ostracoda and CCD Ostracods are mostly epi- and infauna crustaceans with calcite valves. Their occurrence and distribution is thought to be limited by the level of calcite saturation on and near the sea floor (e.g., Whatley, 1996; see discussion below). They are small-sized animals (mostly 0.3–1 mm), which inhabit virtually all kinds of aquatic ecosystems and also a few, very humid terrestrial environments (e.g., Brandão et al., 2019). Although most species are benthic deposit feeders, some marine ostracods are part of the plankton, where their shell has no calcification. The shell of the benthic species is, on the other hand, impregnated by calcite just after each mount. Due to these calcified carapaces, Ostracoda show an impressive fossil record since the Ordovician, which is among the most abundant and diverse in the animal kingdom (e.g., Brandão et al., 2019). Concerning the occurrence of ostracods in relation to the CCD, Whatley (1996) revised the available knowledge on fossil and (geologically) Recent, deep-sea Ostracoda in the light of their application to paleoenvironmental reconstruction (from millions of years to decades ago) and concluded that “hadal depths, being below the CCD, are barren of ostracods”. Boomer (1999) discussed the biogeography of Late Cretaceous and Cenozoic bathyal ostracods from the Pacific Ocean, and expressed support to the hypotheses that ostracods cannot survive below the CCD because of their calcite shells. The latter author also speculated that ostracods are incapable of migrating over the seafloor between seamounts that are shallower than the CCD but surrounded by abyssal depths below the CCD. Yasuhara et al. (2008) studied one living and 135 dead ostracods collected from 5030 to 5150 m depth in the eastern Atlantic Ocean, and considered the assemblage to be representative of the modern faunal assemblage living in the region. The authors concluded that ostracods inhabit environments near the CCD and this suggests that the CCD may 2

3

– N NW NW SE

SE

SW

SE

SE

SE

SE

SE

SE S

– W Central E S

Atlantic Atlantic Atlantic Atlantic Atlantic

Atlantic

Atlantic

Atlantic

Atlantic

Atlantic

Atlantic

Atlantic

Atlantic Atlantic

Atlantic Ocean Indian Indian Indian Indian Indian

Pacific Pacific Pacific Pacific Pacific

N W Equatorial Central Equatorial E Equatorial SW SE W Equatorial –

NW NE W Equatorial E Equatorial SW SE –

Atlantic Atlantic Atlantic Atlantic Atlantic Atlantic Atlantic

Indian Ocean Pacific Pacific Pacific

N/S

Ocean

– – – Philippine Basin –

Summary – – –

Summary – – – – –

Southeastern Adjacent (north) to the Polar Front

Guinea Basin

Cape Basin

Cape Basin

Cape basin

Cabo Verde and Canary basins

Brazilian Basin

Angola Basin

“other basins” North Northern North American Basin Southern North American Basin Angola Basin

– – – – – – –

Sea/region

3545 3952 3659 3731 3500

3500 3396 4372 4136

4107 4502 4142 4901 3842 3500

> 5000 > 5000

5400

5000

5000

5200

5700

4700

5500

4700 > 5000 5500 5900 5600

4901 5075 4552 5692 3900 4107 > 5000

min.

CCD (m)

Table 1 Depth of the Calcite Compensation Depth in different oceanic regions according to previous publications.

4207 4526 4275 4363 4500

5363 5376 4910 4688

6014 4992 4664 5363 4418 4500

– –

–

–

5100

–

–

4800

5600

6000 – 5600 6000 –

5271 5431 4982 6014 4460 4609 –

max.

Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Bickert (2009)

Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018)

Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Bickert (2009)

Schmiedl et al. (1997) Dittert and Henrich (2000) Dittert and Henrich (2000) Bickert (2009) Mackensen et al. (1993)

Emelyanov (2005)

Emelyanov (2005)

Schmiedl et al. (1997) Emelyanov (2005)

Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Sulpis et al. (2018) Levin and Gooday (20030 Emelyanov (2005) Bickert (2009) Emelyanov (2005) Emelyanov (2005) Emelyanov (2005)

Reference

(continued on next page)

Minimum and maximum values for this publication are the calculated Carbonate Compensation Depth minus and plus the standard deviation provided in Table S1

Minimum and maximum values for this publication are the calculated Carbonate Compensation Depth minus and plus the standard deviation provided in Table S1

“Well supplied with cold and aggressive (with respect to CaCO3) Antarctic waters” High biological productivity and low supply of Antarctic bottom waters High biological productivity and low supply of Antarctic bottom waters Values from Fig. 6

High biological productivity and low supply of Antarctic bottom waters Values from Fig. 6

Minimum and maximum values for this publication are the calculated Carbonate Compensation Depth minus and plus the standard deviation provided in Table S1

Comments

S.N. Brandão, et al.

Progress in Oceanography 178 (2019) 102144

4

S S

S

Southern Southern

Southern

Ross Sea “Polar areas” “neighboring the Antarctic” “Polar areas” “neighboring the Antarctic”

Summary Eastern Weddell Sea Western Weddell Sea Weddell Sea

Summary

S S S

Pacific Ocean Southern Southern Southern

10°N to 50° N South China Sea – – Ontong Java Plateau “low latitude” “near continent”

Worldwide

N NW Equatorial Equatorial W Equatorial SE SE

Pacific Pacific Pacific Pacific Pacific Pacific Pacific

– 50°N to 50°S 50°S to 10°N – Guatemala Deep Central, 19°N to 25°N

Summary

– N+S N+S N NE N

Pacific Pacific Pacific Pacific Pacific Pacific

Sea/region

Southern Ocean

N/S

Ocean

Table 1 (continued)

0

0

100

500 0

3000 500 1500 –

5500 3500 5100 4500 5250 4400 3700

4200 3000 – 4000 3400 3700

min.

CCD (m)

6014

4000

– 200

> 5500 1190 3700 4000

5500 – – –

– 3800

4600 5500 > 5500 4300 – –

max.

Emelyanov (2005)

Anderson (1975) Anderson (1975) Mackensen et al. (1990) Kennett (1966) Emelyanov (2005)

Pälike et al. (2012) Berger (1971) Pytkowicz (1970) Chen (1988) Emelyanov (2005) Ben-Yaakov et al. (1974) Pytkowicz (1970) Wang et al. (1995) Emelyanov (2005) Berger et al. (1982) Valencia (1973) Berger (1970) Berger (1970)

Reference

For aragonite

For calcite

Values from Fig. 5

Values from Fig. 5 Values from Fig. 5

High biological productivity Values from Fig. 1b

Values from Fig. 3

Value 4200 m from Fig. 2, value 4600 m from the text Values from Fig. 10

Comments

S.N. Brandão, et al.

Progress in Oceanography 178 (2019) 102144

SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO223 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250 SO250

KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio KuramBio

I I I I I I I I I I I I I I I II II II II II II II II II II II II II II II II II II II II II II II

Cruise abbreviation

Cruise name

2-4 2-5 3-4 3-5 3-10 4-5 5-5 6-4 7-4 8-4 9-4 9-5 10-4 11-4 12-2 5-1 6-1 10-1 14-1 20-1 25-1 26-1 36-1 37-1 51-1 61-1 63-1 74-1 75-1 77-1 83-1 86-1 89-1 90-1 94-1 98-1 100-1 103-1

Station 02/August/2012 02/August/2012 04/August/2012 04/August/2012 05/August/2012 07/August/2012 10/August/2012 13/August/2012 16/August/2012 19/August/2012 23/August/2012 23/August/2012 25/August/2012 29/August/2012 31/August/2012 18/August/2016 18/August/2016 20/August/2016 21/August/2016 24/August/2016 25/August/2017 25/August/2017 28/August/2017 28/August/2017 05/September/2017 08September/2017 09/September/2017 12/September/2017 12/September/2017 13/September/2017 15/September/2017 15/September/2017 16/September/2017 17/September/2017 18/September/2017 19/September/2017 20/September/2017 21/September/2017

Date (begin) 02:47 06:37 15:23 19:18 23:01 10:57 11:50 00:23 15:23 19:16 00:08 04:23 23:55 03:55 16:22 09:08 1:39 1:05 09:18 01:18 07:33 13:40 08:40 14:52 11:38 16:08 00:00 03:10 08:42 05:43 01:23 20:55 22:36 11:29 03:54 08:54 03:58 09:34

Time UTC (begin) BC BC BC BC AGT BC BC BC BC BC BC BC BC BC BC MUC BC EBS BC AGT BC MUC BC BC MUC BC MUC MUC BC EBS MUC AGT EBS AGT BC AGT BC AGT

Gear 46° 46° 47° 47° 47° 46° 43° 42° 43° 42° 40° 40° 41° 40° 39° 43° 43° 43° 45° 45° 45° 45° 45° 45° 45° 45° 45° 44° 44° 45° 45° 45° 44° 44° 44° 44° 44° 44°

13,95′ N 13,99′ N 14,32′ N 14,30′ N 14,27′ N 57,97′ N 34,97′ N 28,98′ N 2,31′ N 14,57′ N 35,03′ N 34,96′ N 12,02′ N 12,86′ N 43,43′ N 49,192′ N 49,197′ N 48,602′ N 50,879′ N 52,105′ N 55,235′ N 55,226′ N 38,610′ N 38,604′ N 28,751′ N 9,997′ N 10,007′ N 39,883′ N 39,883′ N 13,892′ N 1,356′ N 1,202′ N 39,325′ N 41,759′ N 6,852′ N 6,152′ N 12,378′ N 12,499′ N

Latitude (begin) 155° 155° 154° 154° 154° 154° 153° 153° 152° 151° 151° 151° 150° 148° 147° 151° 151° 151° 153° 153° 152° 152° 152° 152° 153° 153° 153° 151° 151° 152° 151° 151° 151° 151° 151° 151° 150° 150°

33,15′ E 33,10′ E 42,26′ E 42,23′ E 42,17′ E 32,49′ E 58,03′ E 59,97′ E 59,16′ E 43,51′ E 0,06′ E 0,07′ E 5,76′ E 5,92′ E 9,98′ E 45,599′ E 45,609′ E 47,124′ E 47,991′ E 51,287′ E 47,464′ E 47,468′ E 55,921′ E 55,911′ E 11,644′ E 45,419′ E 45,420′ E 28,106′ E 28,136′ E 50,774′ E 2,901′ E 6,008′ E 27,340′ E 26,554′ E 25,539′ E 25,705′ E 39,053′ E 39,055′ E

Longitude (begin) 4868 4869 4982 4984 4977 5766 5379 5297 5222 5130 5404 5401 5249 5348 5243 5147 5497 5352 8251 8191 6068 6065 7135 7136 8735 5741 5739 8221 8221 9577 5211 5572 8215 8271 6531 6441 9305 9301

Depth (begin) (m) – – – – 47° – – – – – – – – – – – – 43° – 45° – – – – – – – – – 45° – 45° 44° 44° – 44° – 44°

5

12,502′ N

6,253′ N

1,371′ N 39,053′ N 41,992′ N

14,219′ N

52,203′ N

48,455′ N

14,94′ N

Latitude (end) – – – – 154° – – – – – – – – – – – – 151° – 153° – – – – – – – – – 152° – 151° 151° 151° – 151° – 150°

37,258′ E

25,935′ E

6,001′ E 27,343′ E 26,321′ E

49,956′ E

51,435′ E

47,171′ E

43,18′ E

Longitude (end)

– – – – 4986 – – – – – – – – – – – – 5104 – 8199 – – – – – – – – – 9583 – 5530 8217 8273 – 6442 – 9431

Depth (end) (m)

Table 2 KuramBio I and II stations (northwestern Pacific Ocean) with ostracods, isopods and bivalves studied herein. Abbreviations: AGT, Agassiz Trawl. BC, boxcorer. EBS, epibenthic sledge. KuramBio, Kuril Kamchatka Biodiversity Studies. KuramBio I, first expedition of the KuramBio Project (initially this expedition was simply named KuramBio without the number one (I); only after the second expedition (KuramBio II) took place the number I was added to this expedition's name; herein we prefer to use KuramBio I for this first expedition, instead of the historical KuramBio, in order to avoid ambiguity with the project name and the second expedition). KuramBio II, second expedition of the KuramBio Project. MUC, Multicorer sampler.

S.N. Brandão, et al.

Progress in Oceanography 178 (2019) 102144

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

not be a barrier for their dispersion in the deep sea. However, their assemblages were almost entirely composed of empty valves, the dataset was relatively small (136 specimens) and the depth studied was very close or maybe even above the CCD (Table 1 herein). Therefore, in our opinion this last study did not definitely confirm the occurrence of ostracods below the CCD.

Chernyshev et al., 2015; Downey and Janussen, 2015; Golovan, 2015; Jażdżewska, 2015; Krylova et al., 2015; Chaban et al., 2018; Golovan et al., 2019). Molecular data on macrostylid isopods suggested that for some abyssal benthic organisms, the oceanic trench may restrict gene flow and hence contribute to genetic structure amongst populations and ultimately diversification (Bober et al., 2018). Besides studying abyssal and hadal ostracods collected during the KuramBio I and II expeditions, we survey the literature on deep-sea ostracods and compile all published data on (geologically) Recent (living and dead) ostracods collected worldwide in regions deeper than 3500 m, and verify their occurrence with respect to the CCD (Table 1). Data on pelagic ostracods were also compiled (App. A), but are excluded from the discussion because they lack a calcified carapace and therefore do not fit in the present study. Polycopids are also excluded from the present paper, because they are considered elsewhere. Additionally, the chemical composition of the shell of one bivalve and of the carapace of one isopod collected form the Kuril-Kamchatka Trench during the KuramBio II expedition was analyzed with Energy-Dispersive X-Ray Spectroscopy (EDX).

1.4. Fauna of the Kuril-Kamchatka Trench and adjacent areas Herein, we study hadal ostracods collected from 4863 to 9307 m depth in the Kuril-Kamchatka Trench and adjacent abyssal areas during the KuramBio I and KuramBio II expeditions. The region is characterised by a high surface productivity and is inhabited by a diverse and abundant benthic fauna (Zenkevitch, 1963; Sokolova, 1981; Abelmann et al., 2013). The Kuril-Kamchatka Trench is a northward extension of the Mariana, Izu-Bonin and Japan trenches and extends to depths of 9717 m (Mikhailov, 1970; Belyaev, 1989). In the mid-twentieth century, the northwestern Pacific became one of the best-studied deep-sea regions of the world thanks to the immense effort by Russian scientists between 1949 and 1976 during almost 30 expeditions with Research Vessel Vityaz (Monin, 1983). These studies targeted mostly bathyal and abyssal benthos and were the first to collect samples from the deep areas of the Kuril-Kamchatka Trench as well, one of the deepest oceanic trenches worldwide, together with the neighboring Aleutian and Mariana trenches. The Russian work represented a milestone upon which today’s deep-sea researchers build. Their historic zoological accounts (Birstein, 1963, 1970, 1971; Zenkevitch, 1963; Kussakin, 1971; Belyaev, 1972, 1989; Filatova, 1976; Ivanova, 1977; Filatova and Schileyko, 1984, 1985) represented a major proportion of the globally known species for many deep-sea taxa at that time and, still today, the fauna of the Kuril-Kamchatka Trench is one of the best studied hadal faunas. The deep-sea fauna of the northwestern Pacific is rich and diverse (Zenkevitch, 1963; Birstein, 1970, 1971), which anticipated that major fractions of the fauna were still unknown due to inappropriate sampling gear and methods used for sieving. Since these early Russian expeditions, no biological survey had been performed in the area until the Russian-German joint expeditions in the 21st century, which began with the Russian-German joint expedition SoJaBio (Sea of Japan Biodiversity Studies) with Research Vessel Akademik M.A. Lavrentyev in 2010 (Malyutina et al., 2010), when this deep-sea region received new attention. Altogether, four joint German-Russian campaigns have since been conducted in the northwestern Pacific and adjacent marginal seas with support from both the German and Russian governmental research funding agencies. After SoJaBio, the abyssal plain of the Pacific Ocean adjacent to the Kuril-Kamchatka Trench was studied during the KuramBio (Kuril-Kamchatka Biodiversity Studies) I expedition in 2012 with the German Research Vessel Sonne (Brandt and Malyutina, 2012, 2015). In 2015, the Research Vessel Akademik M.A. Lavrentyev set out to study the deep Kuril Basin in the Sea of Okhotsk and the bathyal Bussol Strait connecting the Sea of Okhotsk with the Pacific Ocean (Malyutina et al., 2018) (SokhoBio Project - Sea of Okhotsk Biodiversity Studies); and in 2016, again on Research Vessel Sonne (KuramBio II), the Kuril-Kamchatka Trench and adjacent abyssal plain were studied (Brandt and shipboard scientific party, 2016). During these last four expeditions, modern equipment and sampling methods were applied in a standardized way. The study area of these expeditions is briefly described in the introduction of this volume (Brandt et al., this issue). Amongst the goals of the KuramBio II expedition were an updated inventory of the hadal Kuril-Kamchatka Trench fauna, as well as the biogeography of benthic fauna with the Kuril-Kamchatka Trench as a potential barrier to the dispersion of abyssal species (Brandt and shipboard scientific party, 2016). Special focus on small-sized animals revealed many still undescribed taxa (e.g., Kamenev, 2013, 2014, 2015, 2018c; Alalykina, 2015; Błażewicz-Paszkowycz et al., 2015; Brandt et al., 2015a,b;

2. Material and methods 2.1. Ostracods from the Kuril-Kamchatka Trench (KuramBio I and II expeditions) The samples studied in the present study were collected during both cruises of the collaborative German-Russian project KuramBio. The KuramBio I expedition took place on board the German Research Vessel Sonne between 21st July and 7th September 2012 (cruise SO223) with the aim of surveying the benthos of the abyssal plain adjacent to the Kuril-Kamchatka Trench (Brandt and Malyutina, 2012). The hadal sampling campaign KuramBio II was conducted between 16th August and 26th September 2016 during cruise SO250 again with the Research Vessel Sonne (Brandt and shipboard scientific party, 2016). During both expeditions, samples were taken using various gear, including two kinds of epibenthic sledges (EBS, C-EBS) (Brandt et al., 2013; Brenke, 2005), multiple corer (MUC), boxcorer (BC), and Agassiz Trawl (AGT) (for details on gear deployment, see Brandt and Malyutina, 2012, Brandt and shipboard scientific party, 2016). On deck, the samples (except freshly picked material for biochemical analyses) were immediately transferred into either (1) chilled (−20 °C) 96% ethanol and kept in a −20 °C freezer for at least 48 h for subsequent DNA studies; or (2) formalin 4%. After fixation, the samples were sorted both on board and in the home laboratories. Although ostracods are traditionally seen as part of the meiofauna, they are generally present in samples of all gear, i.e., those aimed for sampling meiofauna (MUC), macrofauna (BC, C-EBS, EBS) and megafauna (AGT). Although the latter is equipped with a very wide mesh of 10 mm, in some cases it retained a large amount of sediment, which contained numerous small organisms (Brandt et al., this issue). Ostracod specimens were made available to three of us (SNB, IK, HY) in small glass vials containing ethanol or on micropalaeontological slides. Specimens were identified according to their valve morphology. Empty valves were kept or transferred to micropalaeontological slides. Specimens collected with soft parts were (1) either kept in ethanol; or (2) dissected with soft parts transferred to DNA extraction buffer; or (3) the soft parts of every selected specimen were dissected for taxonomic study on a glass slide with Hydromatrix medium. The valves of extracted and dissected specimens were transferred to micropalaeontological slides. For future correct assignment of soft parts or scanning electron microscope (SEM) photos to the respective valves, every dissected or photographed specimen received an identifier with prefix SNB (SNB 0998 to SNB 1175, see App. B). Selected valves were gold coated, mounted on SEM stubs and photographed with Hitachi S4700 scanning electron microscope at Eulji University (Seoul, South Korea). 6

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

Fig. 1. Ostracoda collected during the KuramBio I and KuramBio II expeditions from the Kuril-Kamchatka Trench and adjacent deep areas, Pacific Ocean: a, Krithe sp. (SNB 1226, KuramBio II, Station 100-1, 9307 m); b, Abyssocythere sp. nov. 1 (SNB 1056, KuramBio II, Station 10, 5352 m); c, Abyssocythereis sp. (SNB 1054, KuramBio II, Station 10, 5352 m); d, Acetabulastoma sp. (SNB 1026A, KuramBio I, Station 10-4, 5249 m); e, Argilloecia sp. (SNB 1024, KuramBio I, Station 11-4, 5349 m); f, Cytheropteron sp. (SNB 1101, KuramBio II, Station 51, 8735 m); g, Trachyleberididae sp. (SNB 1094, KuramBio II, Station 61, 5741 m); h, Henryhowella sp. (SNB 1083, KuramBio II, Station 86, 5572 m); i, Macropyxis sp. (SNB 1075, KuramBio II, Station 10, 5352 m); j, Legitimocythere sp. 1 (SNB 1000, KuramBio I, Station 3-5, 4984 m); k, Marwickcythereis sp. (SNB 1020, KuramBio I, Station 11-4, 5349 m); l, cf. Propontocypris sp. (SNB 1087, KuramBio II, Station 10, 5352 m); m, Retibythere sp. (SNB 1143, KuramBio II, Station 98, 6441 m); n, Vitjasiella sp. (SNB 1082, KuramBio II, Station 86, 5572 m); o, Zabythocypris sp. 1 (SNB 0998, KuramBio I, Station 2-4, 4868 m). Scale bars: a, e, f, 300 μm; b, c, h–k, m–o, 500 μm; g, 400 μm; d, l, 200 μm. Details on stations in Table 2.

7

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

Table 3 Summary of the previously published information on (geologically) Recent Ostracoda below 3500 m depth. Living

Dead

Total = Living + Dead

Depth (m)

Records

Localities

Species

Families

Papers

Records

Localities

Species

Families

Papers

Records

Localities

Species

Families

Papers

3500–3999 4000–4499 4500–4999 5000–5499 5500–5999 6000–6499 6500–6999 7000–7499 7500–7999 8000–8499 8500–8999 9000–9499 Total 3500–9499

118 62 92 56 5 6 0 0 0 0 1 0

47 33 49 25 4 3 0 0 0 0 1 0

67 34 39 38 5 6 0 0 0 0 1 0

18 16 15 12 1 3 0 0 0 0 1 0

23 20 20 12 1 4 0 0 0 0 1 0

276 159 58 27 0 1 0 0 0 4 0 0

68 45 16 7 0 1 0 0 0 1 0 0

67 47 25 11 0 1 0 0 0 3 0 0

12 15 8 7 0 1 0 0 0 3 0 0

28 18 13 2 0 1 0 0 0 1 0 0

394 221 150 83 5 7 0 0 0 4 1 0

109 76 62 32 4 4 0 0 0 1 1 0

122 38 50 44 5 7 0 0 0 3 1 0

19 13 13 13 1 4 0 0 0 3 1 0

51 36 33 14 1 5 0 0 0 1 1 0

340

162

134

22

42

525

138

94

18

42

865

289

206

25

81

In the species counts, an unidentified species (e.g., Pseudocythere sp.) was counted as one species, as soon as there was no other fully identified species in the same genus in the same depth range, unless all records of the identified and unidentified species in the same genus comes from a single publication, and the author clearly stated that the unidentified species is different from the other recorded in the same genus. For example, Maddocks (1990) recorded Macropyxis adrecta, Macropyxis adunca, Macropyxis antonbruunae, Macropyxis eltaninae, and Macropyxis sp. 20 from the depth range between 5500 and 6000 m. Unidentified ostracods were counted as one species when this was the single ostracod species recorded in a depth range, e.g., George and Higgins (1979) reported the single living ostracod as “ostracods” from the depth range > 8000 m (i.e., 8860 m). Benson (1975) was excluded from the localities', species' and records' count, because it is not possible to know, whether the single records are from living or dead specimens. “Record” is defined as a record of one taxon in each single locality, therefore one sample with 10 specimens, for example, yielded 10 records. The deepest previously published record of an ostracod (unidentified) is at 8860 m (George and Higgins, 1979).

400

200

6

Species

4

Records Localities

2

Species

100

Records Localities Species

0 3500-3999

4000-4499

4500-4999

5000-5499

5500-5999

6000-6499

6500-7999

8000-8499

Living + Dead

0

Dead

Count

300

Localities

Living

Records

8

8500-8999

Depth zone (m) Fig. 2. Bathymetrical distribution of published records of living* and dead** ostracods. Depth zones considered: 3500–3999 m; 4000–4499 m; 4500–4499 m; 4500–4999 m; 5000–5499 m; 5500–5999 m; 6000–6499 m; 6500–6999 m; 7000–7499 m; 7500–7999 m; 8000–8499 m; 8500–8999 m (data from table 3). See Appendix C for a complete list of papers used for this compilation. Living* specimens were collected with soft parts (e.g., limbs, body wall, internal organs). Dead** valves or carapaces (i.e. closed right and left valves) were collected without soft parts but not fossilised.

Herein, we define the abyssal zone from 3000 to 5999 m and the hadal zone as the regions deeper than 6000 m. Previous authors have interchangeably used diverse terms for ostracods collected alive or dead. In order to avoid confusion, we use the term living (in italics) for specimens collected with soft parts (e.g., limbs, body wall, internal organs) and dead (in italics) for valves or carapaces (i.e. closed right and left valves) collected without soft parts.

south, sector of Southern Ocean”; research vessel; cruise name and number; station number; sampling date; gear; abundance (number of specimens); “(geologically) Recent (living, =with soft parts) or Subfossil (dead, =without soft parts)”; notes. Maps were plotted in the program Ocean Data View (Schlitzer, 2012). Papers' information (authors; title; journal; volume; pages; doi; comments) was also compiled in another sheet, so the ostracod records can be traced back to the papers (see App. C). Records of ostracods geologically older than the Holocene were not compiled.

2.2. Compilation of previous deep-sea ostracod records

2.3. EDX analyses of bivalvia and isopoda from the Kuril-Kamchatka Trench

A detailed search was made on Zoological Records, Google Scholar and other indexes for papers on (geologically) Recent (i.e., living and dead, as defined above) deep-sea, benthic Ostracoda with terms such as: ostracod, Ostracoda, deep-sea, deep, myodocop, podocop, benthic, etc. If available, the following information was compiled in a digital sheet: family; genus; species; author of species; year of species; latitude; longitude; water depth; geographical region; ocean; “ocean: north,

We also include in our present study SEM photographs and EDX analyses of two bivalves and one isopod. For the taxonomic study, the shells of bivalve mollusks were cleaned of traces of soft tissues and periostracum in 50% diluted commercial bleach. All the cleaned valves 8

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

spectroscopy. ETOH, ethanol. KB number, number in the KuramBio Project database (given during the expedition to samples and subsamples). F, female. J, juvenile. LV, left valve. KuramBio, Kuril Kamchatka Biodiversity Studies. KuramBio I, first expedition of the KuramBio Project (initially this expedition was simply named KuramBio without the number one (I); only after the second expedition (KuramBio II) took place the number I was added to this expedition name; herein we prefer to use KuramBio I for this first expedition, instead of the historical KuramBio, in order to avoid ambiguosity with the project name and the second expedition). KuramBio II, second expedition of the KuramBio Project. LV, left valve. M, male. MP, micropalaeontological slide. MUC, Multicorer sampler. RV, right valve. RLV, closed right and left valves. SEM, scanning electron microscope. SNB Number, specimens number as given by SNB to each single dissected, photographed or extracted specimen for latter assignment of valves, DNA extracts, soft parts and photos of each single specimen (e.g., SNB 0998). SNBt Seoul, SEM stub number as given by SNB. V, valve. SoJaBio Project, Sea of Japan Biodiversity Studies. SokhoBio Project, Sea of Okhotsk Biodiversity Studies.

R² = 0.8556 100 R² = 0.9840

Living Dead

0

Living + Dead

R² = 0.8791

50

0

50

100

150

Fig. 3. Simple, linear relationship between number of species of ostracods and number of localities sampled in the deep sea (> 2000 m) worldwide, showing that the deep-sea is under sampled (at least for for ostracods, i.e., as new samples are taken, more biodiversity is discovered).

were washed in distilled water, dried, mounted onto aluminum stubs using an adhesive tape, and coated with carbon for examination with an SIGMA 300VP SEM (Carl Zeiss SMT) at the National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences (Vladivostok, Russia). The EDX analyses of two bivalves and one isopod from KuramBio II station 103 (details in Table 2) were performed in the LEO 1525 SEM (Carl Zeiss SMT) at the Center of Natural History (CeNak) in the Zoological Museum Hamburg (University of Hamburg, Germany).

3. Results 3.1. Deepest record of Ostracoda Thousands of living and dead ostracods were collected during the KuramBio I and II expeditions. The EBS samples of KuramBio II, for example, provided 618 specimens from the abyss and 2474 ostracods from the hadal stations (Brandt et al., this issue: supplementary Table 2d). Furthermore, the KuramBio II expedition provided the deepest record (9307 m) of an ostracod, this record refers to a living specimen with calcified carapace, which belongs to the genus Krithe (Fig. 1a). The very time-consuming taxonomic identifications are still ongoing, but at least 30 species and 21 genera were identified in the samples: Abyssocythere sp., Abyssocythere sp. nov. 1, Abyssocythere sp. nov. 2, Abyssocythereis sp., Acetabulastoma sp., cf. Argilloecia sp., Bythocytheridae sp., Cytheropteron spp., Cytheruridae sp.,

2.4. Abbreviations A, adult. (A-1), last juvenile stage (adult minus 1 stage). AGT, Agassiz Trawl. BC, boxcorer. CCD, Calcite Compensation Depth. C-EBS, epibenthic sledge equipped with a camera system and physicochemical sensors. EBS, epibenthic sledge. EDX, Energy-Dispersive X-ray

60˚N

30˚N

EQ

60˚S

living ostracods* dead ostracods** 90˚E

3500m - 3999m 180˚W

90˚W

0˚

Ocean Data View

30˚S

90˚E

Fig. 4. Previously published records of living* and dead** ostracods from localities between 3500 m and 3999 m. See Appendix C for a complete list of papers used for this compilation. Living* specimens were collected with soft parts (e.g., limbs, body wall, internal organs). Dead** valves or carapaces (i.e. closed right and left valves) were collected without soft parts but not fossilised.

9

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

60˚N

30˚N

EQ

30˚S

living ostracods* dead ostracods**

4000m - 4499m 180˚W

90˚E

Ocean Data View

60˚S

90˚W

0˚

90˚E

Fig. 5. Previously published records of living* and dead** ostracods from localities between 4000 m and 4499 m. See Appendix C for a complete list of papers used for this compilation. Living* specimens were collected with soft parts (e.g., limbs, body wall, internal organs). Dead** valves or carapaces (i.e. closed right and left valves) were collected without soft parts but not fossilised.

60˚N

30˚N

EQ

60˚S

living ostracods* dead ostracods** 90˚E

KuramBio ostracods 180˚W

4500m - 4999m 90˚W

0˚

Ocean Data View

30˚S

90˚E

Fig. 6. Previously published and KuramBio records of living* and dead** ostracods from localities between 4500 m and 4999 m. See Appendix C for a complete list of papers used for this compilation. Living* specimens were collected with soft parts (e.g., limbs, body wall, internal organs). Dead** valves or carapaces (i.e. closed right and left valves) were collected without soft parts but not fossilised. KuramBio ostracods were collected living (yellow circles) from stations between 5115 and 5429 m depth. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Trachyleberididae sp. (?gen. nov.), Henryhowella sp., Krithe spp., Legitimocythere spp., Macropyxis sp., Marwickcythereis sp., Ostracoda indet., Poseidonamicus sp., cf. Propontocypris sp., Retibythere sp., Ryugucivis sp., Trachyleberididae sp., Vitjasiella sp., Zabythocypris sp. (Fig. 1).

3.2. High diversity of Ostracoda in areas deeper than 3500 m According to our compilation, at least 206 species of benthic ostracods with calcified carapaces have been recorded as living and/or as dead shells from deeper than 3500 m in several oceanic regions (Apps A, D). This depth (3500 m) represents one of the shallowest CCD depths 10

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

60˚N

30˚N

EQ

30˚S

90˚E

Ocean Data View

60˚S

180˚W

9 0˚ W

0˚

90˚E

Fig. 7. Previously published and KuramBio records of living* and dead** ostracods from localities deeper than 5000 m. See Appendix C for a complete list of papers used for this compilation. Living* specimens were collected with soft parts (e.g., limbs, body wall, internal organs). Dead** valves or carapaces (i.e. closed right and left valves) were collected without soft parts but not fossilised. Previously published records: unlabelled black circles are localities where living ostracods where collected from 5000 m to 5499 m water depth (Brady, 1880; Benson, 1975; Kornicker, 1975; Schornikov, 1975, 1976, 1980, 1981; Chavtur, 1981; Hartmann, 1985; Maddocks, 1990; Jellinek et al., 2006; Yasuhara et al., 2008; Karanovic and Brandão, 2012, 2015). Labelled black circles with an *: 1, the deepest record of a (possibly not calcified) ostracod from the Brownson Deep, in the Puerto Rico Trench, northwestern Atlantic (George and Higgins, 1979: Table 1); 2, records of living ostracods collected at or deeper than 6000 m in a total of 4 localities (Poulsen, 1962; Maddocks, 1969, 1990; Schornikov, 1980); 3, single record of a dead ostracod deeper than 6000 m (Rudjakov, 1961); 4, records of living ostracods from 5500 m to 5999 m (Maddocks, 1990). KuramBio ostracods were collected living: yellow circles, stations between 5115 and 5429 m depth; orange circle, station at 5681 m depth; green circles, stations between 7902 and 8165 m depth; blue circles, deepest record of an ostracod (KuramBio II working area A6, Station 100-1) 9307 m depth. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

and 5029 m (Brady, 1880). According to our survey, at least 85 publications (Suppl. data 3) recorded more than 200 species (89 genera, 25 families) of living or dead ostracods from regions deeper than 3500 m in different oceanic areas. In some cases, the bottom depth of the regions studied is close to the CCD or even above it, as mentioned above for the abyssal (5030–5150 m) ostracods from the Cape and Guinea basins, eastern Atlantic (Yasuhara et al., 2008). In another case, 22 specimens of Keysercytheridae plus a few bairdioids were collected from a wood fall in the region adjacent to the Kuril-Kamchatka Trench at a depth of 5217 m (Karanovic and Brandão, 2015). A diverse ostracod fauna was reported from two grab samples, also from the Kuril-Kamchatka Trench region in depths of 5200–5240 m. The latter fauna included ten living polycopid (Chavtur, 1981) and one living trachyleberidid species (Schornikov, 1975). In these last two studies, 12 of the 13 species were collected with well-preserved soft parts, as illustrated by the investigators (Chavtur, 1981; Karanovic and Brandão, 2015). Even below 5500 m (which is deeper than the CCD in almost all oceanic regions), 10 living species (seven podocope macrocypridids, two podocope bythocypridids, and one myodocope cypridinid) were recorded from 8 localities in the world oceans (Poulsen, 1962; Maddocks, 1969, 1990; George and Higgins, 1979; Schornikov, 1980). Another species was collected with fragmented soft parts (i.e., Krithe, 6487 m) (Rudjakov, 1961) and other two were collected dead (i.e., Retibythere (Bathybythere) scaberrima at 3535–8100 m and Krithe sp. at 8100 m) (Schornikov, 1987). Belyaev (1989) summarized the occurrence of hadal organisms (> 6000 m deep) from all oceans collected during Russian and international expeditions from 1875 to 1985. He recorded more than 800 species of “protists” and animals. The book listed 6 planktonic, non-

and is somehow intermediate between the shallowest and deepest CCDs in the world oceans, i.e., 0 m in the Southern Ocean and ≃6000 m in the “southern North American Basin“ (Emelyanov, 2005) (see Table 1 and references therein). The information on ostracods recorded living or dead deeper than 3500 m are summarized in Table 3, Figs. 2–7 and Appendices A and D. Appendix C lists all papers with records of living or dead ostracods below 3500 m depth. The number of localities sampled diminish gradually with depth (Figs. 2, 4–7), and the numbers of localities and species show a strong, positive, linear correlation (Fig. 3). In total, 91 genera and 25 families have been recorded and they belong to both ostracod subclasses with living representatives and to four (among five) orders with living representatives. No ostracod from the order Palaeocopida has been recorded from > 3500 m depth. This order was very diverse in the Paleozoic, but is represented in (geologically) Recent oceans by merely two genera (i.e., Manawa and Puncia), which occur exclusively in shallow ecosystems. 3.3. EDX analyses of bivalvia and isopoda The EDX analyses show that the one isopod and two bivalve specimens contain high proportion of calcium (22, 41 and 32%, respectively), which show that they possess calcified shell or carapace (Suppl. A, Figs. A.1 and A.2). 4. Discussion Already in the 19th century the HMS Challenger worldwide expedition collected eleven ostracod species from depths between 3547 m 11

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

Fig. 8. Parayoldiella ultraabyssalis (Filatova, 1971) (a–c) and Vesicomya sergeevi Filatova, 1971 (d–f) from the Kuril-Kamchatka Trench, Pacific Ocean (KuramBio II, Station 103-1). Scale bars: 1 mm. Details on station in Table 2.

calcified ostracods and 8 benthic, calcified ostracods, with the deepest record of a calcified ostracod being a dead specimen of “Retibythere (Bathybythere) scaberrima” from a sledge sample collected from 7950 to 8100 m in the Puerto-Rico Trench (Schornikov, 1987). In sum, the high diversity reported for regions deeper than 3500 m, at both low and high taxonomic levels (4 suborders, 25 families, 89 genera), shows that ostracods are well adapted to live in habitats below the CCD. The number of species recorded in our compilation decreases with depth, but this decrease is strongly correlated to the sampling effort, and should therefore not be attributed to processes associated with the CCD (i.e. localities in Table 3, Fig. 2). The correlation between number of localities and number of species in relation to the depth zones (3500–3999 m; 4000–4499 m; 4500–4499 m; 4500–4999 m; 5000–5499 m; 5500–5999 m; 6000–6499 m; 6500–6999 m; 7000–7499 m; 7500–7999 m; 8000–8499 m; 8500–8999 m) is very high for all species, those collected living (R2 = 0,8791), the ones collected dead (R2 = 0,9840), and for both together (R2 = 0,8556) (Fig. 3). Additionally, the strongest evidence for the ability of ostracods to thrive below the CCD is the high number of specimens collected considerably below the CCD during the KuramBio II cruise (see Brandt et al., this issue: suppl. Table 2d). For example, tens to hundreds of living ostracods were collected in single EBS samples of the study areas A1 (8191 m, 752 ostracods), A2 (6575 m, 314), A4 (8745 m, 20), and A5 (7123 m, 34). Among those there was a high number of living specimens further supporting the evidence that the ostracods really live in these corrosive environments, while downslope contamination (i.e., animals brought from shallower regions by turbidity currents, for example) is very unlikely. The EBS used during KuramBio cruises has a very heavy, metal door, which only opens when the gear reaches the bottom and closes immediately after the gear leaves the bottom (Brandt and Barthel, 1995), therefore no organism is collected in the water column. The occurrence of ostracods below the CCD helps to explain the cosmopolitan or widespread distribution of many ostracod deep-sea genera and monophyletic groups of closely related species (e.g.,

Yasuhara et al., 2019), e.g., Cytheropteron, Henryhowella, Krithe, Legitimocythere, Macropyxis, Zabythocypris, specially because benthic ostracods lack pelagic larvae (e.g., Hartmann, 1966). Pelagic larvae would be a means of ostracods being dispersed in the water column in depths above the CCD. However, as mentioned by previous authors (e.g., Brandão and Horne, 2009), ostracods are known to survive ingestion by marine fishes and terrestrial vertebrates (e.g., Lopez et al., 1999). So, passive dispersal above or below the CCD is also a possible way to benthic, deep-sea ostracods’ dispersion. Based on the KuramBio samples and our compilation of previously published records, ten genera, i.e. Argilloecia, Cytheropteron, Henryhowella, Krithe, Legitimocythere, Macropyxis, cf. Propontocypris, Retibythere, Vitjasiella, Zabythocypris (Suppl. data 1 and 4), occur in regions deeper than 5500 m, which is at or below the CCD for most of the world’s oceans (Table 1). Three of these genera (Argilloecia, Cytheropteron, Propontocypris) have been recorded not only from many localities in the deep-sea worldwide, but also from shallow, marine habitats. Due to their extremely loose morphological concept, the inclusion in a biogeographical discussion does not seem appropriate to us. However, the remaining genera (Henryhowella, Krithe, Legitimocythere, Macropyxis, Retibythere, Vitjasiella, Zabythocypris) are cosmopolitan in the deep sea, with also records in shallow, but cold regions of the worlds’ oceans (e.g., Maddocks, 1990). The widespread distribution of these latter genera can be explained by their occurrence below the CCD, together with bathyal and abyssal seaways which exist (e.g., Drake Passage in the Southern Ocean) or have existed in the past (Tethyan, Central American and Arctic pathways) as discussed by Yasuhara et al. (2019). Moreover, a further fact that reinforces the theory that ostracods can survive conditions which favour carbonate dissolution (like the CCD), is that ostracods from evolutionary lineages that split in the Ordovician (~445 million years), i.e. the suborders Cytherocopina and Cypridocopina are able to survive after being ingested and passing through the entire digestive system of “fishes” (Osteichthyes), 12

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

amphibians and mammals (Vinyard, 1979; Lopez et al., 2002). Digestive systems of vertebrates are far more acid (usually pH < 3.0) and consequently far more corrosive for carbonate than the marine environments below the CCD. Adding to this conclusion, as mentioned by Yasuhara et al. (2008), ostracods have been collected alive in lakes with pH as low as 2.7. For example, Australocypris bennetti is frequently found at pH lower than 4 (e.g., Halse and McRae, 2004). The ability of surviving acid waters is related to the structure of the ostracod carapace. In living ostracods, the calcite part of the shell is not external, but an internal calcified layer within the epidermis of the duplicature (i.e., the double-layered portion of the ostracod carapace), so in living animals it is protected from direct contact with external fluids by the sclerotized (pseudochitinous) outer epidermal layer (see Keyser and Walter, 2004 and references therein). When the animal dies, the protective outer pseudochitin is digested and the calcite comes in contact with the ambient water, which is corrosive below the CCD. As mentioned by Horne (David J. Horne, personal communication), a further factor to be considered is the duration of contact with the corrosive fluids. Ostracod shells may spend only hours or days in the gut of a vertebrate, but centuries or millennia in waters below the CCD. Even when only ostracod shells from the very superficial layers of sediment are considered, the valves may have been there for at least years or decades, if not centuries and millennia, a fact that will favour calcite dissolution. Another factor worthwhile mentioning is the ratio between Mg and Ca in the valve. It has been shown in numerous studies (see Dwyer et al., 2002 and references therein) that Mg/Ca ratio in ostracod shell is positively correlated with water temperature. Despite this variation being also species, and sometimes region (or ecological conditions) specific, Mg/Ca ratio in the ostracod shell, has been an important tool in paleotemperature resonstruction (see Cronin et al., 2000). The Mg/Ca ratio in ostracod shell influences the preservation of calcareous remains in the sea floor, since a higher content of Mg favours the calcite dissolution. This may explain why, although ostracods (and other organisms with calcified skeleton) live in regions deeper than the CCD, no calcified remains are found in the fossil record from these depths. Concerning organisms other than ostracods, a characteristic example of animals with a pronounced calcified exoskeleton, widely distributed in the hadal zone, are the bivalves. As a rule, abyssal and hadal species of bivalve mollusks have quite a delicate shell with a poorly developed external sculpture (Knudsen, 1970). However, this may be associated with not only shortage of CaCO3 at depths below CCD, but also with the conditions of living on very soft bottom sediments and exposure to extremely low dynamics of near-bottom water (i.e. near-stagnant water). Bivalves were recorded from all depths of the Kuril-Kamchatka Trench, and species such as Parayoldiella ultraabyssalis (Filatova, 1971) and Vesicomya sergeevi Filatova, 1971 form large populations with very high population density on the trench floor (deeper than 9000 m) (Filatova, 1971; Filatova and Schileyko, 1985; Kamenev, 2019). In some trawl samples from the seafloor, each species was represented by over 3000 specimens (Belyaev, 1989). These species have quite a thick shell with well-defined and large hinge teeth (Fig. 8). In thickness of their shell and in hinge structure, they do not differ from the closely related species inhabiting the bathyal and abyssal zones of the adjacent Pacific areas shallower than the CCD (Kamenev, 2013, 2018c; Krylova et al., 2015). Moreover, the abyssal and hadal species Hyalopecten abyssalis Kamenev, 2018, Hyalopecten hadalis (Knudsen, 1970), Hyalopecten vityazi Kamenev, 2018, and Parvamussium pacificum Kamenev, 2017, living on relatively hard bottom sediments of the abyssal plain and slopes of several trenches in the Pacific Ocean at a depth more than 5000 m, are characterized not only by quite a thick shell, but also by the external sculpture of shell with pronounced commarginal and radial ribs and spines (Knudsen, 1970; Kamenev, 2018a, 2018b). Many other animals from the hadal zone, being exposed to the conditions of acute shortage of CaCO3 in the habitat, also successfully overcome the problem of building the skeleton. Their skeletons are sometimes even thicker than those in related species from

shallower waters (e.g., the thicker cuticle in the hadal isopod Rectisura herculea (Birstein, 1957) or the more numerous and larger spicules in the deepest holoturian Elpidia hanseni Belyaev, 1971) (Belyaev, 1989). Cedhagen et al. (2012) highlight living benthic, calcareous foraminifera collected from regions deeper than 5000 m in the border of Southern and Atlantic oceans. Therefore, although the calcium carbonate shortage at depths below the CCD is most likely one of the limiting factors in the vertical distribution of many animal species having skeletons, there is no doubt that a diverse group of species from distant phylogenetic lineages have adapted to the extremely low CaCO3 level. For these species at least, the CCD does not limit the distribution of life in the hadal zone of the world’s oceans. 5. Conclusions Based on the compilation of published ostracods deep-sea records and the new data from the Kurile-Kamchatka Trench (KuramBio Project), we conclude that ostracods (together with other calcified organisms) are able to live below the Carbonate Compensation Depth, but because of post mortem dissolution their valves and carapaces are rarely preserved in the sediment or sedimentary rocks from these depths. Acknowledgements This is the KuramBio publication #45. David J. Horne (Queen Mary University of London) is kindly acknowledged for valuable comments and suggestions in an early stage of this project. The crew and scientists of the KuramBio I and II expeditions are kindly acknowledged for the logistics and support during sampling. We are indebted to the two anonymous referees and to the editor Marina Malyutina for valuable suggestions. We are thankful to Mrs. Renate Walter and Dietmar Keyser (Zoologisches Museum, University of Hamburg) for their assistance during EDX analyses. Many thanks to Oliver Meyer and his friendly and professional team on board of the Research Vessel Sonne. Moriaki Yasuhara kindly revised the manuscript and provided literature. The Census of Abyssal Marine life (CeDAMar) Program of the Census of Marine Life (CoML) provided funds to SNB for the compilation of deepsea records of Ostracoda. The Alexander von Humboldt Foundation, CNPq (processes 400116/2013-8, 374397/2013-9, 442550/2014-6 and 311413/2016-1) and CAPES (1627957 and 88887.123925/2015-00) provided financial support to SNB and HV in different periods of this study. The study of bivalve mollusks of the Kuril-Kamchatka Trench performed by GMK was supported by the Russian Foundation for Basic Research (grant no. 19-04-00281 -a). IK and HY were supported by the Korean National Research Foundation (NRF, number 2016R1D1A1B01009806). The collaborative German-Russian project KuramBio was funded by the German ministry for education and research (BMBF) under project # 03GO250A to AB. We are also grateful to the German Ministry of Education and Research for providing Research Vessel Sonne for this expedition and the shipping company Briese for logistics. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.pocean.2019.102144. References Abelmann, A., Adrianov, A.V., Azovsky, A.I., Borisanova, A.O., Buzhinskaja, G.N., Chaban, E.M., Chavtur, V.G., Chernyshov, A.V., Chertoprud, E.S., Dautova, T.N., Denisenko, N.V., Dzhurinskyi, V.L., Ezhova, O.V., Golovan, O.A., Grebelnyi, S.D., Gulbin, V.V., Ivanov, D.L., Kantor, Y.I., Kasatkina, A.P., Katugin, O.N., Kobekov, F.V., Kolbasov, G.A., Kosyan, A.R., Kruglikova, S.B., Lukina, T.G., Lutaenko, K.A., Maiorova, A.S., Marin, I.N., Markhaseva, E.L., Martynov, A.V., Matul, A.G., Mazei,

13

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al. Y.A., Merkuliev, A.V., Molodtsova, T.N., Nikitina, M.P., Petrjashov, V.V., Petrov, A.A., Pushkin, A.F., Schornikov, E.I., Semenova, T.N., Shedko, M.B., Shevtsov, G.A., Shoshin, A.V., Sirenko, B.I., Smirnov, A.V., Smirnov, I.S., Smirnov, R.V., Spiridonov, V.A., Stepanjants, S.D., Sysoev, A.V., Tarasova, T.S., Timm, T., Temereva, E.N., Tumanov, D.V., Tzareva, L.A., Utevsky, S.Y., Vyshkvartseva, N.V., Zasko, D.N., Zezina, O.N., Zhuravleva, N.E., 2013. Check-list of species of free-living invertebrates of the Russian Far Eastern seas. In: In: Sirenko, B.I. (Ed.), Explorations of the Fauna of the Seas, vol. 75(83). Russian Academy of Sciences, Zoological Institute, St. Petersburg, pp. 256. Alalykina, I.L., 2015. Polychaete composition from the abyssal plain adjacent to the KurilKamchatka Trench with the description of a new species of Sphaerephesia (Polychaeta: Sphaerodoridae). Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 166–174. https://doi.org/10.1016/j.dsr2.2014.09.006. Anderson, J.B., 1975. Factors controlling CaCO3 dissolution in the Weddell Sea from foraminiferal distribution patterns. Mar. Geol. 19, 315–332. https://doi.org/10. 1016/0025-3227(75)90083-3. Belyaev, G.M., 1972. Hadal Bottom Fauna of the World Ocean. Publ. for the Smithsonian Institution, Washington by the Israel Progr. Of Sci. Translat, Jerusalem, pp. 199. Belyaev, G.M., 1989. Deep-Sea Oceanic Trenches and their Fauna. Nauka Press, Moscow (in Russian). Ben-Yaakov, S., Ruth, E., Kaplan, I.R., 1974. Carbonate compensation depth: relation to carbonate solubility in ocean waters. Science 184, 982–984. https://doi.org/10. 1126/science.184.4140.982. Benson, R.H., 1975. The origin of the psychrosphere as recorded in changes of deep-sea ostracode assemblages. Lethaia 8, 69–83. https://doi.org/10.1111/j.1502-3931. 1975.tb00919.x. Berger, W.H., 1970. Planktonic Foraminifera: selective solution and the lysocline. Mar. Geol. 8, 111–138. Berger, W.H., 1971. Sedimentation of planktonic foraminifera. Mar. Geol. 11, 325–358. Berger, W.H., Parker, F.L., Jolla, L., 1982. Foraminifera on the deep-sea floor: lysocline and dissolution rate. Oceanol. Acta 5, 249–258. Berner, R.A., Morse, J.W., 1974. Dissolution kinetics of calcium carbonate in sea water; IV, Theory of calcite dissolution. Am. J. Sci. 274, 108–134. https://doi.org/10.2475/ ajs.274.2.108. Bickert, T., 2009. Carbonate compensation depth. In: Gornitz, V. (Ed.), Encyclopedia of Paleoclimatology and Ancient Environments. Springer, Netherlands, Dordrecht, pp. 136–138. https://doi.org/10.1007/978-1-4020-4411-3_33. Birstein, Y.A., 1963. Deep water isopods (Crustacea, Isopoda) of the north-western part of the Pacific Ocean. Akad. Nauk SSSR Mosc. 1–213. Birstein, Y.A., 1970. New Crustacea Isopoda from the Kurile-Kamchatka Trench area. In: Bogorov, V.G. (Ed.), Fauna of the Kurile-Kamchatka Trench and its environment. Proceedings of the Shirshov Institute of Oceanology. Academy of Sciences of the USSR, Moscow, pp. 308–356. Birstein, J.A., 1971. Additions to the Fauna of Isopods (Crustacea, Isopoda) of the KurileKamchatka Trench. Part II. Asellota 2, Fauna of the Kurile-Kamchatka Trench. Akademiya Nauk, SSSR, Moskova [Moscow]. Błażewicz-Paszkowycz, M., Pabis, K., Jóźwiak, P., 2015. Tanaidacean fauna of the KurilKamchatka Trench and adjacent abyssal plain – abundance, diversity and rare species. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 325–332. https://doi.org/10. 1016/j.dsr2.2014.08.021. Bober, S., Riehl, T., Henne, S., Brandt, A., 2018. New Macrostylidae (Crustacea, Isopoda) from the abyssal Northwest Pacific Basin described by means of integrative taxonomy with a reference to geographic barriers in the abyssal deep sea. Zool. J. Linn. Soc. 182, 549–603. https://doi.org/10.1093/zoolinnean/zlx042. Boomer, I., 1999. Late Cretaceous and Cainozoic bathyal Ostracoda from the Central Pacific (DSDP Site 463). Mar. Micropaleontol. 37, 131–147. https://doi.org/10. 1016/S0377-8398(99)00015-8. Brady, G.S., 1880. Report on the Ostracoda dredged by H.M.S. Challenger during the Years 1873–1876. In: Report on the scientific results of the voyage of H.M.S. Challenger. Zoology, vol. 1. pp. 1–184. Brandão, S.N., Angel, M.V., Karanovic, I., Perrier, V., Meidla, T., 2019. World Ostracoda Database. Updated at http://www.marinespecies.org/ostracoda (accessed on 1 July 2019). Brandão, S.N., Horne, D.V., 2009. The Platycopid Signal of oxygen depletion in the ocean: a critical evaluation of the evidence from modern ostracod biology, ecology and depth distribution. Paleogeogr. Paleoclimatol. Paleoecol. 283, 126–133. Brandt, A., Alalykina, I., Brix, S., Brenke, N., Blażewicz, M., Golovan, O.A., Johannsen, N., Hrinko, A.M., Jażdżewska, A.M., Jeskulke, K., Kamenev, G.M., Lavrenteva, A.V., Malyutina, M.V., Riehl, T., Lins, L., 2019. Depth zonation of Northwest Pacific deepsea macrofauna (this issue). Prog. Oceanogr. https://doi.org/10.1016/j.pocean.2019. 102131. Brandt, A., Barthel, D., 1995. An improved supra- and epibenthic sledge for catching Peracarida (Crustacea, Malacostraca). Ophelia 43, 15–23. https://doi.org/10.1080/ 00785326.1995.10430574. Brandt, A., Elsner, N.O., Malyutina, M.V., Brenke, N., Golovan, O.A., Lavrenteva, A.V., Riehl, T., 2015a. Abyssal macrofauna of the Kuril-Kamchatka Trench area (Northwest Pacific) collected by means of a camera–epibenthic sledge. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 175–187. https://doi.org/10.1016/j.dsr2.2014.11.002. Brandt, A., Kristin Stüven, J., Caurant, C., Oskar Elsner, N., 2015b. An account of the Ischnomesidae (Peracarida, Isopoda) from the Kuril-Kamchatka Trench and abyssal plain (Northwest Pacific) with the description of two new species. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 279–293. https://doi.org/10.1016/j.dsr2.2014.08.014. Brandt, A., Malyutina, M.V., 2012. The German-Russian deep-sea expedition KuramBio (Kurile Kamchatka Biodiversity Study): to the Kuril-Kamchatka Trench and abyssal plain on board of the R/V Sonne, 223rd Expedition, July 21th–September 7th 2012 (Cruise Report), R/V Sonne Cruise Reports. University of Hamburg; Biozentrum

Grindel and Zoologisches Museum Hamburg, Hamburg. Brandt, A., Malyutina, M.V., 2015. The German-Russian deep-sea expedition KuramBio (Kurile Kamchatka biodiversity studies) on board of the RV Sonne in 2012 following the footsteps of the legendary expeditions with RV Vityaz. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 1–9. https://doi.org/10.1016/j.dsr2.2014.11.001. Brandt, A., shipboard scientific party, 2016. Kuril-Kamchatka Biodiversity Studies II - RV Sonne SO250, Tomakomai-Yokohama (Japan), 16.08.-26.09.2016 (Cruise report). University of Hamburg, Hamburg, Germany. Brenke, N., 2005. An epibenthic sledge for operations on marine soft bottom and bedrock. Mar. Technol. Soc. J. 39, 10–21. https://doi.org/10.4031/002533205787444015. Cedhagen, T., Lejzerowicz, F., Pawlowski, J., 2012. Foraminifera of the deep Southern Ocean: bentho-pelagic distribution and past and present metagenetics. Berichte zur Polar- und Meeresforsch. 661, 87–90. Chaban, E.M., Kano, Y., Fukumori, H., Chernyshev, A.V., 2018. Deep-sea gastropods of the family Ringiculidae (Gastropoda, Heterobranchia) from the Sea of Okhotsk, KurilKamchatka Trench, and adjacent waters with the description of three new species. Deep Sea Res. Part II Top. Stud. Oceanogr. 154, 197–213. https://doi.org/10.1016/j. dsr2.2017.11.008. Chavtur, V.G., 1981. New species of the deep-sea Ostracoda (Polycopidae) from KurilKamchatka Trench. Tr. Instituta Okeanol. Akad. Nauk SSSR 115, 62–75. Chen, A., 1988. Lysocline, calcium carbonate compensation depth, and calcareous sediments in the North Pacific Ocean. Pacific Sci. 42, 237–252. Chernyshev, A.V., 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 Res. Part II Top. Stud. Oceanogr. 111, 119–127. https://doi.org/10.1016/j.dsr2.2014.07.014. Cronin, T.M., Dwyer, G.S., Baker, P.A., Rodriguez-Lazaro, J., Demartino, D.M., 2000. Orbital and suborbital variability in North Atlantic bottom water temperature obtained from ostracod Mg/Ca ratios. Palaeogeogr. Palaeoclimatol. Palaeoecol. 162, 45–57. Dittert, N., Henrich, R., 2000. Carbonate dissolution in the South Atlantic Ocean: evidence from ultrastructure breakdown in Globigerina bulloides. Deep Sea Res. Part I Oceanogr. Res. Pap. 47, 603–620. https://doi.org/10.1016/S0967-0637(99)00069-2. Downey, R.V., Janussen, D., 2015. New insights into the abyssal sponge fauna of the Kurile-Kamchatka plain and Trench region (Northwest Pacific). Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 34–43. https://doi.org/10.1016/j.dsr2.2014.08.010. Dwyer, G.S., Cronin, T.M., Baker, P.A., 2002. Trace elements in marine ostracods. Geoph. Monogr. 131, 205–226. Emelyanov, E.M., 2005. Calcium carbonate compensation depth (CCD). In: The Barrier Zones in the Ocean. Springer-Verlag, Berlin/Heidelberg, pp. 345–361. https://doi. org/10.1007/3-540-26230-X_20. Filatova, Z.A., 1971. On some mass species of bivalve mollusks from the ultra-abyssal zone of the Kuril-Kamchatka Trench. Proc. P.P. Shirshov Inst. Oceanol. 92, 46–60 (in Russian). Filatova, Z.A., 1976. Structure of the deep-sea genus of bivalve mollusca Spinula (Dall, 1908, Malletidae) and its distribution in the World Ocean. Proc. P.P. Shirshov Inst. Oceanol. 99, 219–240 (in Russian). Filatova, Z.A., Schileyko, A.A., 1984. Size, structure and distribution of the deep-sea Bivalvia of the family Ledellidae (Protobranchia). Proc. P.P. Shirshov Inst. Oceanol. 119, 106–144 (in Russian). Filatova, Z.A., Schileyko, A.A., 1985. Composition, morphology and distribution of the ultra-abyssal genus Parayoldiella (Bivalvia: Protobranchia). Proc. P.P. Shirshov Inst. Oceanol. 135, 76–94 (in Russian). George, R.Y., Higgins, R.P., 1979. Eutrophic hadal benthic community in the Puerto Rico Trench. In: The Deep Sea: Ecology and Exploitation. Ambio Special Report. Allen Press, pp. 51–58. Golovan, O.A., 2015. Desmosomatidae (Isopoda: Asellota) from the abyssal plain to the east of the Kuril-Kamchatka Trench: new data on diversity with the description of two new species. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 256–278. https://doi. org/10.1016/j.dsr2.2014.08.020. Golovan, Olga A., Błażewicz, Magdalena, Brandt, Angelika, Jażdżewska, Anna М., Jóźwiak, Piotr, Lavrenteva, Anna V., Malyutina, Marina V., Petryashov, Victor V., Riehl, Torben, Sattarova, Valentina V., 2019. Diversity and distribution of peracarid crustaceans (Malacostraca) from the abyss adjacent to the Kuril-Kamchatka Trench. Mar. Biodiv. 49 (3), 1343–1360. https://doi.org/10.1007/s12526-018-0908-3. Hartmann, G., 1966. Ostracoda, Dr. H.G. Bronns Klassen und Ordnungen des Tierreichs. Fünfter Band: Arthropoda. I. Abteilung: Crustacea. 2. Buch, IV. Teil., 3. Lieferung. VEB Gustav Fischer Verlag, Jena. Halse, S.A., McRae, J.M., 2004. New Genera and Species of “Giant” Ostracods (Crustacea: Cyprididae) from Australia. Hydrobiologia 524, 1–52. https://doi.org/10.1023/ B:HYDR.0000036197.03776.46. Hartmann, G., 1985. Ostracoden aus der Tiefsee des Indischen Ozeans und der Iberischen See sowie von ostatlantischen sublitoralen Plateaus und Kuppen. Mit einer Tabelle der bislang bekannten rezenten Tiefseeostracoden. Senckenbergiana Maritima 17, 89–146. Hauck, J., Gerdes, D., Hillenbrand, C.-D., Hoppema, M., Kuhn, G., Nehrke, G., Völker, C., Wolf-Gladrow, D.A., 2012. Distribution and mineralogy of carbonate sediments on Antarctic shelves. J. Mar. Syst. 90, 77–87. https://doi.org/10.1016/j.jmarsys.2011. 09.005. Ivanova, V.L., 1977. New data on the composition and distribution of the deep-sea Bivalvia of the genus Policordia (fam. Verticordiida). Proc. P.P. Shirshov Inst. Oceanol. 108, 173–197 (in Russian). Jamieson, A.J., 2015. The Hadal Zone: Life in the Deepest Oceans. Cambridge University Press, United Kingdom. Jamieson, A.J., Fujii, T., Mayor, D.J., Solan, M., Priede, I.G., 2010. Hadal trenches: the ecology of the deepest places on Earth. Trends Ecol. Evol. 25, 190–197. https://doi.

14

Progress in Oceanography 178 (2019) 102144

S.N. Brandão, et al.

Maddocks, R.F., 1990. Living and fossil Macrocyprididae (Ostracoda). Univ. Kansas Paleontol. Contrib. Monogr. 2, 1–285. Malyutina, M.V., Brandt, A., Bashmanov, A., Brenke, N., Elsner, N.O., Göcke, C., Golovan, O.A., Kharlamenko, V.I., Kudryavtsev, A., Lejzerowicz, F., Lutaenko, K., Lyevin, S., Mayorova, A., Miljutin, D., Minin, K., Nekrasov, D., Radashevsky, V., Riehl, T., Savelyev, P., Schott, T., Schwabe, E., Trebuchova, J., Würzberg, L., 2010. The Russian-German deep-sea expedition (SoJaBio) to the Sea of Japan onboard of the R/ V Akademik Lavrentyev. 51st Cruise, August 11th–September 5th, 2010 (Cruise Report). A.V.Zhirmunsky’s Institute of Marine Biology, Vladivostok, Russia. Malyutina, M.V., Chernyshev, A.V., Brandt, A., 2018. Introduction to the SokhoBio (Sea of Okhotsk Biodiversity Studies) expedition 2015. Deep Sea Res. Part II Top. Stud. Oceanogr. 154, 1–9. https://doi.org/10.1016/j.dsr2.2018.08.012. Mikhailov, O.V., 1970. Some new data on the bottom relief of the Kuril-Kamchatka Trench. Proc. P.P. Shirshov Inst. Oceanol. 86, 72–76 (in Russian). Monin, A.S. (Ed.), 1983. Research Vessel “Vityaz” and her Expeditions 1949–1979. Nauka Press, Moscow (in Russian). Nybelin, O., 1951. Introduction and station list. Reports of the Swedish Deep-sea Expedition, 1947–1948. Zoology II (1), 1–28. Pälike, H., Lyle, M.W., Nishi, H., Raffi, I., Ridgwell, A., Gamage, K., Klaus, A., Acton, G., Anderson, L., Backman, J., Baldauf, J., Beltran, C., Bohaty, S.M., Bown, P., Busch, W., Channell, J.E.T., Chun, C.O.J., Delaney, M., Dewangan, P., Dunkley Jones, T., Edgar, K.M., Evans, H., Fitch, P., Foster, G.L., Gussone, N., Hasegawa, H., Hathorne, E.C., Hayashi, H., Herrle, J.O., Holbourn, A., Hovan, S., Hyeong, K., Iijima, K., Ito, T., Kamikuri, S., Kimoto, K., Kuroda, J., Leon-Rodriguez, L., Malinverno, A., Moore Jr., T.C., Murphy, B.H., Murphy, D.P., Nakamura, H., Ogane, K., Ohneiser, C., Richter, C., Robinson, R., Rohling, E.J., Romero, O., Sawada, K., Scher, H., Schneider, L., Sluijs, A., Takata, H., Tian, J., Tsujimoto, A., Wade, B.S., Westerhold, T., Wilkens, R., Williams, T., Wilson, P.A., Yamamoto, Y., Yamamoto, S., Yamazaki, T., Zeebe, R.E., 2012. A Cenozoic record of the equatorial Pacific carbonate compensation depth. Nature 488, 609–614. https://doi.org/10.1038/nature11360. Petterson, H., 1948. Rätsel der Tiefsee. A. Francke, Bern, pp. 149. Poulsen, E.M., 1962. Ostracoda - Myodocopa, Part I: Cypridiniformes - Cypridinidae. Dana Rep. Carlsb. Found. No 57, pp. 1–414. Pytkowicz, R.M., 1970. On the carbonate compensation depth in the Pacific Ocean. Geochim. Cosmochim. Acta 34, 836–839. Rudjakov, J.A., 1961. A new ostracod species of the family Cytheridae from the ultraabyssal depths of the Java trench. Tr. Instituta Okeanol. Moskau 51, 116–120. Schlitzer, R., 2012. Ocean Data View 4. http://odv.awi.de. Schmiedl, G., Mackensen, A., Miiller, P.J., 1997. Recent benthic foraminifera from the eastern South Atlantic Ocean: dependence on food supply and water masses. Mar. Micropaleontol. 32, 249–287. Schornikov, E.I., 1975. Ostracod fauna of the intertidal zone in the vicinity of the Seto Marine Biological Laboratory. Publ. Seto Mar. Biol. Lab. 22, 1–30. Schornikov, E.I., 1976. Adaption pathways of Ostracoda to seistonophagy. Abhandlungen und Verhandlungen des Naturwissenschaftlichen Vereins Hambg. 18–19, 247–257. Schornikov, E.I., 1980. A review of the genus Zabythocypris (Ostracoda, Bairdiacea). Zool. Zhurnal 59, 186–198. Schornikov, E.I., 1981. Ostracods of the Family Bythocytheridae of Far Eastern Seas. Nauka, Moscow, pp. 278. Schornikov, E.I., 1987. Two new subgenera of bythocytherid ostracodes. Zool. Zhurnal 66, 996–1004. Sokolova, M.N., 1981. On characteristic features of the deep-sea benthic eutrophic regions of the World Ocean. Proc. P.P. Shirshov Inst. Oceanol. 115, 5–13 (in Russian). Sulpis, O., Boudreau, B.P., Mucci, A., Jenkins, C., Trossman, D.S., Arbic, B.K., Key, R.M., 2018. Current CaCO3 dissolution at the seafloor caused by anthropogenic CO2. Proc. Natl. Acad. Sci. https://doi.org/10.1073/PNAS.1804250115. 201804250. Ushakov, P.V., 1952. Study of deep-sea fauna. Priroda 6, 100–102 (in Russian). Valencia, M., 1973. Calcium Carbonate and Gross-Size Analysis of Surface Sediments, Western Equatorial Pacific I. Pacific Sci. 27, 290–303. Vinyard, G., 1979. An ostracod (Cypridopsis vidua) can reduce predation from fish by resisting digestion. Am. Midl. Nat. 102, 188–190. Wang, P., Wang, L., Bian, Y., Jian, Z., 1995. Late Quaternary paleoceanography of the South China Sea: surface circulation and carbonate cycles. Mar. Geol. 127, 145–165. https://doi.org/10.1016/0025-3227(95)00008-M. Whatley, R.C., 1996. The bonds of things unloosed the contribution of Ostracods to our understanding of deep sea events and processes. In: Moguilevsky, A., Whatley, R.C. (Eds.), Microfossils and Oceanic Environments. University of Wales, pp. 3–26. Yasuhara, M., Cronin, T.M., Martínez Arbizu, P., 2008. Abyssal ostracods from the South and Equatorial Atlantic Ocean: biological and paleoceanographic implications. Deep Sea Res. Part I Oceanogr. Res. Pap. 55, 490–497. https://doi.org/10.1016/j.dsr.2008. 01.004. Yasuhara, M., Hunt, G., Okahashi, H., 2019. Quaternary deep-sea ostracods from the north-western Pacific Ocean: global biogeography and Drake-Passage, Tethyan, Central American and Arctic pathways. J. Syst. Palaeontol. 17, 91–110. https://doi. org/10.1080/14772019.2017.1393019. Zenkevitch, L.A., 1963. Biology of the Seas of the U.S.S.R. George Allen and Unwin Ltd., London.

org/10.1016/j.tree.2009.09.009. Jażdżewska, A., 2015. Kuril-Kamchatka deep sea revisited – insights into the amphipod abyssal fauna. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 294–300. https://doi. org/10.1016/j.dsr2.2014.08.008. Jellinek, T., Swanson, K.M., Mazzini, I., 2006. Is the cosmopolitan model still valid for deep-sea podocopid ostracods? With the discussion of two new species of the genus PseudobosquetinaGuernet & Moullade, 1994 and Cytheropteron testudo (Ostracoda) as case studies. Senckenbergiana Maritima 36, 29–50. Kamenev, G.M., 2013. Species composition and distribution of bivalves in bathyal and abyssal depths of the Sea of Japan. Deep Sea Res. Part II Top. Stud. Oceanogr. 86–87, 124–139. https://doi.org/10.1016/j.dsr2.2012.08.004. Kamenev, G.M., 2014. Two new species of the genus Silicula (Bivalvia: Siliculidae) from the northwestern Pacific, with notes on Silicula sandersi (Bernard, 1989) and Propeleda soyomaruae (Okutani, 1962). Malacologia 57, 255–277. https://doi.org/10. 4002/040.057.0201. Kamenev, G.M., 2015. Composition and distribution of bivalves of the abyssal plain adjacent to the Kuril-Kamchatka Trench (Pacific Ocean). Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 188–197. https://doi.org/10.1016/j.dsr2.2014.08.005. Kamenev, G.M., 2018a. Three new species of the genus Hyalopecten (Bivalvia: Pectinidae) from the abyssal and hadal zones of the North-western Pacific Ocean. J. Mar. Biol. Assoc. United Kingdom 98, 357–374. https://doi.org/10.1017/ S0025315416001387. Kamenev, G.M., 2018b. Four new species of the family Propeamussiidae (Mollusca: Bivalvia) from the abyssal zone of the northwestern Pacific, with notes on Catillopecten squamiformis (Bernard, 1978). Mar. Biodivers. 48, 647–676. https:// doi.org/10.1007/s12526-017-0821-1. Kamenev, G.M., 2018c. Bivalve molluscs of the abyssal zone of the Sea of Okhotsk: Species composition, taxonomic remarks, and comparison with the abyssal fauna of the Pacific Ocean. Deep-Sea Res. II 154, 230–248. https://doi.org/10.1016/j.dsr2. 2017.10.006. Kamenev, G.M., 2019. Bivalve mollusks of the Kuril-Kamchatka Trench, Northwest Pacific Ocean: species composition, distribution and taxonomic remarks. Prog. Oceanogr. 176. https://doi.org/10.1016/j.pocean.2019.102127. Karanovic, I., Brandão, S.N., 2012. Review and phylogeny of the Recent Polycopidae (Ostracoda, Cladocopina), with descriptions of nine new species, one new genus, and one new subgenus from the deep South Atlantic. Mar. Biodivers. 42, 329–393. https://doi.org/10.1007/s12526-012-0116-5. Karanovic, I., Brandão, S.N., 2015. Biogeography of deep-sea wood fall, cold seep and hydrothermal vent Ostracoda (Crustacea), with the description of a new family and a taxonomic key to living Cytheroidea. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 76–94. https://doi.org/10.1016/j.dsr2.2014.09.008. Kennett, J.P., 1966. Foraminiferal evidence of a shallow calcium carbonate solution boundary, Ross Sea, Antarctica. Science 153, 191–193. Keyser, D., Walter, R., 2004. Calcification in Ostracodes. Rev. Española Micropaleontol. 36, 1–11. Knudsen, J., 1970. The systematic and biology of abyssal and hadal Bivalvia. Galathea Rep. 11, 1–238. Kornicker, L.S., 1975. Antarctic Ostracoda (Myodocopina). Smithson. Contrib. Zool. 1–720. Krylova, E.M., Kamenev, G.M., Vladychenskaya, I.P., Petrov, N.B., 2015. Vesicomyinae (Bivalvia: Vesicomyidae) of the Kuril-Kamchatka Trench and adjacent abyssal regions. Deep Sea Res. Part II Top. Stud. Oceanogr. 111, 198–209. https://doi.org/10. 1016/j.dsr2.2014.10.004. Kussakin, O.G., 1971. Additions to the fauna of isopods (Crustacea, Isopoda) of the KurileKamchatka Trench. Part III. Flabellifera and Valvifera. Tr. Instituta Okeaonogiya Akad. Nauk SSSR Mosc. 92, 239–273. Lee, G.H., Park, S.C., Kim, D.C., 2000. Fluctuations of the calcite compensation depth (CCD) in the East Sea (Sea of Japan). Geo-Marine Lett. 20, 20–26. https://doi.org/10. 1007/s003670000029. Levin, L.A., Gooday, A.J., 2003. The deep Atlantic Ocean. In: In: Tyler, P.A. (Ed.), Ecosystems of the Deep Oceans. Ecosystems of the World, vol. 28. Elsevier Science B.V., Amsterdam, pp. 111–178. Lopez, L.C.S., Rodrigues, P.J.F.P., Rios, R.I., 1999. Frogs and snakes as phoretic dispersal agents of bromeliad ostracods (Limnocytheridae : Elpidium) and annelids (Naididae : Dero). Biotropica 31, 705–708. Lopez, L.C.S., Gonçalves, D.A., Mantovani, A., Rios, R.I., 2002. Bromeliad ostracods pass through amphibian (Scinaxax perpusillus) and mammalian guts alive. Hydrobiologia 485, 209–211. https://doi.org/10.1023/A:1021315223774. Mackensen, A., Fütterer, D.K., Grobe, H., Schmiedl, G., 1993. Benthic foraminiferal assemblages from the eastern South Atlantic Polar Front region between 35° and 57°S: distribution, ecology and fossilization potential. Mar. Micropaleontol. 22, 33–69. https://doi.org/10.1016/0377-8398(93)90003-G. Mackensen, A., Grobe, H., Kuhn, G., Fütterer, D.K., 1990. Benthic foraminiferal assemblages from the eastern Weddell Sea between 68 and 73°S: distribution, ecology and fossilization potential. Mar. Micropaleontol. 16, 241–283. https://doi.org/10.1016/ 0377-8398(90)90006-8. Maddocks, R.F., 1969. Revision of recent Bairdiidae (Ostracoda). U.S. Natl. Museum Bull. 296, 1–126.

15