The zoogeography, diversity and origin of the deep-sea protobranch bivalves of the Atlantic: The epilogue

doi:10.1016/S0079-6611(96)00011-0

Progress in Oceanography

Volume 38, Issue 2, 1996, Pages 95-153

https://doi.org/10.1016/S0079-6611(96)00011-0 Get rights and content

Abstract

From the detailed examination of more than 80,000 specimens comprising of 100 species and 9 subspecies of protobranch bivalves collected from the deep-sea floor of the Atlantic, it has been possible for the first time to determine and compare the diversity and distribution patterns in ten abyssal basins of an abyssal higher taxon. In addition, the general ecological characteristics of a major deep-sea taxon which has one of the longest known geological histories are presented. Overall this has provided an opportunity to debate the origin and evolution of the Protobranchia in the Atlantic following its formation ca 130Ma ago.

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Cited by (91)

Form and function of the mantle edge in Protobranchia (Mollusca: Bivalvia)
2022, Zoology
Citation Excerpt :
Independently of its function, the periostracum can also provide useful characters for systematics (Salas et al., 2012, for Astartidae). The subclass Protobranchia is one of the less well known bivalve clades, probably because most of its ca. 750 species are inhabitants of the deep sea (Allen and Sanders, 1996; Zardus, 2002; Zardus et al., 2006). The highest level of genetic and morphological divergence among protobranchs is found in the bathyal zone, suggesting that the bathyal may be a more active area of species formation than the abyssal zone, probably due to its strong biotic and abiotic heterogeneity (Etter et al., 2005).
We analyzed, by optical and transmission electron microscopy, the morphology and function of the mantle edge, including the formation of the periostracum, of ten species of protobranchs. Five species from the order Nuculida, four species from the order Nuculanida and one species from the order Solemyida were studied. A second outer fold, which seems to function as a template for the internal marginal crenulations of the valves, is present in the crenulated species of Nucula. The minute non-crenulated Ennucula aegeensis shows the glandular basal cells displaced toward the periostracal groove, resembling a minute additional fold between the outer and middle folds. Intense secretion of glycocalyx, together with active uptake of particles, have been observed in the inner epithelium of the middle mantle fold and the whole epithelium of the inner mantle fold in all the studied species. Contrary to the rest of the bivalves, all the protobranchs analyzed have two basal cells involved in the formation of the external nanometric pellicle of the periostracum, a character that would support the monophyly of protobranchs. A three-layered pattern is the general rule for the periostracum in protobranchs, like for other bivalves. The presence of pouches of translucent layer inside the tanned dark layer under periostracal folds is characteristic of the species with a folded periostracum; its function is unclear but could give flexibility to the periostracum. The non-nacreous internal shell layer and the presence of translucent pouches under periostracal folds in Sarepta speciosa resemble those found in nuculanids. However, the free periostracum is rather similar to those of N. hanleyi and E. aegeensis, with a continuous vesicular layer. All the latter supports the inclusion of Sarepta in the order Nuculanida but could indicate either a basal lineage or that the translucent vesicular layer is an adaptive trait.
Biodiversity and distribution patterns of deep-sea fauna along the temperate NW Pacific
2020, Progress in Oceanography
The deep NW Pacific has been intensively analyzed in the last decade, during an international collaboration between German and Russian scientists, which has resulted in a vast, unique collection of material from previously unexplored areas. Until now, the environmental forces that could be driving species richness patterns in the deep NW Pacific have not been explored widely. Therefore, in this paper, we utilize new species distribution data from four deep-sea expeditions to the NW Pacific (2010–2016), which include the Sea of Japan, Sea of Okhotsk, the abyssal plain adjacent to the Kuril-Kamchatka Trench (KKT) and the KKT, to better understand species connectivity, biodiversity patterns, and distribution ranges in deep-sea benthos in this region. To determine the best environmental predictors driving these deep-sea species richness patterns, we applied generalized additive (GAMs) and linear models (GLMs). We calculated the total number of geographic distribution records, alpha (total number of species per 10,000 km² hexagonal cells) and gamma species richness (total number of species per 1° latitudinal bands), and expected number of species (rarefaction ES15). Our highest number of distribution records and gamma species richness during the last decade peaked at intermediate latitudes (42°−44°N) along the mesopelagic zone (500–1000 m) of the Sea of Japan and abyssopelagic zone (4000–6000 m) of the NW Pacific and KKT. When sampling bias was accounted for, the alpha species richness in bathypelagic zone (1000–4000 m) of Sea of Okhotsk and abyssopelagic zone (4000–6000 m) of the NW Pacific and KKT were as high as mesopelagic zone of the Sea of Japan. The similarity cluster analysis of species presence/absence in lower bathyal/hadal (3000–8500 m) revealed three distinct geographic regions including Sea of Japan, Sea of Okhotsk, and KKT in the NW Pacific. The eastern sector of the Sea of Okhotsk and western KKT had c. 50% of species in common. Several species of deep-sea Bivalves, such as Dacrydium rostriferum and Vesicomya pacifica, had the greatest latitudinal distribution ranges among all species. Echinoderm Ophiura leptoctenia, had instead, the broadest bathymetric distribution ranges compared to all other collected species. GAM models indicated that dissolved oxygen was the best explanatory variable for predicting numbers of species, closely followed by the model including all environmental variables plus topography. However, the GLM models of species richness, with latitudinal intervals of 1° and 5°, found that the topography and temperature were the best predictors of number of species. GLM model outputs indicated that a model that contains only the number of distribution records is, for all practical purposes, as good as any model that contains an environmental predictor. This study provides new insights on the NW Pacific deep-sea species richness patterns, where dissolved oxygen might play an important role, especially when considering the Oxygen Minimum Zones (OMZs) in the deep NW Pacific.
Biodiversity of echiurans (Echiura) of the Kuril-Kamchatka Trench area
2020, Progress in Oceanography
During KuramBio and KuramBioII (Kuril Kamchatka Biodiversity Studies) expeditions of 2012 and 2016 years, 12 sites across the Kuril-Kamchatka abyssal plain and 11 sites along Kuril-Kamchatka Trench area (KKT) were surveyed and sampled and benthic communities were investigated. Samples, which comprised over 300 echiurans from 12 species of 11 genera belonging to the family Bonelliidae and Thalassematidae, were collected. The family Bonelliidae is most common in abyssal and hadal environments in the world ocean with high abundances in all investigated regions, while Thalassematidae is reported first time from the hadal depth. Species identified as representative of the genera Maxmuelleria have been noted first time in Pacific. Previously known echiuran Bonellia pacifica suggested to be Pseudoikedella achaeta. The description of deep-water echiurans from the investigated areas is the second one based on complete specimens with living colouration. The descriptions provide new information on the distribution, abundance, morphology and taxonomic details of the species, which were previously noted from the northwestern Pacific and described from damaged or incomplete specimens. The knowledge of the geographic ranges of these genera are expanded and discussed.
Endemicity and community composition of marine species along the NW Pacific and the adjacent Arctic Ocean
2019, Progress in Oceanography
Citation Excerpt :
However, Carney (2005) suggested that many species often possess restricted vertical ranges despite the potential for broad horizontal distribution ranges because abiotic and biotic factors vary greatly with depth. For example, about half of the deep-sea bivalves and gastropods in the North Atlantic Ocean have wide distribution ranges along the entire basin (Allen and Sanders, 1996; Rex et al., 2005). Studies have argued that in some unique deep-sea habitats such as seamounts, hard rock substrate, and coral/sponge reefs, the distribution ranges of species are narrow because their geochemical cycles and biological activity promotes restricted ranges and isolation, generating highly endemic faunas (McClain et al., 2009; Richer de Forges et al., 2000).
The NW Pacific lies in the most productive, rich, and diverse region of the World Ocean. The NW Pacific includes several shallow-water oceanic islands and deep-sea basins differing in depths, hydrology and isolation. The adjacent Arctic Ocean includes the northern Bering and southern Chukchi Sea, areas of high productivity characterized by short food chains and shallow depths. Despite the NW Pacifićs high species richness, characterization of species diversity and species composition in this region remains poorly explored and/or unknown. Here we attempt to discover how geographic boundaries and depth shape current community assemblages in this area by limiting species richness and geographic distribution ranges. All geographic distribution records were extracted from Ocean Biogeographic Information System (OBIS) and Global Biodiversity Information Facility (GBIF). Distribution data were then cleaned, resulting in a final dataset including 324,916 distribution records of 17,414 species ranging from 0 to 10,900 m depth. We calculated the rate of endemicity and alpha species richness per ecoregion. We also showed how species composition and community structure varies between the tropical and temperate NW Pacific and adjacent Arctic Ocean when sampling bias is accounted for using rarefaction. After accounting for sampling bias, the Eastern Philippines had the greatest species richness (for both pelagic and benthic species) in the NW Pacific and its adjacent Arctic Ocean, and the lowest species richness was observed in Papua. Despite the high species richness in the Eastern Philippines, the Yellow Sea and Gulf of Tonkin had the highest benthic species endemicity rates (ca. 70%) and Aleutian Islands had the highest pelagic endemicity rate (ca. 45%) among all other ecoregions. In the NW Pacific, Chordata, Arthropoda, and Mollusca contributed more than 50% to the species composition of the community. In the Arctic Ocean, Arthropoda, Annelida, and Mollusca were the dominant taxa comprising ca. 82% of the species community. Two significantly distinguished clusters (North and South clusters) were identified based on species similarity analysis including ecoregions of the (1) polar Arctic Ocean and temperate North NW Pacific, and (2) tropical and sub-tropical NW Pacific. We also calculated marine species richness hotspots (actual and expected ES50) and centers of endemism in the NW Pacific and adjacent Arctic Ocean. These analyses reveal an opportunity for marine conservation planning effort as reporting species richness and endemicity hotspots could be highly effective in pinpointing and preventing biodiversity loss.
Depth zonation of Northwest Pacific deep-sea macrofauna
2019, Progress in Oceanography
Areas of the Northwest (NW) Pacific have been investigated in the last century from board of the Russian RV Vityaz. During the past decade intensive collaboration between German and Russian scientists has yielded a wealth of precious material partly from unknown areas. The samples are comparable and were retrieved using comparative epibenthic sledge (EBS) deployments following a standardized sampling approach. In the present paper we investigate a large number of EBS samples (76) from a widespread geographic area.
Macrofaunal high-taxonomic-level taxa composition is analysed based on four joint expeditions performed between 2010 and 2016, led by German and Russian teams in the NW Pacific, the Sea of Japan, the Sea of Okhotsk, and the Kuril-Kamchatka Trench and adjacent abyssal plain. In total, 410,279 invertebrates were sampled with an epibenthic sledge and more than half of all animals were collected in the Sea of Japan (240,803 individuals). Arthropods, represented by crustaceans, were dominant throughout all geographic areas (199,044 ind.), followed by Annelida (84,751 ind.), Echinodermata (46,317 ind.), and Mollusca (43,391 ind.). Within these phyla, eleven taxa occurred with more than 10,000 individuals in the samples from all geographic areas. The most numerous were the Peracarida (104,139 ind., represented by Isopoda [42,511 ind.], Amphipoda [29,375 ind.], Cumacea [16,364 ind.], Tanaidacea [15,889 ind.]), followed by Polychaeta (84,751 ind.), Copepoda 76,496 ind., Bivalvia (36,286 ind.), Ophiuroidea (34,818 ind.), Nematoda (24,968 ind.), Ostracoda (11,304 ind.), and Holothuroidea (10,772 ind.). The pattern of occurrence per taxon varied between geographic areas. In general, Bivalvia and Holothuroidea were more frequently recorded from hadal stations, but no significant differences could be observed between geographic areas (Sea of Japan, Sea of Okhotsk, and open NW Pacific) at high level taxa (classes, subclasses, superorders) when community composition is compared and depth differences are taken into account. However, significant differences between all depth zones (p < 0.05) were revealed for both PERMANOVA and non-parametric pairwise t-tests.
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
2018, Deep-Sea Research Part II: Topical Studies in Oceanography
Citation Excerpt :
The oceans cover 71% of our planet's surface, with 50% below 3000 m depth (Ramirez-Llodra et al., 2010). Thus, the deep sea represents the largest ecosystem on the planet and it supports one of the highest levels of biodiversity (Allen and Sanders, 1996; Hessler and Sanders, 1967; Rex et al., 2005; Stuart et al., 2003). Deep-water seas with abyssal depths (in excess of 3000 m), separated from world's oceans by a threshold, are distinct deep-sea ecosystems, along with abyssal plains, seamounts, mid-ocean ridges, and hadal trenches (Allen and Sanders, 1996; Knudsen, 1970, 1979; Ramirez-Llodra et al., 2010).
SokhoBio expedition Until recently hardly anything was known about the abyssal bivalve fauna of the Sea of Okhotsk, which communicates with the Pacific Ocean via many straits between the Kuril Islands with a maximum depth of 2318 m in Bussol Strait, and about its similarity with the deep-water fauna of the Pacific. Investigation of the materials collected by the SokhoBio Russian-German deep-sea expedition (RV “Akademik M.A. Lavrentyev”, 2015), and two Russian expeditions (RV “Toporok”, 1948; RV “Vityaz”, 1949) from the bottom of the Kuril Basin of the Sea of Okhotsk (2850–3366 m depth) revealed a rich fauna of bivalves including 25 species belonging to 12 families, of which only 12 species (48.0%) were determined to the species level. Nine species (Poroleda extenuata, Katadesmia vincula, Dacrydium rostriferum, Bathyarca imitata, Catillopecten squamiformis, Channelaxinus excavata, Vesicomya pacifica, Cuspidaria cf. abyssopacifica, Myonera garretti) were first records for the Sea of Okhotsk. The richest families were Thyasiridae (7 species) and Cuspidariidae (6 species). The high diversity and richness of the bivalve fauna on the bottom of the Kuril Basin are probably caused by the favorable trophic conditions. The Kuril Basin is characterized by very high rates of sedimentation and high content of organic matter in the sediments. For estimation of connections between deep-water faunas of the Sea of Okhotsk and the Pacific Ocean, the SokhoBio expedition performed 1 station at the maximum depth of the Bussol Strait and 2 stations (3342–3432 and 4679–5013 m) on the Pacific slope of the Kuril Islands opposite to the Bussol Strait, where 24 species belonging to 13 families were found. Among the 25 species found in the deep part of the Kuril Basin more than half of species (17 species, 68%) occur in the Pacific Ocean. Most of them are widespread in the northern Pacific and are eurybathic bathyal-abyssal species. This probably allows them to penetrate into the Sea of Okhotsk through deep straits between the Kuril Islands. Photographs and taxonomic remarks are provided for all identified species (15) that were found in the Sea of Okhotsk and/or the Pacific Ocean. Taxonomic decisions herein: Nuculana aikawai Habe, 1958 and Nuculana sagamiensis Okutani, 1962 are synonymized with Nuculana leonina (Dall, 1896); Arca (Bathyarca) nucleator Dall, 1908 is synonymized with Bathyarca imitata (Smith, 1885); for Leda extenuata Dall, 1897, a new combination is suggested, Poroleda extenuata (Dall, 1897).

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The zoogeography, diversity and origin of the deep-sea protobranch bivalves of the Atlantic: The epilogue

Abstract

Evolution of the protobranch bivalves

Philosophical Transactions of the Royal Society of London B

The ecology of deep-sea molluscs

A reclassification of the Recent genera of the subclass Protobranchia (Mollusca: Bivalvia)

Journal of Conchology

Studies on the deep-sea Protobranchia

The subfamily Ledellinae (Nuculanidae)

Bulletin of the British Museum (Natural History), Zoology

The functional morphology of the families Cuspidariidae and Poromyidae (Mollusca: Bivalvia) of the abyssal Atlantic

Philosophical Transactions of the Royal Society of London

On the functional morphology of the family Verticordiidae (Bivalvia) with descriptions of new species from the abyssal Atlantic

Philosophical Transactions of the Royal Society of London

Nucinella serrei (Protobranchia) a monomyarian solemyid and possible living actinodont

Malacologia

Studies on the deep-sea Protobranchia

The families Siliculidae and Lametilidae

Bulletin of the Museum of Comparative Zoology Harvard

Studies on the deep sea Protobranchia

The subfamily Spinulinae (family Nuculanidae)

Bulletin of the Museum of Comparative Zoology Harvard

Studies on the deep-sea Protobranchia (Bivalvia); the family Neilonellidae and the subfamily Nuculaninae

Bulletin of the British Museum (Natural History), Zoology

Studies on deep-sea Protobranchia (Bivalvia); the subfamily Yoldiellinae

Bulletin of the British Museum (Natural History), Zoology

The origin of the psychrosphere as recorded in deep-sea ostracode assemblages

Lethaia

In search of lost oceans; a paradox in discovery

Evidence from the Ostracoda of major events in the South Atlantic and world-wide over the past 80 million years

Paleogeography, biogeography and the history of the circulation of the Atlantic Ocean

Plate tectonics and paleocirculation: commotion in the ocean

Tectonophysics

Seasonal sedimentation of phytoplankton to the deep-sea benthos

Nature, London

The molluscan fauna of the Norwegian Sea and its relation to other faunas

Sarsia

Food of bottom fishes

Texas A & M University Oceanographic Studies

The Storegga Slide

Philosophical Transactions of the Royal Society of London

Zonation of fauna in the deep sea

Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature

Deep-Sea Research

Abyssal mollusks of the South Atlantic Ocean

Bulletin of the Museum of Comparative Zoology Harvard

Annotated list and bibliography of the abyssal marine molluscs of the world

Bulletin. National Museum of Canada

Some quantitative results on the benthic communities of the deep Norwegian Sea

Astarte

Role of biological disturbance in maintaining diversity in the deep sea

Deep-Sea Research

Antarctic and Sub-Antarctic Mollusca: Amphineura, Scaphapoda, Bivalvia

‘Discovery’ Reports

Antarctic benthos

Advances in Marine Biology

Reconstruction of Pangaea: breakup and dispersion of continents, Permian to present

Journal of Geophysical Research

Population differentiation decreases with depth in deep-sea gastropods

Deep-Sea Research

Morphology of abyssal mudwaves at project MUDWAVES sites in the Argentine Basin

Deep-Sea Research

Eocene echinoids and the Drake Passage

Nature, London

Biological rates in the deep sea: a perspective from studies on processes in the benethic boundary layer

Reviews in Aquatic Sciences

Benthic secondary production in the deep sea

Deep-sea biology: a natural history of the organisms at the deep sea floor

Deep-sea faunal zonation of benthos along the Beaufort-Bermuda transect in the northwestern Atlantic

Circulation of bottom waters in the southwestern South Atlantic

Deep-Sea Research

Species diversity in deep-sea communities

Trends in Ecology and Evolution

Deep-sea species richness: regional and local diversity estimates from quantitative bottom samples

The American Naturalist

Macrofaunal colonization of disturbed deep-sea environments and the structure of deep-sea benthic communities

Deep-Sea Research

Life histories and the role of disturbance

Deep-Sea Research

A similarity measure sensitive to the contribution of rare species and its use in investigation of variation in marine benthic communities