Andrew J. Gooday

First insights into the biodiversity and biogeography of the Southern Ocean deep sea

Shallow marine benthic communities around Antarctica show high levels of endemism, gigantism, slow growth, longevity and late maturity, as well as adaptive radiations that have generated considerable biodiversity in some taxa. The deeper parts of the Southern Ocean exhibit some unique environmental features, including a very deep continental shelf and a weakly stratified water column, and are the source for much of the deep water in the world ocean. These features suggest that deep-sea faunas around the Antarctic may be related both to adjacent shelf communities and to those in other oceans. Unlike shallow-water Antarctic benthic communities, however, little is known about life in this vast deep-sea region. Here, we report new data from recent sampling expeditions in the deep Weddell Sea and adjacent areas (748–6,348 m water depth) that reveal high levels of new biodiversity; for example, 674 isopods species, of which 585 were new to science. Bathymetric and biogeographic trends varied between taxa. In groups such as the isopods and polychaetes, slope assemblages included species that have invaded from the shelf. In other taxa, the shelf and slope assemblages were more distinct. Abyssal faunas tended to have stronger links to other oceans, particularly the Atlantic, but mainly in taxa with good dispersal capabilities, such as the Foraminifera. The isopods, ostracods and nematodes, which are poor dispersers, include many species currently known only from the Southern Ocean. Our findings challenge suggestions that deep-sea diversity is depressed in the Southern Ocean and provide a basis for exploring the evolutionary significance of the varied biogeographic patterns observed in this remote environment.

Deep-sea benthic foraminiferal species which exploit phytodetritus: Characteristic features and controls on distribution

Previous biological studies in the Northeast Atlantic have suggested that phytodetrital aggregates, which originate in the euphotic zone and settle rapidly to the seafloor following the spring bloom, constitute an important microhabitat and food source for certain bathyal and abyssal benthic foraminifera, including the rotaliidsAlabaminella weddellensis, Epistominella exigua, E. pusilla and the allogromiidTinogullmia riemanni. New data from a site at 4850 m depth on the Porcupine Abyssal Plain (49°N, 16°30′W), where phytodetritus deposition is an important phenomenon, support these observations. Here, the live foraminiferal populations which inhabit phytodetrital aggregates are dominated byE. exigua; A. weddellensis andT. riemanni are also abundant. Such species are much less common at a more southerly site on the Madeira Abyssal Plain (31°N, 21°W; 4940 m) where only traces of phytodetritus have been observed. The most common calcareous members of these assemblages share several characteristics. They have small tests with trochospiral coiling (indicating an epifaunal microhabitat preference) and thin, smooth, transparent or translucent walls. Almost certainly, they are opportunists, adapted to a fluctuating nutrient supply and able to grow and reproduce rapidly when a suitable food source (phytodetritus) is present. The best known species,Epistominella exigua, is abundant in areas of the Northeast Atlantic where phytodetritus deposition is known or believed to occur. It is tentatively suggested that the distribution and abundance ofE. exigua is controlled largely by the presence of this organic material on the seafloor.

Biological responses to seasonally varying fluxes of organic matter to the ocean floor: a review

Deep-sea benthic ecosystems are sustained largely by organic matter settling from the euphotic zone. These fluxes usually have a more or less well-defined seasonal component, often with two peaks, one in spring/early summer, the other later in the year. Long time-series datasets suggest that inter-annual variability in the intensity, timing and composition of flux maxima is normal. The settling material may form a deposit of “phytodetritus” on the deep-seafloor. These deposits, which are most common in temperate and high latitude regions, particularly the North Atlantic, evoke a response by the benthic biota. Much of our knowledge of these responses comes from a few time-series programmes, which suggest that the nature of the response varies in different oceanographic settings. In particular, there are contrasts between seasonal processes in oligotrophic, central oceanic areas and those along eutrophic continental margins. In the former, it is mainly “small organisms” (bacteria and protozoans) that respond to pulsed inputs. Initial responses are biochemical (e.g. secretion of bacterial exoenzymes) and any biomass increases are time lagged. Increased metabolic activity of small organisms probably leads to seasonal fluctuations in sediment community oxygen consumption, reported mainly in the North Pacific. Metazoan meiofauna are generally less responsive than protozoans (foraminifera), although seasonal increases in abundance and body size have been reported. Measurable population responses by macrofauna and megafauna are less common and confined largely to continental margins. In addition, seasonally synchronised reproduction and larval settlement occur in some larger animals, again mainly in continental margin settings. Although seasonal benthic responses to pulsed food inputs are apparently widespread on the ocean floor, they are not ubiquitous. Most deep-sea species are not seasonal breeders and there are probably large areas, particularly at abyssal depths, where biological process rates are fairly uniform over time. As with other aspects of deep-sea ecology, temporal processes cannot be encapsulated by a single paradigm. Further long time-series studies are needed to understand better the nature and extent of seasonality in deep-sea benthic ecosystems.

Deep-Sea Biodiversity in the Mediterranean Sea: The Known, the Unknown, and the Unknowable

Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.

Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas

Previous work has shown that some foraminiferal species thrive in organically enriched, oxygen-depleted environments. Here, we compare ‘live’ (stained) faunas in multicorer samples (0–1 cm layer) obtained at two sites on the Oman margin, one located at 412 m within the oxygen minimum zone (OMZ) (O2=0.13 ml l?1), the other located at 3350 m, well below the main OMZ (O2~3.00 ml l?1). While earlier studies have focused on the hard-shelled (predominantly calcareous) foraminifera, we consider complete stained assemblages, including poorly known, soft-shelled, monothalamous forms. Densities at the 412-m site were much higher (16,107 individuals.10 cm?2 in the >63-m fraction) than at the 3350-m site (625 indiv.10 cm?2). Species richness (E(S100)), diversity (H?, Fishers Alpha index) and evenness (J?) were much lower, and dominance (R1D) was higher, at 412 m compared with 3350 m. At 412 m, small calcareous foraminifera predominated and soft-shelled allogromiids and sacamminids were a minor faunal element. At 3350 m, calcareous individuals were much less common and allogromiids and saccamminids formed a substantial component of the fauna. There were also strong contrasts between the foraminiferal macrofauna (>300-m fraction) at these two sites; relatively small species of Bathysiphon, Globobulimina and Lagenammina dominated at 412 m, very large, tubular, agglutinated species of Bathysiphon, Hyperammina, Rhabdammina and Saccorhiza were important at 3350 m. Our observations suggest that, because they contain fewer soft-shelled and agglutinated foraminifera, a smaller proportion of bathyal, low-oxygen faunas is lost during fossilization compared to faunas from well-oxygenated environments. Trends among foraminifera (>63 m fraction) in the Santa Barbara Basin (590 and 610 m depth; O2=0.05 and 0.15 ml l?1 respectively), and macrofaunal foraminifera (>300 m) on the Peru margin (300–1250 m depth; O2=0.02–1.60 ml l?1), matched those observed on the Oman margin. In particular, soft-shelled monothalamous taxa were rare and large agglutinated taxa were absent in the most oxygen-depleted ( Foraminifera often outnumber metazoans (both meiofaunal and macrofaunal) in bathyal oxygen-depleted settings. However, although phylogenetically distant, foraminifera and metazoans exhibit similar population responses to oxygen depletion; species diversity decreases, dominance increases, and the relative abundance of the major taxa changes. The foraminiferal macrofauna (>300 m) were 5 times more abundant than the metazoan macrofauna at 412 m on the Oman margin but 16 times more abundant at the 3350 m site. Among the meiofauna (63–300 m), the trend was reversed; foraminifera were 17 times more abundant than metazoan taxa at 412 m but only 1.4 times more abundant at 3350 m. An abundance of food combined with oxygen levels which are not depressed sufficiently to eliminate the more tolerant taxa, probably explains why foraminifera and macrofaunal metazoans flourished at the 412-m site, perhaps to the detriment of the metazoan meiofauna.

THE ROLE OF BENTHIC FORAMINIFERA IN DEEP-SEA FOOD WEBS AND CARBON CYCLING

Benthic foraminifers are a major element in deep-sea sediment and hard-substrate communities, sometimes accounting for 50% or more of eukaryotic biomass. They feed at a low trophic level, consuming mainly planktonic and other detritus and bacteria. Some species have metabolic adaptations enabling them to respond quickly to pulsed detrital inputs with rapid rates of reproduction and growth. These foraminifers probably assist microorganisms in the breakdown of fresh detrital material, while others are deposit feeders which convert more refractory organic substances into biomass. DOM uptake may be important, although no data exist as yet to substantiate this. Foraminifers are consumed by a wide variety of organisms, including selective and non-selective deposit feeders and specialised predators, and probably represent an important link between lower and higher levels of deep-sea food webs. A variety of non-trophic interactions between metazoans and foraminifers, for example, the provision of physical substrates, may facilitate access to enhanced food supplies. Thus, foraminifera playa largely unquantified but potentially significant role in deep-sea carbon cycling

Cenozoic deep-sea benthic foraminifers: Tracers for changes in oceanic productivity?

From late middle Eocene through earliest Oligocene, high-latitude regions cooled, and by the end of the period, continental ice sheets existed in Antarctica. Diversity of planktonic microorganisms declined, and modern groups of terrestrial vertebrates originated. Coeval faunal changes in deep-sea benthic foraminifers have been related to cooling of deep waters and increased oxygenation. Cooling, however, occurred globally, whereas species richness declined at high latitudes and not in the tropics. The late Eocene and younger lower-diversity, high-latitude faunas typically contain common Epistominella exigua and Alabaminella weddellensis , opportunistic phytodetritus-exploiting species that indicate a seasonally fluctuating input of organic matter to the sea floor. We speculate that the species-richness gradient and increase in abundance of phytodetritus-exploiting species resulted largely from the onset of a more unpredictable and seasonally fluctuating food supply, especially at high latitudes.

The evolution of early Foraminifera

Fossil Foraminifera appear in the Early Cambrian, at about the same time as the first skeletonized metazoans. However, due to the inadequate preservation of early unilocular (single-chambered) foraminiferal tests and difficulties in their identification, the evolution of early foraminifers is poorly understood. By using molecular data from a wide range of extant naked and testate unilocular species, we demonstrate that a large radiation of nonfossilized unilocular Foraminifera preceded the diversification of multilocular lineages during the Carboniferous. Within this radiation, similar test morphologies and wall types developed several times independently. Our findings indicate that the early Foraminifera were an important component of Neoproterozoic protistan community, whose ecological complexity was probably much higher than has been generally accepted.

Does Presence of a Mid-Ocean Ridge Enhance Biomass and Biodiversity?

In contrast to generally sparse biological communities in open-ocean settings, seamounts and ridges are perceived as areas of elevated productivity and biodiversity capable of supporting commercial fisheries. We investigated the origin of this apparent biological enhancement over a segment of the North Mid-Atlantic Ridge (MAR) using sonar, corers, trawls, traps, and a remotely operated vehicle to survey habitat, biomass, and biodiversity. Satellite remote sensing provided information on flow patterns, thermal fronts, and primary production, while sediment traps measured export flux during 2007–2010. The MAR, 3,704,404 km2 in area, accounts for 44.7% lower bathyal habitat (800–3500 m depth) in the North Atlantic and is dominated by fine soft sediment substrate (95% of area) on a series of flat terraces with intervening slopes either side of the ridge axis contributing to habitat heterogeneity. The MAR fauna comprises mainly species known from continental margins with no evidence of greater biodiversity. Primary production and export flux over the MAR were not enhanced compared with a nearby reference station over the Porcupine Abyssal Plain. Biomasses of benthic macrofauna and megafauna were similar to global averages at the same depths totalling an estimated 258.9 kt C over the entire lower bathyal north MAR. A hypothetical flat plain at 3500 m depth in place of the MAR would contain 85.6 kt C, implying an increase of 173.3 kt C attributable to the presence of the Ridge. This is approximately equal to 167 kt C of estimated pelagic biomass displaced by the volume of the MAR. There is no enhancement of biological productivity over the MAR; oceanic bathypelagic species are replaced by benthic fauna otherwise unable to survive in the mid ocean. We propose that globally sea floor elevation has no effect on deep sea biomass; pelagic plus benthic biomass is constant within a given surface productivity regime.

Meiobenthos of the deep Northeast Atlantic

This chapter throws the attention on the meiobenthos of the deep northeast Atlantic. The main purpose of this chapter is to summarize new results from an area lying between 15°N and 53°N and extending from the continental margin of western Europe and northwest Africa to the Mid-Atlantic Ridge. It considers first the nature and scope of meiofaunal research in the northeast Atlantic and then discuss the environmental parameters, which are believed to influence meiofaunal organisms. This chapter then discusses the various types and scales of pattern observed among meiofaunal populations within the study area, progressing from the large-scale bathymetric and latitudinal trends and then to small-scale horizontal patterns within particular areas. Faunal densities and faunal composition are considered separately and compared with data from other regions. This chapter also deals with the distribution of meiofauna within sediment profiles and the temporal variability of populations. This chapter concludes by discussing the recent review of deep-sea meiofauna, which focused mainly on the abundance and biomass data from different oceans and on the relationship between the biomass of the meiofauna and that of other faunal components