Description: © The Authors, 2010. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 7 (2010): 2851-2899, doi:10.5194/bg-7-2851-2010.

Description: The deep sea, the largest biome on Earth, has a series of characteristics that make this environment both distinct from other marine and land ecosystems and unique for the entire planet. This review describes these patterns and processes, from geological settings to biological processes, biodiversity and biogeographical patterns. It concludes with a brief discussion of current threats from anthropogenic activities to deep-sea habitats and their fauna. Investigations of deep-sea habitats and their fauna began in the late 19th century. In the intervening years, technological developments and stimulating discoveries have promoted deep-sea research and changed our way of understanding life on the planet. Nevertheless, the deep sea is still mostly unknown and current discovery rates of both habitats and species remain high. The geological, physical and geochemical settings of the deep-sea floor and the water column form a series of different habitats with unique characteristics that support specific faunal communities. Since 1840, 28 new habitats/ecosystems have been discovered from the shelf break to the deep trenches and discoveries of new habitats are still happening in the early 21st century. However, for most of these habitats the global area covered is unknown or has been only very roughly estimated; an even smaller – indeed, minimal – proportion has actually been sampled and investigated. We currently perceive most of the deep-sea ecosystems as heterotrophic, depending ultimately on the flux on organic matter produced in the overlying surface ocean through photosynthesis. The resulting strong food limitation thus shapes deep-sea biota and communities, with exceptions only in reducing ecosystems such as inter alia hydrothermal vents or cold seeps. Here, chemoautolithotrophic bacteria play the role of primary producers fuelled by chemical energy sources rather than sunlight. Other ecosystems, such as seamounts, canyons or cold-water corals have an increased productivity through specific physical processes, such as topographic modification of currents and enhanced transport of particles and detrital matter. Because of its unique abiotic attributes, the deep sea hosts a specialized fauna. Although there are no phyla unique to deep waters, at lower taxonomic levels the composition of the fauna is distinct from that found in the upper ocean. Amongst other characteristic patterns, deep-sea species may exhibit either gigantism or dwarfism, related to the decrease in food availability with depth. Food limitation on the seafloor and water column is also reflected in the trophic structure of heterotrophic deep-sea communities, which are adapted to low energy availability. In most of these heterotrophic habitats, the dominant megafauna is composed of detritivores, while filter feeders are abundant in habitats with hard substrata (e.g. mid-ocean ridges, seamounts, canyon walls and coral reefs). Chemoautotrophy through symbiotic relationships is dominant in reducing habitats. Deep-sea biodiversity is among of the highest on the planet, mainly composed of macro and meiofauna, with high evenness. This is true for most of the continental margins and abyssal plains with hot spots of diversity such as seamounts or cold-water corals. However, in some ecosystems with particularly "extreme" physicochemical processes (e.g. hydrothermal vents), biodiversity is low but abundance and biomass are high and the communities are dominated by a few species. Two large-scale diversity patterns have been discussed for deep-sea benthic communities. First, a unimodal relationship between diversity and depth is observed, with a peak at intermediate depths (2000–3000 m), although this is not universal and particular abiotic processes can modify the trend. Secondly, a poleward trend of decreasing diversity has been discussed, but this remains controversial and studies with larger and more robust data sets are needed. Because of the paucity in our knowledge of habitat coverage and species composition, biogeographic studies are mostly based on regional data or on specific taxonomic groups. Recently, global biogeographic provinces for the pelagic and benthic deep ocean have been described, using environmental and, where data were available, taxonomic information. This classification described 30 pelagic provinces and 38 benthic provinces divided into 4 depth ranges, as well as 10 hydrothermal vent provinces. One of the major issues faced by deep-sea biodiversity and biogeographical studies is related to the high number of species new to science that are collected regularly, together with the slow description rates for these new species. Taxonomic coordination at the global scale is particularly difficult, but is essential if we are to analyse large diversity and biogeographic trends. Because of their remoteness, anthropogenic impacts on deep-sea ecosystems have not been addressed very thoroughly until recently. The depletion of biological and mineral resources on land and in shallow waters, coupled with technological developments, are promoting the increased interest in services provided by deep-water resources. Although often largely unknown, evidence for the effects of human activities in deep-water ecosystems – such as deep-sea mining, hydrocarbon exploration and exploitation, fishing, dumping and littering – is already accumulating. Because of our limited knowledge of deep-sea biodiversity and ecosystem functioning and because of the specific life-history adaptations of many deep-sea species (e.g. slow growth and delayed maturity), it is essential that the scientific community works closely with industry, conservation organisations and policy makers to develop robust and efficient conservation and management options.

Description: This paper has been written under the umbrella of the Census of Marine Life synthesis initiative SYNDEEP, supported by the Alfred P. Sloan Foundation, Fondation Total and EuroCoML, which are gratefully acknowledged. ERLL is funded by the CoML-ChEss programme (A. P. Sloan Foundation) and Fondation Total. CRG acknowledges support from the CoMLChEss programme. LAL acknowledges support from the National Science Foundation and the CoML-COMARGE and ChEss programmes. DPT acknowledges funding from the CoML-FMAP programme. MV acknowledges the CoML-MAR-ECO programme (Sloan Foundation and NOAA).

Description: The mating behavior of deep-sea squids is shrouded in mystery. The squids for which mating has been observed use a hectocotylus, a modified arm, for the transfer of sperm packets called spermatophores. However, many deep-sea squid species lack a hectocotylus. We present the first in situ observations of mating behavior in a deep-sea squid that has no hectocotylus but instead uses an elongated terminal organ for the transfer of spermatangia, which are released from the spermatophores and burrow deeply into the female tissue. With remotely operated vehicles (ROVs), we observed two mating pairs of the deep-sea squid Pholidoteuthis adami in the Gulf of Mexico. The male adopted a peculiar position during mating, with its ventral side up and its posterior mantle above the female's head. While the male held the female in what looked like a firm grip, we observed the long terminal organ extending through the funnel of the male, contacting the female dorsal mantle. Examinations of museum specimens show that spermatangia burrow from the outer dorsal mantle into the inner dorsal mantle. This combination of serendipitous in situ observations and archived specimens can be a powerful tool for understanding the behavior of deep-sea animals.

Description: The deep-sea squid Grimalditeuthis bonplandi has tentacles unique among known squids. The elastic stalk is extremely thin and fragile, whereas the clubs bear no suckers, hooks or photophores. It is unknown whether and how these tentacles are used in prey capture and handling. We present, to our knowledge, the first in situ observations of this species obtained by remotely operated vehicles (ROVs) in the Atlantic and North Pacific. Unexpectedly, G. bonplandi is unable to rapidly extend and retract the tentacle stalk as do other squids, but instead manoeuvres the tentacles by undulation and flapping of the clubs’ trabecular protective membranes. These tentacle club movements superficially resemble the movements of small marine organisms and suggest the possibility that G. bonplandi uses aggressive mimicry by the tentacle clubs to lure prey, which we find to consist of crustaceans and cephalopods. In the darkness of the meso- and bathypelagic zones the flapping and undulatory movements of the tentacle may: (i) stimulate bioluminescence in the surrounding water, (ii) create low-frequency vibrations and/or (iii) produce a hydrodynamic wake. Potential prey of G. bonplandi may be attracted to one or more of these as signals. This singular use of the tentacle adds to the diverse foraging and feeding strategies known in deep-sea cephalopods.

Description: Many members of the benthic fauna of the Antarctic continental shelf share close phylogenetic relationships to the deep-sea fauna adjacent to Antarctica and in other ocean basins. It has been suggested that connections between the Southern Ocean and the deep sea have been facilitated by the presence of a deep Antarctic continental shelf coupled with submerging Antarctic bottom water and emerging circumpolar deep water. These conditions may have allowed ‘polar submergence’, whereby shallow Southern Ocean fauna have colonised the deep sea and ‘polar emergence’, whereby deep-sea fauna colonised the shallow Southern Ocean. A recent molecular study showed that a lineage of deep-sea and Southern Ocean octopuses with a uniserial sucker arrangement on their arms appear to have arisen via polar submergence. A distantly related clade of octopuses with a biserial sucker arrangement on their arms (historically placed in the genus Benthoctopus) is also present in the deep-sea basins of the world and the Southern Ocean. To date their evolutionary history has not been examined. The present study investigated the origins of this group using 3133 base pairs (bp) of nucleotide data from five mitochondrial genes (12S rRNA, 16S rRNA, cytochrome c oxidase subunit I, cytochrome c oxidase subunit III, cytochrome b) and the nuclear gene rhodopsin from at least 18 species (and 7 outgroup taxa). Bayesian relaxed clock analyses showed that Benthoctopus species with a high-latitude distribution in the Southern Hemisphere represent a paraphyletic group comprised of three independent clades. The results suggest that the Benthoctopus clade originated in relatively shallow Northern Hemisphere waters. Benthoctopus species distributed in the Southern Ocean are representative of polar emergence and occur at shallower depths than non-polar Benthoctopus species.