J. Copley

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Ecology goes underground

The functioning of terrestrial ecosystems seems to depend heavily on soil biodiversity. But what controls this diversity, and how will it fare in the global greenhouse? Jon Copley digs for some answers.

All at sea

The oceans are full of microorganisms, which are thought to cycle nutrients and mediate climate on a global scale. Despite these environmental consequences, marine microbial biodiversity remains poorly understood. Jon Copley reports.

Assessment of decadal-scale ecological change at a deep Mid-Atlantic hydrothermal vent and reproductive time-series in the shrimp Rimicaris exoculata

This study presents a comparison of distribution and abundance of dominant megafaunal species at the TAG hydrothermal mound on the Mid-Atlantic Ridge from 1994 to 2004. A geographical information system (GIS) database was compiled from georeferenced observations of faunal abundances at 534 locations on the TAG hydrothermal mound, determined by image analysis of ROV dive footage from November 2004. These data are compared with observations from submersible dives in 1994 to assess changes in the extent and population density of aggregations of the shrimp Rimicaris exoculata at the central black smokers of TAG. The GIS database was also used to assess changes in abundance and distribution of the anemone Maractis rimicarivora by simulating the path of a biotransect conducted in 1994 and 1995. There was no evidence of a decline in the extent of shrimp aggregations at the central black smokers of TAG between 1994 and 2004. This result indicates that occasional exposure to high-intensity submersible lighting, which took place during several scientific expeditions in the intervening period, does not pose an immediate conservation threat to populations of R. exoculata. Similarly, there were no significant differences in the distribution and abundance of anemones between 1994 and 2004. These results indicate a constancy in the identity, distribution and abundance of dominant species at TAG that contrasts with other vent sites where quantitative time-series have been established. The reproductive pattern of R. exoculata was also examined by dissection and direct measurement of oocytes from females collected in September 1994 and November 2004, providing the first comparison of reproductive development in samples from different months for this species. There was no significant difference in oocyte size–frequency distributions of females collected in these samples, indicating a lack of seasonal reproduction in R. exoculata.

The biogeography of the yeti crabs (Kiwaidae) with notes on the phylogeny of the Chirostyloidea (Decapoda: Anomura).

The phylogeny of the superfamily Chirostyloidea (Decapoda: Anomura) has been poorly understood owing to limited taxon sampling and discordance between different genes. We present a nine-gene dataset across 15 chirostyloids, including all known yeti crabs (Kiwaidae), to improve the resolution of phylogenetic affinities within and between the different families, and to date key divergences using fossil calibrations. This study supports the monophyly of Chirostyloidea and, within this, a basal split between Eumunididae and a Kiwaidae–Chirostylidae clade. All three families originated in the Mid-Cretaceous, but extant kiwaids and most chirostylids radiated from the Eocene onwards. Within Kiwaidae, the basal split between the seep-endemic Kiwa puravida and a vent clade comprising Kiwa hirsuta and Kiwa spp. found on the East Scotia and Southwest Indian ridges is compatible with a hypothesized seep-to-vent evolutionary trajectory. A divergence date estimate of 13.4–25.9 Ma between the Pacific and non-Pacific lineages is consistent with Kiwaidae spreading into the Atlantic sector of the Southern Ocean via the newly opened Drake Passage. The recent radiation of Kiwaidae adds to the list of chemosynthetic fauna that appear to have diversified after the Palaeocene/Eocene Thermal Maximum, a period of possibly widespread anoxia/dysoxia in deep-sea basins.

Reproductive biology of three caridean shrimp, Rimicaris exoculata , Chorocaris chacei and Mirocaris fortunata (Caridea: Decapoda), from hydrothermal vents

The caridean shrimp Rimicaris exoculata, Chorocaris chacei and Mirocaris fortunata , together with bathymodiolid mussels, dominate the vent fauna along the Mid-Atlantic Ridge. Vent shrimp show the characteristic reproductive patterns of caridean decapods. The gonads are paired organs overlying the digestive gland under the carapace. In the ovaries, the oogonia (∼20-30 μm diameter) proliferate in the germinal epithelium at the periphery of the gonad, developing into previtellogenic oocytes. The previtellogenic oocytes grow to 70-100 μm before undergoing vitellogenesis. The maximum size for mature oocytes ranged between 200 and 500 μm depending on the species and the sample. The oocyte size–frequency data show no evidence of synchrony in oogenesis at population level for any of the species studied. Mirocaris fortunata is the only species where gravid females are commonly collected. The brood is carried on the pleopods, and the number of eggs per female ranges from 25 to 503, with a mean egg length of 0.79±0.14 mm. There is a positive correlation between fecundity and body size, characteristic of crustaceans. One ovigerous C. chacei and two R.exoculata have been studied. The former was carrying 2510 eggs and the later 988 small eggs in an early stage of development. The fecundity of M. fortunata , C. chacei and R. exoculata is significantly higher than that of species from the Acanthephyra group collected in the north-east Atlantic.

Diversity of meiofauna and free-living nematodes in hydrothermal vent mussel beds on the northern and southern East Pacific Rise

The ecology and biogeography of meiofauna at deep-sea hydrothermal vents have historically received less attention than those of mega- and macrofauna. This study examines the composition of major meiofaunal taxa in beds of the mussel Bathymodiolus thermophilus at hydrothermal vents on the northern and southern East Pacific Rise (EPR) and presents the first comparison of species assemblages of the dominant taxon, the nematodes, among sites spanning 27 degrees of latitude. Meiofaunal samples were collected by submersible from three mussel beds at 9°N on the EPR and four mussel beds between 17 and 18°S in 1999. Estimated ages of the mussel beds at the time of sampling range from 4 to >20 years, enabling investigation of the influence of mussel bed age on meiofaunal assemblages. Overall, the meiofauna of the mussel beds was dominated by nematodes, with copepods constituting the second most abundant meiofaunal group. There was variation in the ratio of nematodes to copepods between sites, however, with copepods more abundant than nematodes in the youngest mussel beds. Apart from polychaete larvae, other meiofaunal groups were generally present at very low abundance (<1%) in the samples and restricted in diversity to gastropod larvae, acari, foraminifera, ostracoda and turbellaria. Seventeen nematode species from 14 genera and 11 families were found in the samples, with no evidence of endemicity to hydrothermal vents at the generic level. Four genera present were not previously recorded at hydrothermal vents. Nematode species richness, species:genus ratios and abundances were low compared with other deep-sea habitats, though the ecological relevance of comparisons with soft-sediment benthos is discussed. Nematode assemblages exhibited high dominance by a few species, with one species of Thalassomonhystera most abundant at five of the seven vent sites. Multivariate analysis of nematode assemblages reveals similarities among sites that do not match geographical proximity. The youngest mussel beds were most similar to each other and exhibited lower species richness than other sites, consistent with colonization of mussel bed habitat by nematodes over time. Similarity in the composition of nematode assemblages among sites separated by ∼3000 km indicates that they lie within a single biogeographic province, consistent with that proposed for mussel bed macrofauna. At a generic level, samples exhibited some overlap with nematode assemblages at vents elsewhere on the EPR, on the Mid Atlantic Ridge and in the North Fiji Basin.

Geochemical and Visual Indicators of Hydrothermal Fluid Flow through a Sediment-Hosted Volcanic Ridge in the Central Bransfield Basin (Antarctica)

In the austral summer of 2011 we undertook an investigation of three volcanic highs in the Central Bransfield Basin, Antarctica, in search of hydrothermal activity and associated fauna to assess changes since previous surveys and to evaluate the extent of hydrothermalism in this basin. At Hook Ridge, a submarine volcanic edifice at the eastern end of the basin, anomalies in water column redox potential (Eh) were detected close to the seafloor, unaccompanied by temperature or turbidity anomalies, indicating low-temperature hydrothermal discharge. Seepage was manifested as shimmering water emanating from the sediment and from mineralised structures on the seafloor; recognisable vent endemic fauna were not observed. Pore fluids extracted from Hook Ridge sediment were depleted in chloride, sulfate and magnesium by up to 8% relative to seawater, enriched in lithium, boron and calcium, and had a distinct strontium isotope composition (87Sr/86Sr  = 0.708776 at core base) compared with modern seawater (87Sr/86Sr ≈0.70918), indicating advection of hydrothermal fluid through sediment at this site. Biogeochemical zonation of redox active species implies significant moderation of the hydrothermal fluid with in situ diagenetic processes. At Middle Sister, the central ridge of the Three Sisters complex located about 100 km southwest of Hook Ridge, small water column Eh anomalies were detected but visual observations of the seafloor and pore fluid profiles provided no evidence of active hydrothermal circulation. At The Axe, located about 50 km southwest of Three Sisters, no water column anomalies in Eh, temperature or turbidity were detected. These observations demonstrate that the temperature anomalies observed in previous surveys are episodic features, and suggest that hydrothermal circulation in the Bransfield Strait is ephemeral in nature and therefore may not support vent biota.

A new species of Lebbeus (Crustacea: Decapoda: Caridea: Hippolytidae) from the Von Damm Vent Field, Caribbean Sea

A new species of the hippolytid shrimp genus Lebbeus White, 1847 is described from the Von Damm Vent Field (VDVF) on the Mid-Cayman Spreading Centre, Caribbean Sea, at 2294 m water depth. Lebbeus virentova sp. nov. is defined and illustrated from seven specimens, with brief notes on its distribution and habitat. Molecular phylogenetic data from the COI mDNA region are used to analyse the species’ phylogenetic position, and its morphology is compared with previously described species. This new species represents the second family of caridean shrimp to be reported from the VDVF. Lebbeus virentova sp. nov. is the eighth member of the genus to be described from hydrothermal vents and appears to be the first hippolytid shrimp at a vent field known from outside the Pacific Ocean.

Connectivity in the cold: the comparative population genetics of vent-endemic fauna in the Scotia Sea, Southern Ocean

We report the first comparative population genetics study for vent fauna in the Southern Ocean using cytochrome C oxidase I and microsatellite markers. Three species are examined: the kiwaid squat lobster, Kiwa tyleri, the peltospirid gastropod, Gigantopelta chessoia, and a lepetodrilid limpet, Lepetodrilus sp., collected from vent fields 440 km apart on the East Scotia Ridge (ESR) and from the Kemp Caldera on the South Sandwich Island Arc, ~95 km eastwards. We report no differentiation for all species across the ESR, consistent with panmixia or recent range expansions. A lack of differentiation is notable for Kiwa tyleri, which exhibits extremely abbreviated lecithotrophic larval development, suggestive of a very limited dispersal range. Larval lifespans may, however, be extended by low temperature‐induced metabolic rate reduction in the Southern Ocean, muting the impact of dispersal strategy on patterns of population structure. COI diversity patterns suggest all species experienced demographic bottlenecks or selective sweeps in the past million years and possibly at different times. ESR and Kemp limpets are divergent, although with evidence of very recent ESR‐Kemp immigration. Their divergence, possibility indicative of incipient speciation, along with the absence of the other two species at Kemp, may be the consequence of differing dispersal capabilities across a ~1000 m depth range and/or different selective regimes between the two areas. Estimates of historic and recent limpet gene flow between the ESR and Kemp are consistent with predominantly easterly currents and potentially therefore, cross‐axis currents on the ESR, with biogeographic implications for the region.