Adrian G. Glover

The deep-sea floor ecosystem: current status and prospects of anthropogenic change by the year 2025

The goal of this paper is to review current impacts of human activities on the deep-sea floor ecosystem, and to predict anthropogenic changes to this ecosystem by the year 2025. The deep-sea floor ecosystem is one of the largest on the planet, covering roughly 60% of the Earths solid surface. Despite this vast size, our knowledge of the deep sea is poor relative to other marine ecosystems, and future human threats are difficult to predict. Low productivity, low physical energy, low biological rates, and the vastness of the soft-sediment deep sea create an unusual suite of conservation challenges relative to shallow water. The numerous, but widely spaced, island habitats of the deep ocean (for example seamounts, hydrothermal vents and submarine canyons) differ from typical deep-sea soft sediments in substrate type (hard) and levels of productivity (often high); these habitats will respond differently to anthropogenic impacts and climate change. The principal human threats to the deep sea are the disposal of wastes (structures, radioactive wastes, munitions and carbon dioxide), deep-sea fishing, oil and gas extraction, marine mineral extraction, and climate change. Current international regulations prohibit deep-sea dumping of structures, radioactive waste and munitions. Future disposal activities that could be significant by 2025 include deep-sea carbon-dioxide sequestration, sewage-sludge emplacement and dredge-spoil disposal. As fish stocks dwindle in the upper ocean, deep-sea fisheries are increasingly targeted. Most (perhaps all) of these deep-sea fisheries are not sustainable in the long term given current management practices; deep-sea fish are long-lived, slow growing and very slow to recruit in the face of sustained fishing pressure. Oil and gas exploitation has begun, and will continue, in deep water, creating significant localized impacts resulting mainly from accumulation of contaminated drill cuttings. Marine mineral extraction, in particular manganese nodule mining, represents one of the most significant conservation challenges in the deep sea. The vast spatial scales planned for nodule mining dwarf other potential direct human impacts. Nodule-mining disturbance will likely affect tens to hundreds of thousands of square kilometres with ecosystem recovery requiring many decades to millions of years (for nodule regrowth). Limited knowledge of the taxonomy, species structure, biogeography and basic natural history of deep-sea animals prevents accurate assessment of the risk of species extinctions from large-scale mining. While there are close linkages between benthic, pelagic and climatic processes, it is difficult to predict the impact of climate change on deep-sea benthic ecosystems; it is certain, however, that changes in primary production in surface waters will alter the standing stocks in the food-limited, deep-sea benthic. Long time-series studies from the abyssal North Pacific and North Atlantic suggest that even seemingly stable deep-sea ecosystems may exhibit change in key ecological parameters on decadal time scales. The causes of these decadal changes remain enigmatic. Compared to the rest of the planet, the bulk of the deep sea will probably remain relatively unimpacted by human activities and climate change in the year 2025. However, increased pressure on terrestrial resources will certainly lead to an expansion of direct human activities in the deep sea, and to direct and indirect environmental impacts. Because so little is known about this remote environment, the deep-sea ecosystem may well be substantially modified before its natural state is fully understood.

World-wide whale worms? A new species of Osedax from the shallow north Atlantic

We describe a new species of the remarkable whalebone-eating siboglinid worm genus, Osedax, from a whale carcass in the shallow north Atlantic, west of Sweden. Previously only recorded from deep-sea (1500–3000 m) whale-falls in the northeast Pacific, this is the first species of Osedax known from a shelf-depth whale-fall, and the first from the Atlantic Ocean. The new species, Osedax mucofloris sp. n., is abundant on the bones of an experimentally implanted Minke whale carcass (Balaenoptera acutorostrata) at 125 m depth in the shallow North Sea. O. mucofloris can be cultured on bones maintained in aquaria. The presence of O. mucofloris in the shallow North Sea and northeast Pacific suggests global distribution on whale-falls for the Osedax clade. Molecular evidence from mitochondrial cytochrome oxidase 1 (CO1) and 18S rRNA sequences suggests that O. mucofloris has high dispersal rates, and provides support for the idea of whale-falls acting as ‘stepping-stones’ for the global dispersal of siboglinid annelids over ecological and evolutionary time.

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).

Climate Change and Biosphere Response: Unlocking the Collections Vault

Natural history collections (NHCs) are an important source of the long-term data needed to understand how biota respond to ongoing anthropogenic climate change. These include taxon occurrence data for ecological modeling, as well as information that can be used to reconstruct mechanisms through which biota respond to changing climates. The full potential of NHCs for climate change research cannot be fully realized until high-quality data sets are conveniently accessible for research, but this requires that higher priority be placed on digitizing the holdings most useful for climate change research (e.g., whole-biota studies, time series, records of intensively sampled common taxa). Natural history collections must not neglect the proliferation of new information from efforts to understand how present-day ecosystems are responding to environmental change. These new directions require a strategic realignment for many NHC holders to complement their existing focus on taxonomy and systematics. To set these new priorities, we need strong partnerships between NHC holders and global change biologists.

Patterns in polychaete abundance and diversity from the Madeira Abyssal Plain, northeast Atlantic

Polychaete abundance and diversity patterns from the Madeira Abyssal Plain (MAP) were studied together with data from three other sites on the northeastern Atlantic abyssal plains. Polychaete abundance at MAP was significantly lower than at any of the other sites, including those lying under comparable productivity regimes. Analysis of diversity, using rarefaction and species counts per unit area, suggests that MAP is extremely species poor and shows dominance by a few common species. The MAP site is characterised by a superficial layer of turbidite sediment, and the hypothesis is put forward that the unusual sediment characteristics at MAP have affected macrofaunal abundance over a vast area (>2000 km2). Analysis of species composition indicates that the MAP site is not faunistically unique; rather it contains a high proportion of widespread, abundant, cosmopolitan species. We suggest that these are the opportunists of the abyssal benthic habitat. Differences in abundance between the other abyssal sites are the result of both productivity and local environmental conditions. Equitability at the other north Atlantic sites is not affected by productivity, although the actual number of species per unit area is affected, showing a south–north gradient.

Whale-Fall Ecosystems: Recent Insights into Ecology, Paleoecology, and Evolution

Whale falls produce remarkable organic- and sulfide-rich habitat islands at the seafloor. The past decade has seen a dramatic increase in studies of modern and fossil whale remains, yielding exciting new insights into whale-fall ecosystems. Giant body sizes and especially high bone-lipid content allow great-whale carcasses to support a sequence of heterotrophic and chemosynthetic microbial assemblages in the energy-poor deep sea. Deep-sea metazoan communities at whale falls pass through a series of overlapping successional stages that vary with carcass size, water depth, and environmental conditions. These metazoan communities contain many new species and evolutionary novelties, including bone-eating worms and snails and a diversity of grazers on sulfur bacteria. Molecular and paleoecological studies suggest that whale falls have served as hot spots of adaptive radiation for a specialized fauna; they have also provided evolutionary stepping stones for vent and seep mussels and could have facilitated speciation in other vent/seep taxa.

New perspectives on the ecology and evolution of siboglinid tubeworms

Siboglinids are tube-dweling annelids that are important members of deep-sea chemosynthetic communities, which include hydrothermal vents, cold seeps, whale falls and reduced sediments. As adults, they lack a functional digestive system and rely on microbial endosymbionts for their energetic needs. Recent years have seen a revolution in our understanding of these fascinating worms. Molecular systematic methods now place these animals, formerly known as the phyla Pogonophora and Vestimentifera, within the polychaete clade Siboglinidae. Furthermore, an entirely new radiation of siboglinids, Osedax, has just recently been discovered living on whale bones. The unique and intricate evolutionary association of siboglinids with both geology, in the formation of spreading centres and seeps, and biology with the evolution of large whales, offers opportunities for studies of vicariant evolution and the calibration of molecular clocks. Moreover, new advances in our knowledge of siboglinid anatomy coupled with molecular characterization of microbial symbiont communities are revolutionizing our knowledge of host-symbiont relationships in the Metazoa. Despite these advances, considerable debate persists concerning the evolutionary history of siboglinids. Here we review the morphological, molecular, ecological and fossil data in order to address when and how siboglinids evolved. We discuss the role of ecological conditions in the evolution of siboglinids and present possible scenarios of the evolutionary origin of the symbiotic relationships between siboglinids and their endosymbiotic bacteria.

Insights into the abundance and diversity of abyssal megafauna in a polymetallic-nodule region in the eastern Clarion-Clipperton Zone.

There is growing interest in mining polymetallic nodules in the abyssal Clarion-Clipperton Zone (CCZ) in the Pacific. Nonetheless, benthic communities in this region remain poorly known. The ABYSSLINE Project is conducting benthic biological baseline surveys for the UK Seabed Resources Ltd. exploration contract area (UK-1) in the CCZ. Using a Remotely Operated Vehicle, we surveyed megafauna at four sites within a 900 km2 stratum in the UK-1 contract area, and at a site ~250 km east of the UK-1 area, allowing us to make the first estimates of abundance and diversity. We distinguished 170 morphotypes within the UK-1 contract area but species-richness estimators suggest this could be as high as 229. Megafaunal abundance averaged 1.48 ind. m−2. Seven of 12 collected metazoan species were new to science, and four belonged to new genera. Approximately half of the morphotypes occurred only on polymetallic nodules. There were weak, but statistically significant, positive correlations between megafaunal and nodule abundance. Eastern-CCZ megafaunal diversity is high relative to two abyssal datasets from other regions, however comparisons with CCZ and DISCOL datasets are problematic given the lack of standardised methods and taxonomy. We postulate that CCZ megafaunal diversity is driven in part by habitat heterogeneity.

Aquatic Ecosystems: The near future of the deep-sea floor ecosystems

1 Department of Oceanography, University of Hawaii at Manoa, 1000 Pope Rd., Honolulu HI 96822, USA; email: csmith@soest.hawaii.edu 2 Integrative Oceanography Division, Scripps Institution of Oceanography, La Jolla, CA 92093-0218 USA 3 CSIRO Marine Research, Private Bag 5, Wembley, Perth WA 6913, Australia 4 Southampton Oceanography Centre, University of Southampton, Empress Dock, Southampton SO14 3ZH, UK 5 Zoology Department, The Natural History Museum, Cromwell Rd. London SW7 5BD, UK * Corresponding author

Bone-eating worms from the Antarctic: the contrasting fate of whale and wood remains on the Southern Ocean seafloor.

We report the results from the first experimental study of the fate of whale and wood remains on the Antarctic seafloor. Using a baited free-vehicle lander design, we show that whale-falls in the Antarctic are heavily infested by at least two new species of bone-eating worm, Osedax antarcticus sp. nov. and Osedax deceptionensis sp. nov. In stark contrast, wood remains are remarkably well preserved with the absence of typical wood-eating fauna such as the xylophagainid bivalves. The combined whale-fall and wood-fall experiment provides support to the hypothesis that the Antarctic circumpolar current is a barrier to the larvae of deep-water species that are broadly distributed in other ocean basins. Since humans first started exploring the Antarctic, wood has been deposited on the seafloor in the form of shipwrecks and waste; our data suggest that this anthropogenic wood may be exceptionally well preserved. Alongside the new species descriptions, we conducted a comprehensive phylogenetic analyses of Osedax, suggesting the clade is most closely related to the frenulate tubeworms, not the vestimentiferans as previous reported.