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2017
Hansman, RL, Thurber AR, Levin LA, Aluwihare LI.  2017.  Methane fates in the benthos and water column at cold seep sites along the continental margin of Central and North America. Deep-Sea Research Part I-Oceanographic Research Papers. 120:122-131.   10.1016/j.dsr.2016.12.016   AbstractWebsite

The potential influence of methane seeps on carbon cycling is a key question for global assessments, but the study of carbon cycling in surface sediments and the water column of cold seep environments is complicated by the high temporal and spatial variability of fluid and gas fluxes at these sites. In this study we directly examined carbon sources supporting benthic and planktonic food webs at venting methane seeps using isotopic and molecular approaches that integrate this variability. At four seep environments located along North and Central America, microorganisms from two size fractions were collected over several days from 2800 to 90501 of seawater to provide a time-integrated measure of key microbial groups and the carbon sources supporting the overall planktonic microbial community. In addition to water column measurements, the extent of seafloor methane release was estimated at two of the sites by examining the stable carbon isotopic signature (delta C-13) of benthic metazoan infauna. This signature reveals carbon sources fueling the base of the food chain and thus provides a metric that represents a time-integrated view of the dominant microbial processes within the sediment. The stable carbon isotopic composition of microbial DNA (delta C-13-DNA), which had values between -17.0 and -19.5%(0), indicated that bulk planktonic microbial production was not ultimately linked to methane or other C-13-depleted seep-derived carbon sources. Instead these data support the importance of organic carbon derived from either photo- or chemoautotrophic CO2 fixation to the planktonic food web. Results of qPCR of microbial DNA sequences coding for a subunit of the particulate methane monooxygenase gene (pmoA) showed that only a small percentage of the planktonic microbial community were potential methane oxidizers possessing pmoA (< 5% of 16S rRNA gene copies). There was an overall decrease of C-13-depleted carbon fueling the benthic metazoan community from 3 to 5 cm below the seafloor to the sediment surface, reflecting limited use of isotopically depleted carbon at the sediment surface. Rare methane emission as indicated by limited aerobic methane oxidation acts to corroborate our findings for the planktonic microbial community.

2015
Grupe, BM, Krach ML, Pasulka AL, Maloney JM, Levin LA, Frieder CA.  2015.  Methane seep ecosystem functions and services from a recently discovered southern California seep. Marine Ecology-an Evolutionary Perspective. 36:91-108.   10.1111/maec.12243   AbstractWebsite

The recent discovery of a methane seep with diverse microhabitats and abundant groundfish in the San Diego Trough (1020 m) off the coast of Del Mar, California raised questions about the role of seep ecosystem functions and services in relation to continental margins. We used multicorer and ROV grab samples and an ROV survey to characterize macrofaunal structure, diversity, and trophic patterns in soft sediments and authigenic carbonates; seep microhabitats and taxa observed; and the abundance and spatial patterns of fishery-relevant species. Biogenic microhabitats near the Del Mar Seep included microbially precipitated carbonate boulders, bacterial mats, vesicomyid clam beds, frenulate and ampharetid beds, vestimentiferan tubeworm clumps, and fields of Bathysiphon filiformis tubes. Macrofaunal abundance increased and mean faunal delta C-13 signatures decreased in multicorer samples nearer the seep, suggesting that chemosynthetic production enhanced animal densities outside the seep center. Polychaetes dominated sediments, and ampharetids became especially abundant near microbial mats, while gastropods, hydroids, and sponges dominated carbonate rocks. A wide range of stable isotopic signatures reflected the diversity of microhabitats, and methane-derived carbon was the most prevalent source of nutrition for several taxa, especially those associated with carbonates. Megafaunal species living near the seep included longspine thornyhead (Sebastolobus altivelis), Pacific dover sole (Microstomus pacificus), and lithodid crabs (Paralomis verrilli), which represent targets for demersal fisheries. Sebastolobus altivelis was especially abundant (6.5-8.2 fish.100 m(-2)) and appeared to aggregate near the most active seep microhabitats. The Del Mar Methane Seep, like many others along the world's continental margins, exhibits diverse ecosystem functions and enhances regional diversity. Seeps such as this one may also contribute ecosystem services if they provide habitat for fishery species, export production to support margin food webs, and serve as sinks for methane-derived carbon.

2014
Zapata-Hernandez, G, Sellanes J, Thurber AR, Levin LA.  2014.  Trophic structure of the bathyal benthos at an area with evidence of methane seep activity off southern Chile (similar to 45 degrees S). Journal of the Marine Biological Association of the United Kingdom. 94:659-669.   10.1017/s0025315413001914   AbstractWebsite

Through application of carbon (C) and nitrogen (N) stable isotope analyses, we investigated the benthic trophic structure of the upper-slope off southern Chile (similar to 45 degrees S) including a recent methane seep area discovered as part of this study. The observed fauna comprised 53 invertebrates and seven fish taxa, including remains of chemosymbiotic fauna (e.g. chemosymbiotic bivalves and siboglinid polychaetes), which are typical of methane seep environments. While in close-proximity to a seep, the heterotrophic fauna had a nutrition derived predominantly from photosynthetic sources (delta C-13 > -21 parts per thousand). The absence of chemosynthesis-based nutrition in the consumers was likely a result of using an Agassiz trawl to sample the benthos, a method that is likely to collect a mix of fauna including individuals from adjacent non-seep bathyal environments. While four trophic levels were estimated for invertebrates, the fish assemblage was positioned within the third trophic level of the food web. Differences in corrected standard ellipse area (SEA(C)), which is a proxy of the isotopic niche width, yielded differences for the demersal fish Notophycis marginata (SEA(C) = 5.1 parts per thousand) and Coelorinchus fasciatus (SEA(C) = 1.1 parts per thousand), suggesting distinct trophic behaviours. No ontogenic changes were detected in C. fasciatus regarding food sources and trophic position. The present study contributes the first basic trophic data for the bathyal area off southern Chile, including the identification of a new methane seep area, among the furthest south ever discovered. Such information provides the basis for the proper sustainable management of the benthic environments present along the vast Chilean continental margin.

Zapata-Hernandez, G, Sellanes J, Thurber AR, Levin LA, Chazalon F, Linke P.  2014.  New insights on the trophic ecology of bathyal communities from the methane seep area off Concepcion, Chile (similar to 36 degrees S). Marine Ecology-an Evolutionary Perspective. 35:1-21.   10.1111/maec.12051   AbstractWebsite

Studies of the trophic structure in methane-seep habitats provide insight into the ecological function of deep-sea ecosystems. Methane seep biota on the Chilean margin likely represent a novel biogeographic province; however, little is known about the ecology of the seep fauna and particularly their trophic support. The present study, using natural abundance stable isotopes, reveals a complex trophic structure among heterotrophic consumers, with four trophic levels supported by a diversity of food sources at a methane seep area off Concepcion, Chile (similar to 36 degrees S). Although methanotrophy, thiotrophy and phototrophy are all identified as carbon fixation mechanisms fueling the food web within this area, most of the analysed species (87.5%) incorporate carbon derived from photosynthesis and a smaller number (12%) use carbon derived from chemosynthesis. Methane-derived carbon (MDC) incorporation was documented in 22 taxa, including sipunculids, gastropods, polychaetes and echinoderms. In addition, wide trophic niches were detected in suspension-feeding and deposit-feeding taxa, possibly associated with the use of organic matter in different stages of degradation (e.g. from fresh to refractory). Estimates of Bayesian standard ellipses area (SEA(B)) reveal different isotopic niche breadth in the predator fishes, the Patagonian toothfish Dissostichus eleginoides and the combtooth dogfish Centroscyllium nigrum, suggesting generalist versus specialist feeding behaviors, respectively. Top predators in the ecosystem were the Patagonian toothfish D. eleginoides and the dusky cat shark, Bythaelurus canescens. The blue hake Antimora rostrata also provides a trophic link between the benthic and pelagic systems, with a diet based primarily on pelagic-derived carrion. These findings can inform accurate ecosystem models, which are critical for effective management and conservation of methane seep and adjacent deep-sea habitats in the Southeastern Pacific.

2013
Bowden, DA, Rowden AA, Thurber AR, Baco AR, Levin LA, Smith CR.  2013.  Cold seep epifaunal communities on the Hikurangi Margin, New Zealand: Composition, succession, and vulnerability to human activities. Plos One. 8   10.1371/journal.pone.0076869   AbstractWebsite

Cold seep communities with distinctive chemoautotrophic fauna occur where hydrocarbon-rich fluids escape from the seabed. We describe community composition, population densities, spatial extent, and within-region variability of epifaunal communities at methane-rich cold seep sites on the Hikurangi Margin, New Zealand. Using data from towed camera transects, we match observations to information about the probable life-history characteristics of the principal fauna to develop a hypothetical succession sequence for the Hikurangi seep communities, from the onset of fluid flux to senescence. New Zealand seep communities exhibit taxa characteristic of seeps in other regions, including predominance of large siboglinid tubeworms, vesicomyid clams, and bathymodiolin mussels. Some aspects appear to be novel; however, particularly the association of dense populations of ampharetid polychaetes with high-sulphide, high-methane flux, soft-sediment microhabitats. The common occurrence of these ampharetids suggests they play a role in conditioning sulphide-rich sediments at the sediment-water interface, thus facilitating settlement of clam and tubeworm taxa which dominate space during later successional stages. The seep sites are subject to disturbance from bottom trawling at present and potentially from gas hydrate extraction in future. The likely life-history characteristics of the dominant megafauna suggest that while ampharetids, clams, and mussels exploit ephemeral resources through rapid growth and reproduction, lamellibrachid tubeworm populations may persist potentially for centuries. The potential consequences of gas hydrate extraction cannot be fully assessed until extraction methods and target localities are defined but any long-term modification of fluid flow to seep sites would have consequences for all chemoautotrophic fauna.

2012
Levin, LA, Orphan VJ, Rouse GW, Rathburn AE, Ussler W, Cook GS, Goffredi SK, Perez EM, Waren A, Grupe BM, Chadwick G, Strickrott B.  2012.  A hydrothermal seep on the Costa Rica margin: middle ground in a continuum of reducing ecosystems. Proceedings of the Royal Society B-Biological Sciences. 279:2580-2588.   10.1098/rspb.2012.0205   AbstractWebsite

Upon their initial discovery, hydrothermal vents and methane seeps were considered to be related but distinct ecosystems, with different distributions, geomorphology, temperatures, geochemical properties and mostly different species. However, subsequently discovered vents and seep systems have blurred this distinction. Here, we report on a composite, hydrothermal seep ecosystem at a subducting seamount on the convergent Costa Rica margin that represents an intermediate between vent and seep ecosystems. Diffuse flow of shimmering, warm fluids with high methane concentrations supports a mixture of microbes, animal species, assemblages and trophic pathways with vent and seep affinities. Their coexistence reinforces the continuity of reducing environments and exemplifies a setting conducive to interactive evolution of vent and seep biota.

Guilini, K, Levin LA, Vanreusel A.  2012.  Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Pacific Ocean). Progress in Oceanography. 96:77-92.   10.1016/j.pocean.2011.10.003   AbstractWebsite

Hydrate Ridge (HR), located on the northeastern Pacific margin off Oregon, is characterized by the presence of outcropping hydrates and active methane seepage. Additionally, permanent low oxygen conditions overlay the benthic realm. This study evaluated the relative influence of both seepage and oxygen minima as sources of habitat heterogeneity and potential stress-inducing features on the bathyal metazoan benthos (primarily nematodes) at three different seep and non-seep HR locations, exposed to decreasing bottom-water oxygen concentrations with increasing water depth. The nematode seep communities at HR exhibited low diversity with dominance of only one or two genera (Daptonema and Metadesmolaimus), elevated average individual biomass and delta C-13 evidence for strong dependance on chemosynthesis-derived carbon, resembling deep-sea seeps worldwide. Although the HR seep habitats harbored a distinct nematode community like in other known seep communities, they differed from deep-sea seeps in well-oxygenated waters based on that they shared the dominant genera with the surrounding non-seep sediments overlain by oxygen-deficient bottom water. The homogenizing effect of the oxygen minimum zone on the seep nematode assemblages and surrounding sediments was constant with increasing water depth and concomitant greater oxygen-deficiency, resulting in a loss of habitat heterogeneity. (C) 2011 Elsevier Ltd. All rights reserved.

Bernardino, AF, Levin LA, Thurber AR, Smith CR.  2012.  Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. Plos One. 7   10.1371/journal.pone.0033515   AbstractWebsite

Sediments associated with hydrothermal venting, methane seepage and large organic falls such as whale, wood and plant detritus create deep-sea networks of soft-sediment habitats fueled, at least in part, by the oxidation of reduced chemicals. Biological studies at deep-sea vents, seeps and organic falls have looked at macrofaunal taxa, but there has yet to be a systematic comparison of the community-level attributes of sediment macrobenthos in various reducing ecosystems. Here we review key similarities and differences in the sediment-dwelling assemblages of each system with the goals of (1) generating a predictive framework for the exploration and study of newly identified reducing habitats, and (2) identifying taxa and communities that overlap across ecosystems. We show that deep-sea seep, vent and organic-fall sediments are highly heterogeneous. They sustain different geochemical and microbial processes that are reflected in a complex mosaic of habitats inhabited by a mixture of specialist (heterotrophic and symbiont-associated) and background fauna. Community-level comparisons reveal that vent, seep and organic-fall macrofauna are very distinct in terms of composition at the family level, although they share many dominant taxa among these highly sulphidic habitats. Stress gradients are good predictors of macrofaunal diversity at some sites, but habitat heterogeneity and facilitation often modify community structure. The biogeochemical differences across ecosystems and within habitats result in wide differences in organic utilization (i.e., food sources) and in the prevalence of chemosynthesis-derived nutrition. In the Pacific, vents, seeps and organic-falls exhibit distinct macrofaunal assemblages at broad-scales contributing to beta diversity. This has important implications for the conservation of reducing ecosystems, which face growing threats from human activities.

Levin, LA, Sibuet M.  2012.  Understanding Continental Margin Biodiversity: A New Imperative. Annual Review of Marine Science, Vol 4. 4( Carlson CA, Giovannoni SJ, Eds.).:79-+., Palo Alto: Annual Reviews   10.1146/annurev-marine-120709-142714   Abstract

Until recently, the deep continental margins (200-4,000 m) were perceived as monotonous mud slopes of limited ecological or environmental concern. Progress in seafloor mapping and direct observation now reveals unexpected heterogeneity, with a mosaic of habitats and ecosystems linked to geomorphological, geochemical, and hydrographic features that influence biotic diversity. Interactions among water masses, terrestrial inputs, sediment diagenesis, and tectonic activity create a multitude of ecological settings supporting distinct communities that populate canyons and seamounts, high-stress oxygen minimum zones, and methane seeps, as well as vast reefs of cold corals and sponges. This high regional biodiversity is fundamental to the production of valuable fisheries, energy, and mineral resources, and performs critical ecological services (nutrient cycling, carbon sequestration, nursery and habitat support). It is under significant threat from climate change and human resource extraction activities. Serious actions are required to preserve the functions and services provided by the deep-sea settings we are just now getting to know.

2011
Ramirez-Llodra, E, Tyler PA, Baker MC, Bergstad OA, Clark MR, Escobar E, Levin LA, Menot L, Rowden AA, Smith CR, Vandover CL.  2011.  Man and the last great wilderness: human impact on the deep sea. Plos One. 6   10.1371/journal.pone.0022588   AbstractWebsite

The deep sea, the largest ecosystem on Earth and one of the least studied, harbours high biodiversity and provides a wealth of resources. Although humans have used the oceans for millennia, technological developments now allow exploitation of fisheries resources, hydrocarbons and minerals below 2000 m depth. The remoteness of the deep seafloor has promoted the disposal of residues and litter. Ocean acidification and climate change now bring a new dimension of global effects. Thus the challenges facing the deep sea are large and accelerating, providing a new imperative for the science community, industry and national and international organizations to work together to develop successful exploitation management and conservation of the deep-sea ecosystem. This paper provides scientific expert judgement and a semi-quantitative analysis of past, present and future impacts of human-related activities on global deep-sea habitats within three categories: disposal, exploitation and climate change. The analysis is the result of a Census of Marine Life - SYNDEEP workshop (September 2008). A detailed review of known impacts and their effects is provided. The analysis shows how, in recent decades, the most significant anthropogenic activities that affect the deep sea have evolved from mainly disposal (past) to exploitation (present). We predict that from now and into the future, increases in atmospheric CO(2) and facets and consequences of climate change will have the most impact on deep-sea habitats and their fauna. Synergies between different anthropogenic pressures and associated effects are discussed, indicating that most synergies are related to increased atmospheric CO(2) and climate change effects. We identify deep-sea ecosystems we believe are at higher risk from human impacts in the near future: benthic communities on sedimentary upper slopes, cold-water corals, canyon benthic communities and seamount pelagic and benthic communities. We finalise this review with a short discussion on protection and management methods.

2010
Cordes, EE, Cunha MR, Galeron J, Mora C, Olu-Le Roy K, Sibuet M, Van Gaever S, Vanreusel A, Levin LA.  2010.  The influence of geological, geochemical, and biogenic habitat heterogeneity on seep biodiversity. Marine Ecology-an Evolutionary Perspective. 31:51-65.   10.1111/j.1439-0485.2009.00334.x   AbstractWebsite

Cold seeps are among the most heterogeneous of all continental margin habitats. Abiotic Sources of heterogeneity in these systems include local variability in fluid flow, geochemistry, and substrate type, which give rise to different sets of microbial communities, microbial symbiont-bearing foundation species, and associated heterotrophic species. Biogenic habitats created by microbial mats and the symbiotic species including vesicomyid clams, bathymodiolin mussels, and siboglinid tubeworms add an additional layer of complexity to seep habitats. These forms of habitat heterogeneity result in a variety of macrofaunal and meiofaunal communities that respond to changes in structural complexity, habitat geochemistry, nutrient sources, and interspecific interactions in different ways and at different scales. These responses are predicted by a set of theoretical metacommunity models, the most appropriate of which for seep systems appears to be the 'species sorting' concept, an extension of niche theory. This concept is demonstrated through predictable patterns of community assembly, succession, and beta-level diversity. These processes are described using a newly developed analytical technique examining the change in the slope of the species accumulation curve with the number of habitats examined. The diversity response to heterogeneity has a consistent form, but quantitatively changes at different seep sites around the world as the types of habitats present and the size-classes of fauna analyzed change. The increase in beta diversity across seep habitat types demonstrates that cold seeps and associated biogenic habitats are significant sources of heterogeneity on continental margins globally.

Thurber, AR, Kroger K, Neira C, Wiklund H, Levin LA.  2010.  Stable isotope signatures and methane use by New Zealand cold seep benthos. Marine Geology. 272:260-269.   10.1016/j.margeo.2009.06.001   AbstractWebsite

The carbon isotopic composition of seep faunal tissue represents a time-integrated view of the interaction between biology and the biogeochemical gradients within the environment. Here we provide an initial description of carbon and nitrogen stable isotope signatures of dominant symbiont-bearing megafauna and heterotrophic mega- and macrofauna from 10 methane-seep sites on the continental margin of the North Island of New Zealand (662-1201 m water depth). Isotopic signatures suggest that sulfide oxidation supports symbiont-bearing taxa including solemyid and vesicomyid bivalves, and methanotrophic symbionts are present in the seep mussel Bathymodiolus sp Multiple species of Frenulata (Siboglinidae) are present and have a range of isotopic values that are indicative of both thiotroph- and methanotroph-based nutrition. Isotopic composition of the tubeworm Lamellibrachia sp. varied by 23 3 parts per thousand among individuals although there was no consistent difference among sites Variation in methane use by heterotrophic fauna appears to reflect the availability of hard vs. soft substrate, macrofauna on hard substrates had high delta(13)C signatures, reflecting consumption of photosynthetic-derived organic matter Two unique, biotic assemblages were discovered to be fueled largely by methane: a hard-substrate, multi-phyla sponge-associated community (inhabiting the sponge Pseudosuberites sp) and a soft-sediment assemblage dominated by ampharetid polychaetes Isotope signatures yield estimates of 38-100% and 6-100% methane-derived carbon in sponge associates and ampharetid-bed macrofauna. respectively. These estimates are comparable to those made for deeper methane seeps at the Florida Escarpment (3290 m) and Kodiak. Alaska seeps (4445 m) The overall high use of methane as a carbon source by both symbiont-bearing and heterotrophic fauna suggests that New Zealand methane seeps are an ideal model system to study the interaction among metazoans, bacteria, archaea, and their resulting effect on methane cycles. (C) 2009 Elsevier B V All rights reserved

Ramirez-Llodra, E, Brandt A, Danovaro R, De Mol B, Escobar E, German CR, Levin LA, Arbizu PM, Menot L, Buhl-Mortensen P, Narayanaswamy BE, Smith CR, Tittensor DP, Tyler PA, Vanreusel A, Vecchione M.  2010.  Deep, diverse and definitely different: unique attributes of the world's largest ecosystem. Biogeosciences. 7:2851-2899.   10.5194/bg-7-2851-2010   AbstractWebsite

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.

Rabalais, NN, Diaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J.  2010.  Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences. 7:585-619. AbstractWebsite

Water masses can become undersaturated with oxygen when natural processes alone or in combination with anthropogenic processes produce enough organic carbon that is aerobically decomposed faster than the rate of oxygen re-aeration. The dominant natural processes usually involved are photosynthetic carbon production and microbial respiration. The re-supply rate is indirectly related to its isolation from the surface layer. Hypoxic water masses (< 2 mg L(-1), or approximately 30% saturation) can form, therefore, under 'natural' conditions, and are more likely to occur in marine systems when the water residence time is extended, water exchange and ventilation are minimal, stratification occurs, and where carbon production and export to the bottom layer are relatively high. Hypoxia has occurred through geological time and naturally occurs in oxygen minimum zones, deep basins, eastern boundary upwelling systems, and fjords. Hypoxia development and continuation in many areas of the world's coastal ocean is accelerated by human activities, especially where nutrient loading increased in the Anthropocene. This higher loading set in motion a cascading set of events related to eutrophication. The formation of hypoxic areas has been exacerbated by any combination of interactions that increase primary production and accumulation of organic carbon leading to increased respiratory demand for oxygen below a seasonal or permanent pycnocline. Nutrient loading is likely to increase further as population growth and resource intensification rises, especially with increased dependency on crops using fertilizers, burning of fossil fuels, urbanization, and waste water generation. It is likely that the occurrence and persistence of hypoxia will be even more widespread and have more impacts than presently observed. Global climate change will further complicate the causative factors in both natural and human-caused hypoxia. The likelihood of strengthened stratification alone, from increased surface water temperature as the global climate warms, is sufficient to worsen hypoxia where it currently exists and facilitate its formation in additional waters. Increased precipitation that increases freshwater discharge and flux of nutrients will result in increased primary production in the receiving waters up to a point. The interplay of increased nutrients and stratification where they occur will aggravate and accelerate hypoxia. Changes in wind fields may expand oxygen minimum zones onto more continental shelf areas. On the other hand, not all regions will experience increased precipitation, some oceanic water temperatures may decrease as currents shift, and frequency and severity of tropical storms may increase and temporarily disrupt hypoxia more often. The consequences of global warming and climate change are effectively uncontrollable at least in the near term. On the other hand, the consequences of eutrophication-induced hypoxia can be reversed if long-term, broad-scale, and persistent efforts to reduce substantial nutrient loads are developed and implemented. In the face of globally expanding hypoxia, there is a need for water and resource managers to act now to reduce nutrient loads to maintain, at least, the current status.

2009
Rathburn, AE, Levin LA, Tryon M, Gieskes JM, Martin JM, Perez ME, Fodrie FJ, Neira C, Fryer GJ, Mendoza G, McMillan PA, Kluesner J, Adamic J, Ziebis W.  2009.  Geological and biological heterogeneity of the Aleutian margin (1965-4822 m). Progress in Oceanography. 80:22-50.   10.1016/j.pocean.2008.12.002   AbstractWebsite

Geological, biological and biogeochemical characterization of the previously unexplored margin off Unimak Island, Alaska between 1965 and 4822 m water depth was conducted to examine: (1) the geological processes that shaped the margin, (2) the linkages between depth, geomorphology and environmental disturbance in structuring benthic communities of varying size classes and (3) the existence, composition and nutritional sources of methane seep biota on this margin. The study area was mapped and sampled using multibeam sonar, a remotely operated vehicle (ROV) and a towed camera system. Our results provide the first characterization of the Aleutian margin mid and lower slope benthic communities (micro-biota, foraminifera, macrofauna and megafauna), recognizing diverse habitats in a variety of settings. Our investigations also revealed that the geologic feature known as the "Ugamak Slide" is not a slide at all, and could not have resulted from a large 1946 earthquake. However, sediment disturbance appears to be a pervasive feature of this margin. We speculate that the deep-sea occurrence of high densities of Elphidium, typically a shallow-water foraminiferan, results from the influence of sediment redeposition from shallower habitats. Strong representation of cumacean, amphipod and tanaid crustaceans among the Unimak macrofauna may also reflect sediment instability. Although some faunal abundances decline with depth, habitat heterogeneity and disturbance generated by canyons and methane seepage appear to influence abundances of biota in ways that supercede any clear depth gradient in organic matter input. Measures of sediment organic matter and pigment content as well as C and N isotopic signatures were highly heterogeneous, although the availability of organic matter and the abundance of microorganisms in the upper sediment (1-5 cm) were positively correlated. We report the first methane seep on the Aleutian slope in the Unimak region (3263-3285 m), comprised of clam bed, pogonophoran field and carbonate habitats. Seep foraminiferal assemblages were dominated by agglutinated taxa, except for habitats above the seafloor on pogonophoran tubes. Numerous infaunal taxa in clam bed and pogonophoran field sediments and deep-sea "reef' cnidarians (e.g., corals and hydroids) residing on rocks near seepage sites exhibited light organic delta(13)C signatures indicative of chemosynthetic nutritional sources. The extensive geological, biogeochemical and biological heterogeneity as well as disturbance features observed on the Aleutian slope provide an attractive explanation for the exceptionally high biodiversity characteristic of the world's continental margins. (C) 2008 Elsevier Ltd. All rights reserved.

Middelburg, JJ, Levin LA.  2009.  Coastal hypoxia and sediment biogeochemistry. Biogeosciences. 6:1273-1293. AbstractWebsite

The intensity, duration and frequency of coastal hypoxia (oxygen concentration < 63 mu M) are increasing due to human alteration of coastal ecosystems and changes in oceanographic conditions due to global warming. Here we provide a concise review of the consequences of coastal hypoxia for sediment biogeochemistry. Changes in bottom-water oxygen levels have consequences for early diagenetic pathways (more anaerobic at expense of aerobic pathways), the efficiency of re-oxidation of reduced metabolites and the nature, direction and magnitude of sediment-water exchange fluxes. Hypoxia may also lead to more organic matter accumulation and burial and the organic matter eventually buried is also of higher quality, i.e. less degraded. Bottom-water oxygen levels also affect the organisms involved in organic matter processing with the contribution of metazoans decreasing as oxygen levels drop. Hypoxia has a significant effect on benthic animals with the consequences that ecosystem functions related to macrofauna such as bio-irrigation and bioturbation are significantly affected by hypoxia as well. Since many microbes and microbial-mediated biogeochemical processes depend on animal-induced transport processes (e.g. re-oxidation of particulate reduced sulphur and denitrification), there are indirect hypoxia effects on biogeochemistry via the benthos. Severe long-lasting hypoxia and anoxia may result in the accumulation of reduced compounds in sediments and elimination of macrobenthic communities with the consequences that biogeochemical properties during trajectories of decreasing and increasing oxygen may be different (hysteresis) with consequences for coastal ecosystem dynamics.

Levin, LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J.  2009.  Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences. 6:2063-2098.   10.5194/bg-6-2063-2009   AbstractWebsite

Coastal hypoxia (defined here as < 1.42 ml L(-1); 62.5 mu M; 2 mg L(-1), approx. 30% oxygen saturation) develops seasonally in many estuaries, fjords, and along open coasts as a result of natural upwelling or from anthropogenic eutrophication induced by riverine nutrient inputs. Permanent hypoxia occurs naturally in some isolated seas and marine basins as well as in open slope oxygen minimum zones. Responses of benthos to hypoxia depend on the duration, predictability, and intensity of oxygen depletion and on whether H(2)S is formed. Under suboxic conditions, large mats of filamentous sulfide oxidizing bacteria cover the seabed and consume sulfide. They are hypothesized to provide a detoxified microhabitat for eukaryotic benthic communities. Calcareous foraminiferans and nematodes are particularly tolerant of low oxygen concentrations and may attain high densities and dominance, often in association with microbial mats. When oxygen is sufficient to support metazoans, small, soft-bodied invertebrates (typically annelids), often with short generation times and elaborate branchial structures, predominate. Large taxa are more sensitive than small taxa to hypoxia. Crustaceans and echinoderms are typically more sensitive to hypoxia, with lower oxygen thresholds, than annelids, sipunculans, molluscs and cnidarians. Mobile fish and shellfish will migrate away from low-oxygen areas. Within a species, early life stages may be more subject to oxygen stress than older life stages. Hypoxia alters both the structure and function of benthic communities, but effects may differ with regional hypoxia history. Human-caused hypoxia is generally linked to eutrophication, and occurs adjacent to watersheds with large populations or agricultural activities. Many occurrences are seasonal, within estuaries, fjords or enclosed seas of the North Atlantic and the NW Pacific Oceans. Benthic faunal responses, elicited at oxygen levels below 2 ml L(-1), typically involve avoidance or mortality of large species and elevated abundances of enrichment opportunists, sometimes prior to population crashes. Areas of low oxygen persist seasonally or continuously beneath upwelling regions, associated with the upper parts of oxygen minimum zones (SE Pacific, W Africa, N Indian Ocean). These have a distribution largely distinct from eutrophic areas and support a resident fauna that is adapted to survive and reproduce at oxygen concentrations < 0.5 ml L(-1). Under both natural and eutrophication-caused hypoxia there is loss of diversity, through attrition of intolerant species and elevated dominance, as well as reductions in body size. These shifts in species composition and diversity yield altered trophic structure, energy flow pathways, and corresponding ecosystem services such as production, organic matter cycling and organic C burial. Increasingly the influences of nature and humans interact to generate or exacerbate hypoxia. A warmer ocean is more stratified, holds less oxygen, and may experience greater advection of oxygen-poor source waters, making new regions subject to hypoxia. Future understanding of benthic responses to hypoxia must be established in the context of global climate change and other human influences such as overfishing, pollution, disease, habitat loss, and species invasions.

Gooday, AJ, Jorissen F, Levin LA, Middelburg JJ, Naqvi SWA, Rabalais NN, Scranton M, Zhang J.  2009.  Historical records of coastal eutrophication-induced hypoxia. Biogeosciences. 6:1707-1745.   10.5194/bg-6-1707-2009   AbstractWebsite

Under certain conditions, sediment cores from coastal settings subject to hypoxia can yield records of environmental changes over time scales ranging from decades to millennia, sometimes with a resolution of as little as a few years. A variety of biological and geochemical indicators (proxies) derived from such cores have been used to reconstruct the development of eutrophication and hypoxic conditions over time. Those based on (1) the preserved remains of benthic organisms (mainly foraminiferans and ostracods), (2) sedimentary features (e.g. laminations) and (3) sediment chemistry and mineralogy (e.g. presence of sulphides and redox-sensitive trace elements) reflect conditions at or close to the seafloor. Those based on (4) the preserved remains of planktonic organisms (mainly diatoms and dinoflagellates), (5) pigments and lipid biomarkers derived from prokaryotes and eukaryotes and (6) organic C, N and their stable isotope ratios reflect conditions in the water column. However, the interpretation of these indicators is not straightforward. A central difficulty concerns the fact that hypoxia is strongly correlated with, and often induced by, organic enrichment caused by eutrophication, making it difficult to separate the effects of these phenomena in sediment records. The problem is compounded by the enhanced preservation in anoxic and hypoxic sediments of organic microfossils and biomarkers indicating eutrophication. The use of hypoxia-specific proxies, such as the trace metals molybdenum and rhenium and the bacterial biomarker isorenieratene, together with multi-proxy approaches, may provide a way forward. All proxies of bottom-water hypoxia are basically qualitative; their quantification presents a major challenge to which there is currently no satisfactory solution. Finally, it is important to separate the effects of natural ecosystem variability from anthropogenic effects. Despite these problems, in the absence of historical data for dissolved oxygen concentrations, the analysis of sediment cores can provide plausible reconstructions of the temporal development of human-induced hypoxia, and associated eutrophication, in vulnerable coastal environments.

2005
Levin, LA.  2005.  Ecology of cold seep sediments: Interactions of fauna with flow, chemistry and microbes. Oceanography and Marine Biology - an Annual Review, Vol. 43. 43( Gibson RN, Atkinson RJA, Gordon JDM, Eds.).:1-46., Boca Raton: Crc Press-Taylor & Francis Group Abstract

Cold seeps occur in geologically active and passive continental margins, where pore waters enriched in methane are forced upward through the sediments by pressure gradients. The advective supply of methane leads to dense microbial communities with high metabolic rates. Anaerobic methane oxidation presumably coupled to sulphate reduction facilitates formation of carbonates and, in many places, generates extremely high concentrations of hydrogen sulphide in pore waters. Increased food supply, availability of hard substratum and high concentrations of methane and sulphide supplied to free-living and symbiotic bacteria provide the basis for the complex ecosystems found at these sites. This review examines the structures of animal communities in seep sediments and how they are shaped by hydrologic, geochemical and microbial processes. The full size range of biota is addressed but emphasis is on the mid-size sediment-dwelling infauna (foraminiferans, metazoan meiofauna and macrofauna), which have received less attention than megafauna or microbes. Megafaunal biomass at seeps, which far exceeds that of surrounding non-seep sediments, is dominated by bivalves (mytilids, vesicomyids, lucinids and thyasirids) and vestimentiferan tube worms, with pogonophorans, cladorhizid sponges, gastropods and shrimp sometimes abundant. In contrast, seep sediments at shelf and upper slope depths have infaunal densities that often differ very little from those in ambient sediments. At greater depths, seep infauna exhibit enhanced densities, modified composition and reduced diversity relative to background sediments. Dorvilleid, hesionid and ampharetid polychaetes, nematodes, and calcareous foraminiferans are dominant. There is extensive spatial heterogeneity of microbes and higher organisms at seeps. Specialized infaunal communities are associated with different seep habitats (microbial mats, clam beds, mussel beds and tube worms aggregations) and with different vertical zones in the sediment. Whereas fluid flow and associated porewater properties, in particular sulphide concentration, appear to regulate the distribution, physiological adaptations and sometimes behaviour of many seep biota, sometimes the reverse is true. Animal-microbe interactions at seeps are complex and involve symbioses, heterotrophic nutrition, geochemical feedbacks and habitat structure. Nutrition of seep fauna varies, with thiotrophic and methanotrophic symbiotic bacteria fueling most of the megafaunal forms but macrofauna and most meiofauna are mainly heterotrophic. Macrofaunal food sources are largely photosynthesis-based at shallower seeps but reflect carbon fixation by chemosynthesis and considerable incorporation of methane-derived C at deeper seeps. Export of seep carbon appears to be highly localized based on limited studies in the Gulf of Mexico. Seep ecosystems remain one of the ocean's true frontiers. Seep sediments represent some of the most extreme marine conditions and offer unbounded opportunities for discovery in the realms of animal-microbe-geochemical interactions, physiology, trophic ecology, biogeography, systematics and evolution.

2002
Levin, LA, Michener RH.  2002.  Isotopic evidence for chemosynthesis-based nutrition of macrobenthos: The lightness of being at Pacific methane seeps. Limnology and Oceanography. 47:1336-1345. AbstractWebsite

The importance of chemosynthetic nutritional pathways was examined for macrofaunal invertebrates (>300 mum) from methane seeps in the Gulf of Alaska (4,413-4,443 m), on the Oregon margin (590 m), and on the northern California slope [Eel River margin] (520 m) by use of natural abundance stable isotopic data. Seep macrofauna exhibited lighter delta(13)C and delta(15)N values than those in nonseep sediments, but isotopic signatures varied among seep sites. Macrofaunal isotopic signatures indicated chemosynthetically fixed carbon sources with a significant contribution from methane-derived carbon (MDC) in macrofauna from sediments of pogonophoran fields (average delta(13)C, -46.44parts per thousand, 32%-51% MDC) and Calyptogena phaseoliformis beds (average delta(13)C, -40.89parts per thousand, 12%-40% MDC) in the Gulf of Alaska and in microbial mat sediments on the Oregon margin (average delta(13)C, -43.80parts per thousand, 20%-44% MDC). Lesser influence of MDC was noted in macrofauna from sediments of Calyptogena pacifica beds on the Oregon (average delta(13)C, -33.38parts per thousand, 0%-27% MDC) and California (delta(13)C, -25.10parts per thousand, 0%-22% MDC) margins and from California microbial mat sediments (delta(13)C, -22.23%o, 0%-5% MDC). Although most macrofauna appeared to be heterotrophic, light delta(15)N and delta(13)C values together provided evidence for chemoautotrophic symbioses in selected taxa. Carbon isotopic signatures were consistent with consumption of methane-oxidizing archaea by some dorvilleid polychaetes (delta(13)C, -90.62parts per thousand and -73.80parts per thousand) and with grazing on filamentous sulfur bacteria by gastropods and polychaetes from the Oregon and California seeps. The importance of chemosynthetic trophic pathways varies regionally and among microhabitats, taxonomic groups, and feeding guilds.

2000
Rathburn, AE, Levin LA, Held Z, Lohmann KC.  2000.  Benthic foraminifera associated with cold methane seeps on the northern California margin: Ecology and stable isotopic composition. Marine Micropaleontology. 38:247-266.   10.1016/s0377-8398(00)00005-0   AbstractWebsite

Release of methane from large marine reservoirs has been linked to climate change, as a causal mechanism and a consequence of temperature changes, during the Quaternary and the Paleocene. These inferred linkages are based primarily on variations in benthic foraminiferal stable isotope signatures. Few modem analog data exist, however, to assess the influence of methane flux on the geochemistry or faunal characteristics of benthic foraminiferal assemblages. Here we present analyses of the ecology and stable isotopic compositions of living (Rose Bengal stained) and dead (fossil) foraminifera (>150 mu m) from cold methane seeps on the slope off of the Eel River, northern California (500-525 m), and discuss potential applications for reconstructions of methane release in the past and present. Calcareous foraminiferal assemblages associated with Calyptogena clam bed seeps were comprised of species that are also found in organic-rich environments. Cosmopolitan, paleoceanographically important taxa were abundant; these included Uvigerina, Bolivina, Chilostomella, Globobulimina, and Nonionella. We speculate that seep foraminifera are attracted to the availability of food at cold seeps, and require no adaptations beyond those needed for life in organic-rich, reducing environments. Oxygen isotopic values of the tests of living foraminiferal assemblages from seeps had a high range (up to 0.69 parts per thousand) as did carbon isotopic values (up to 1.02 parts per thousand). Many living foraminiferal isotope values were within the range exhibited by the same or similar species in non-seep environments. Carbon isotopic values of fossil foraminifera found deeper in the sediments (18-20 cm), however, were 4.10 parts per thousand (U. peregrina) and 3.60 parts per thousand (B. subargentea) more negative than living delta(13)C values. These results suggest that delta(13)C values of foraminiferal tests reflect methane seepage and species-specific differences in isotopic composition, and can indicate temporal variations in seep activity. A better understanding of foraminiferal ecology and stable isotopic composition will enhance paleo-seep recognition, and improve interpretations of climatic and paleoceanographic change. (C) 2000 Elsevier Science B.V. All rights reserved.

Levin, LA, James DW, Martin CM, Rathburn AE, Harris LH, Michener RH.  2000.  Do methane seeps support distinct macrofaunal assemblages? Observations on community structure and nutrition from the northern California slope and shelf Marine Ecology-Progress Series. 208:21-39.   10.3354/meps208021   AbstractWebsite

Although the conspicuous epifauna of reducing environments are known to exhibit strong morphological, physiological, and nutritional adaptations for life in these habitats, it is less clear whether infaunal organisms do so as well. We examined metazoan macrofauna from methane-seep sediments on the northern California slope (500 to 525 m depth) and from seep and non-seep sediments at 3 locations on the shelf (31 to 53 m depth) to determine whether the community structure and nutritional sources of seep infauna were distinct from those in non-seep, margin sediments. Seep macrofauna consisted mainly of normal slope and shelf species found in productive settings. Several macrofaunal taxa, such as Capitella sp., Diastylopsis dawsoni, and Synidotea angulata, exhibited a preference for seeps. Other taxa, such as the amphipods Rhepoxynius abronius and R, daboius, avoided seeps. Species richness of shelf macrofauna, evaluated by rarefaction and diversity indices (H' and J'), generally did not differ in seep and non-seep sediments. Similarly, stable isotopic composition (delta C-13, delta N-15) Of active seep and non-seep macrofauna did not differ at the 3 shelf sites. Stable isotopic analyses of calcareous material confirmed the presence of methane-influenced pore waters at the slope study site. At one slope clam bed, macrofaunal delta C-13 signatures were lower and delta N-15 values were higher than at another clam bed, inactive slope sediments and shelf sites. However, only 1 of 14 macrofaunal taxa (a dorvilleid polychaete) exhibited isotopic evidence of chemosynthetic nutritional sources. At these sites, seep influence on the ecology of continental margin infauna appears spatially limited and relatively subtle. At their current level of activity, the northern California slope and shelf seeps appear to function as ephemeral, small-scale disturbances that are not sufficiently persistent to allow chemosynthesis-based trophic specialization by most infauna. Rather, we suggest that many of the infauna inhabiting these seep sediments are shelf and slope species preadapted to organic-rich, reducing environments.