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Sweetman, AK, Thurber AR, Smith CR, Levin LA, Mora C, Wei CL, Gooday AJ, Jones DOB, Rex M, Yasuhara M, Ingels J, Ruhl HA, Frieder CA, Danovaro R, Wurzberg L, Baco A, Grupe BM, Pasulka A, Meyer KS, Dunlop KM, Henry LA, Roberts JM.  2017.  Major impacts of climate change on deep-sea benthic ecosystems. Elementa-Science of the Anthropocene. 5:1-23.   10.1525/elementa.203   AbstractWebsite

The deep sea encompasses the largest ecosystems on Earth. Although poorly known, deep seafloor ecosystems provide services that are vitally important to the entire ocean and biosphere. Rising atmospheric greenhouse gases are bringing about significant changes in the environmental properties of the ocean realm in terms of water column oxygenation, temperature, pH and food supply, with concomitant impacts on deep-sea ecosystems. Projections suggest that abyssal (3000-6000 m) ocean temperatures could increase by 1 degrees C over the next 84 years, while abyssal seafloor habitats under areas of deep-water formation may experience reductions in water column oxygen concentrations by as much as 0.03 mL L-1 by 2100. Bathyal depths (200-3000 m) worldwide will undergo the most significant reductions in pH in all oceans by the year 2100 (0.29 to 0.37 pH units). O-2 concentrations will also decline in the bathyal NE Pacific and Southern Oceans, with losses up to 3.7% or more, especially at intermediate depths. Another important environmental parameter, the flux of particulate organic matter to the seafloor, is likely to decline significantly in most oceans, most notably in the abyssal and bathyal Indian Ocean where it is predicted to decrease by 40-55% by the end of the century. Unfortunately, how these major changes will affect deep-seafloor ecosystems is, in some cases, very poorly understood. In this paper, we provide a detailed overview of the impacts of these changing environmental parameters on deep-seafloor ecosystems that will most likely be seen by 2100 in continental margin, abyssal and polar settings. We also consider how these changes may combine with other anthropogenic stressors (e.g., fishing, mineral mining, oil and gas extraction) to further impact deep-seafloor ecosystems and discuss the possible societal implications.

Levin, LA, Le Bris N.  2015.  The deep ocean under climate change. Science. 350:766-768.   10.1126/science.aad0126   AbstractWebsite

The deep ocean absorbs vast amounts of heat and carbon dioxide, providing a critical buffer to climate change but exposing vulnerable ecosystems to combined stresses of warming, ocean acidification, deoxygenation, and altered food inputs. Resulting changes may threaten biodiversity and compromise key ocean services that maintain a healthy planet and human livelihoods. There exist large gaps in understanding of the physical and ecological feedbacks that will occur. Explicit recognition of deep-ocean climate mitigation and inclusion in adaptation planning by the United Nations Framework Convention on Climate Change (UNFCCC) could help to expand deep-ocean research and observation and to protect the integrity and functions of deep-ocean ecosystems.

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.

Thurber, AR, Levin LA, Rowden AA, Sommer S, Linke P, Kroger K.  2013.  Microbes, macrofauna, and methane: A novel seep community fueled by aerobic methanotrophy. Limnology and Oceanography. 58:1640-1656.   10.4319/lo.2013.58.5.1640   AbstractWebsite

During the discovery and description of seven New Zealand methane seep sites, an infaunal assemblage dominated by ampharetid polychaetes was found in association with high seabed methane emission. This ampharetid-bed assemblage had a mean density of 57,000 +/- 7800 macrofaunal individuals m(-2) and a maximum wet biomass of 274 g m(-2), both being among the greatest recorded from deep-sea methane seeps. We investigated these questions: Does the species assemblage present within these ampharetid beds form a distinct seep community on the New Zealand margin? and What type of chemoautotrophic microbes fuel this heterotrophic community? Unlike the other macro-infaunal assemblages, the ampharetid-bed assemblage composition was homogeneous, independent of location. Based on a mixing model of species-specific mass and isotopic composition, combined with published respiration measurements, we estimated that this community consumes 29-90 mmol C m(-2) d(-1) of methane-fueled biomass; this is > 290 times the carbon fixed by anaerobic methane oxidizers in these ampharetid beds. A fatty acid biomarker approach supported the finding that this community, unlike those previously known, consumes primarily aerobic methanotrophic bacteria. Due to the novel microbial fueling and high methane flux rates, New Zealand's ampharetid beds provide a model system to study the influence of metazoan grazing on microbially mediated biogeochemical cycles, including those that involve greenhouse gas emissions.

Levin, LA, Mendoza GF, Gonzalez JP, Thurber AR, Cordes EE.  2010.  Diversity of bathyal macrofauna on the northeastern Pacific margin: the influence of methane seeps and oxygen minimum zones. Marine Ecology-an Evolutionary Perspective. 31:94-110.   10.1111/j.1439-0485.2009.00335.x   AbstractWebsite

The upper continental slope in the northeastern Pacific Ocean is intercepted by a deep oxygen minimum zone (OMZ; 650-1100 m) and punctuated by conduits of methane seepage. We examined the effects of these two dominant sources of heterogeneity on the density, composition and diversity of heterotrophic macrofauna off Hydrate Ridge, Oregon (OR; 800 m water depth), where the seeps co-occur within an OMZ, and off the Eel River, Northern California (CA; 500 m), where seeps are overlain by better oxygenated waters. We hypothesized that seeps (containing clam beds and microbial mats) should contribute a suite of distinct species to the regional margin species pool but that OMZ-associated hypoxia would dampen seep-related heterogeneity. Macrofaunal densities were highest (23,000-33,510 ind.m(-2)) in the CA seep sediments and in the OR near-seep samples, intermediate in the OR seep, CA near seep and CA and OR 500-m margin sediments (10,05419,777 ind.m(-2)), and lowest in the CA and OR OMZ habitats at 800 m (42697847 ind.m(-2)). Annelids constituted over 50% of the taxa in all but the CA clam bed and OR microbial mat sediments, where mollusks were abundant. Approximately 50% of seep species appeared to be habitat endemic; species present in microbial mats largely formed a subset of those present in the clam beds. Dorvilleid and ampharetid polychaetes were dominant in the seep sediments; non-seep margin sediments at 500 and 800 m were populated heavily by branckiate polychaetes including cossurids and paraonids. Alpha diversity (Es[20] calculated per core) was lowest and rank 1 dominance was highest in the CA and OR microbial mat habitats. Pooled analyses of Es[100] revealed highest species richness in the CA clam bed and near-seep habitats (30.3 and 29.6, respectively), and lowest species richness in the OR microbial mat and near-seep habitats (16.5 and 17.9, respectively). Non-seep sediments (500 and 800 m) off both CA and OR were more homogeneous (55-57% within-habitat similarity) than clam bed and microbial mat sediments (only 32-37% within-habitat similarity). CA sediment macrofauna generally exhibit higher alpha diversity, and as habitats are combined, a higher rate of increase in the slope of the species accumulation curves than do OR margin macrofauna. Methane seeps in the NE Pacific introduce significant heterogeneity that increases margin biodiversity at multiple spatial scales. However, our hypothesis that the OMZ would lessen the seep contributions to diversity was not supported. The better oxygenated CA seeps at 500 in shared more of the background margin fauna (at 500 m) than did the OR seeps at 800 m (with OMZ fauna at 800 in). Geographical differences in the fluxes of methane-rich fluids and the increased reliance on chemosynthetic food sources with increased depth could explain these results.

Gooday, AJ, Bett BJ, Escobar E, Ingole B, Levin LA, Neira C, Raman AV, Sellanes J.  2010.  Habitat heterogeneity and its influence on benthic biodiversity in oxygen minimum zones. Marine Ecology-an Evolutionary Perspective. 31:125-147.   10.1111/j.1439-0485.2009.00348.x   AbstractWebsite

Oxygen minimum zones (OMZs; midwater regions with O(2) concentrations <0.5 ml l(-1)) are mid-water features that intercept continental margins at bathyal depths (100-1000 m). They are particularly well developed in the Eastern Pacific Ocean, the Arabian Sea and the Bay of Bengal. Based on analyses of data from these regions, we consider (i) how benthic habitat heterogeneity is manifested within OMZs, (ii) which aspects of this heterogeneity exert the greatest influence on alpha and beta diversity within particular OMZs and (iii) how heterogeneity associated with OMZs influences regional (gamma) diversity on continental margins. Sources of sea-floor habitat heterogeneity within OMZs include bottom-water oxygen and sulphide gradients, substratum characteristics, bacterial mats, and variations in the organic matter content of the sediment and pH. On some margins, hard grounds, formed of phosphorites, carbonates or biotic substrata, represent distinct subhabitats colonized by encrusting faunas. Most of the heterogeneity associated with OMZs, however, is created by strong sea-floor oxygen gradients, reinforced by changes in sediment characteristics and organic matter content. For the Pakistan margin, combining these parameters revealed clear environmental and faunal differences between the OMZ core and the upper and lower boundary regions. In all Pacific and Arabian Sea OMZs examined, oxygen appears to be the master driver of alpha and beta diversity in all benthic faunal groups for which data exist, as well as macrofaunal assemblage composition, particularly in the OMZ core. However, other factors, notably organic matter quantity and quality and sediment characteristics, come into play as oxygen concentrations begin to rise. The influence of OMZs on meiofaunal, macrofaunal and megafaunal regional (gamma) diversity is difficult to assess. Hypoxia is associated with a reduction in species richness in all benthic faunal groups, but there is also evidence for endemism in OMZ settings. We conclude that, on balance, OMZs probably enhance regional diversity, particularly in taxa such as Foraminifera, which are more tolerant of hypoxia than others. Over evolutionary timescales, they may promote speciation by creating strong gradients in selective pressures and barriers to gene flow.

Blankenship, LE, Yayanos AA, Cadien DB, Levin LA.  2006.  Vertical zonation patterns of scavenging amphipods from the Hadal zone of the Tonga and Kermadec Trenches. Deep-Sea Research Part I-Oceanographic Research Papers. 53:48-61.   10.1016/j.dsr.2005.09.006   AbstractWebsite

Deep-sea trenches present an ideal system in which to study vertical zonation, though the difficulties inherent in studying these great depths have thus far deterred such research. Here, we present the first account of the structure and vertical zonation of the scavenging guild residing in the hadal habitat of the Tonga and Kermadec Trenches (SW Pacific Ocean). Four species of scavenging amphipod (Eurythenes gryllus, Scopelocheirus schellenbergi, Hirondellea dubia, and Uristes sp. nov.) were captured with baited free-vehicle traps set 1 m above the seafloor and deployed to bottom depths between 5155 and 10,787 m. Each species occupied a distinct vertical zone of 3.5 km or less, and the scavenging amphipod assemblage vertically partitioned the hadal zone. Scavenging amphipod diversity and evenness sharply declined below 9 km. For S. schellenbergi and H. dubia, population structure was stratified ontogenetically. Early instars appeared to reside exclusively in the shallower depths of each species' vertical zone, and were functionally missing from the median and deeper regions. We captured brooding Uristes sp. nov. females, documenting the first bait-attendance event of brooding amphipods in the hadal zone. Separation of habitat in conjunction with deviations in reproductive traits, behaviors, and nutritional strategies may facilitate the coexistence of these four related species in this harsh and confining habitat. (c) 2005 Elsevier Ltd. All rights reserved.

Davis, JLD, Levin LA, Walther SM.  2002.  Artificial armored shorelines: sites for open-coast species in a southern California bay. Marine Biology. 140:1249-1262.   10.1007/s00227-002-0779-8   AbstractWebsite

Artificial hard substrates have been used to stabilize naturally soft bay shorelines for centuries. Despite the loss of over half of the natural shoreline in many bays, little attention has been paid to the communities inhabiting armored shorelines and to the ecological implications of armoring. The goal of the present study was to examine factors affecting spatial and temporal variation of intertidal, hard-substrate biota (emergent species and fishes), with emphases on the influence of exposure, distance from the open ocean, and similarity to open-coast, hard-substrate communities. We examined community composition at eight San Diego Bay (California, USA) sites (an exposed and a protected site at four bay locations) in June and November 2000 and two open-coast sites in August 2000. At all bay sites, the shore was armored with granite boulders, a form of shoreline stabilization referred to as "riprap." Community structure was more variable spatially than temporally on the scales we studied, affected more by distance from the bay mouth and exposure to wave energy than by differences between June and November. Exposed sites near the bay mouth were more similar to natural open-coast sites, sharing about 45% of their species, than protected sites and sites farther from the mouth, which shared as few as 8%. Species richness was generally higher in exposed than protected bay sites. Species tended to occur higher in the intertidal zone at exposed than protected sites, and higher in November, when sea level was higher, than in June. Such results will be useful to shoreline managers who examine the ecological implications of hardening long stretches of coastline and may suggest ways to incorporate artificial structures into ecosystems in a more meaningful way.

Levin, LA, Talley TS, Hewitt J.  1998.  Macrobenthos of Spartina foliosa (Pacific cordgrass) salt marshes in southern California: Community structure and comparison to a Pacific mudflat and a Spartina alterniflora (Atlantic smooth cordgrass) marsh. Estuaries. 21:129-144.   10.2307/1352552   AbstractWebsite

Environmental attributes (vegetation and sediment properties) of and macrofaunal community structure in sediments of five southern California Spartina foliosa marshes (San Diego Bay, Mission Bay, Upper Newport Bay, Bolsa Chica Lagoon, and Anaheim Bay) were examined during October 1994. Macrofaunal densities in Pacific S. foliosa marshes (avg. 122,268 indiv. m(-2) > 300 mu m) were 3 to 10 times higher than observed in Atlantic S. alterniflora and S. anglica marshes. The macrofauna of S. foliosa marshes was composed mainly of enchytraeid, naidid, and tubificid oligochaetes (66%), with the enchytraeids dominant at all sites except Bolsa Chica Lagoon. Polychaetes, insects, and peracarid crustaceans accounted for most of the remaining fauna. Multivariate analyses indicated greatest faunal similarity between the two southernmost marshes (Mission Bay and San Diego Bay), and between Anaheim and Newport Bay marshes, with Bolsa Chica Lagoon exhibiting a distinct assemblage. There were strong positive associations of faunal abundance and composition with percent organic matter and percent open area, and negative associations with percent sand and dry weight of algae. For the vegetated marsh in Mission Bay, faunal comparisons were made with an adjacent mudflat and with a S. alterniflora marsh in North Carolina, USA. The unvegetated mudflat exhibited similar macrofaunal densities but higher species richness than the adjacent Spartina marsh. The macrofaunal assemblage of the Mission Bay S. foliosa marsh differed from that of the Atlantic S. alterniflora marsh and the Pacific mudflat in having a greater proportion of oligochaetes, especially Enchytraeidae, and fewer polychaetes. This study represents the first published description that we are aware of for macrofauna in S. foliosa vegetated marsh sediments. The findings document faunal variation among southern California embayments and suggest that differences in macrobenthic community structure occur between marsh and mudflat habitat as web as between east and west coast Spartina marshes. Observed differences may have significant implications for wetland conservation and restoration efforts.