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Ewel, KC, Cressa C, Kneib RT, Lake PS, Levin LA, Palmer MA, Snelgrove P, Wall DH.  2001.  Managing critical transition zones. Ecosystems. 4:452-460.   10.1007/s10021-001-0106-0   AbstractWebsite

Ecosystems that function as critical transition zones (CTZs) among terrestrial, freshwater, and marine habitats are closely connected to the ecosystems adjacent to them and are characterized by a rapid flux of materials and organisms. CTZs play various roles, including mediating water flows, accumulating sediments and organic matter, processing nutrients, and providing opportunities for recreation. They are particularly difficult to manage because they tend to be small, albeit important, components of large watersheds, and managers may not have control over the entire landscape. Moreover, they are often the focus of intensive human activity. Consequently, CTZs are critically important zones, and their preservation and protection are likely to require unique collaboration among scientists, managers, and stakeholders. Scientists can learn a great deal from the study of these ecosystems, taking advantage of small size and the importance of fluxes, but a good understanding of adaptive management strategies is needed to establish a dialogue with managers and stakeholders on technical and management issues. An understanding of risk analysis is also important to help set meaningful goals and establish logical strategies that include all of the interested parties. Successful restoration of a CTZ is the best test of the quality of knowledge about its structure and function. Much has already been learned about coastal CTZs through restoration projects, and the large number of such projects involving riparian CTZs in particular suggests that there is considerable opportunity for fruitful collaborations between scientists and managers.

Neira, C, Grosholz ED, Levin LA, Blake R.  2006.  Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecological Applications. 16:1391-1404.   10.1890/1051-0761(2006)016[1391:mgmobf];2   AbstractWebsite

Many coastal habitats are being substantially altered by introduced plants. In San Francisco Bay,, California, USA, a hybrid form of the eastern cordgrass Spartina alterniflora is rapidly invading open mudflats in southern and central sections of the Bay, altering habitat, reducing macrofaunal densities, and shifting species composition. The invasion has resulted in significant losses of surface-feeding amphipods, bivalves, and cirratulid polychaetes, while subsurface feeding groups such as tubificid oligochaetes and capitellid polychaetes have been unaffected. In the present paper, we document the causes and mechanisms underlying the changes observed. Through a series of in situ manipulative experiments we examined the influence of hybrid Spartina canopy on a range of physical, chemical, and biological properties. The hybrid Spartina canopy exerted a strong influence on. the hydrodynamic regime, triggering a series of physical, chemical, and biological changes in the benthic system. Relative to tidal flats, water velocity was reduced in hybrid patches, promoting deposition of fine-grained, organic-rich particles. The resulting changes in the sediment environment included increased porewater sulfide concentrations and anoxia, which led to poor survivorship. of surface feeders such as, bivalves, amphipods, and polychaetes. These are key taxa that support higher trophic levels including migratory shorebirds that feed on tidal flats. Altered flow in the Spartina canopy further contributed to changes in barnacle recruitment and resuspension of adult benthic invertebrates. Increased crab-induced predation pressure associated with Spartina invasion also contributed to changes in benthic invertebrate communities. Our results suggest that multiple physical, chemical, biotic, and trophic impacts of the Spartina invasion have resulted in substantial changes in benthic communities that are likely to have important effects on the entire ecosystem.

Neira, C, Sellanes J, Levin LA, Arntz WE.  2001.  Meiofaunal distributions on the Peru margin: relationship to oxygen and organic matter availability. Deep-Sea Research Part I-Oceanographic Research Papers. 48:2453-2472.   10.1016/s0967-0637(01)00018-8   AbstractWebsite

A quantitative study of metazoan meiofauna was carried out on bathyal sediments (305, 562, 830 and 1210 m) along a transect within and beneath the oxygen minimum zone (OMZ) in the southeastern Pacific off Callao, Peru (12 degreesS). Meiobenthos densities ranged from 1517 (upper slope, middle of OMZ) to 440-548 ind. 10cm(-2) (lower slope stations, beneath the OMZ). Nematodes were the numerically dominant meiofaunal taxon at every station, followed by copepods and nauplii. Increasing bottom-water oxygen concentration and decreasing organic matter availability downslope were correlated with observed changes in meiofaunal abundance. The 300-m site, located in the middle of the OMZ, differed significantly in meiofaunal abundance, dominance, and in vertical distribution pattern from the deeper sites. At 305 m, nematodes amounted to over 99% of total meiofauna; about 70% of nematodes were found in the 2-5 cm. interval. At the deeper sites, about 50% were restricted to the top I cm. The importance of copepods and nauplii increased consistently with depth, reaching similar to 12% of the total meiofauna at the deepest site. The observation of high nematode abundances at oxygen concentrations <0.02mll(-1) supports the hypothesis that densities are enhanced by an indirect positive effect of low oxygen involving (a) reduction of predators and competitors and (b) preservation of organic matter leading to high food availability and quality. Food input and quality, represented here by chloroplastic pigment equivalents (CPE) and sedimentary labile organic compounds (protein, carbohydrates and lipids), were strongly, positively correlated with nematode abundance. By way of contrast, oxygen exhibited a strong negative correlation, overriding food availability, with abundance of other meiofauna such as copepods and nauplii. These taxa were absent at the 300-m site. The high correlation of labile organic matter (C-LOM, sum of carbon contents in lipids, proteins and carbohydrates) with CPE (Pearson's r = 0.99, p <0.01) suggests that most of the sedimentary organic material sampled was of phytodetrital origin. The fraction of sediment organic carbon potentially available to benthic. heterotrophs, measured as C-LOM/Total organic carbon, was on average 17% at all stations. Thus, a residual, refractory fraction, constitutes the major portion of organic matter at the studied bathyal sites. (C) 2001 Elsevier Science Ltd. All rights reserved.

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.

Case, DH, Pasulka AL, Marlow JJ, Grupe BM, Levin LA, Orphan VJ.  2015.  Methane seep carbonates host distinct, diverse, and dynamic microbial assemblages. Mbio. 6   10.1128/mBio.01348-15   AbstractWebsite

Marine methane seeps are globally distributed geologic features in which reduced fluids, including methane, are advected upward from the subsurface. As a result of alkalinity generation during sulfate-coupled methane oxidation, authigenic carbonates form slabs, nodules, and extensive pavements. These carbonates shape the landscape within methane seeps, persist long after methane flux is diminished, and in some cases are incorporated into the geologic record. In this study, microbial assemblages from 134 native and experimental samples across 5,500 km, representing a range of habitat substrates (carbonate nodules and slabs, sediment, bottom water, and wood) and seepage conditions (active and low activity), were analyzed to address two fundamental questions of seep microbial ecology: (i) whether carbonates host distinct microbial assemblages and (ii) how sensitive microbial assemblages are to habitat substrate type and temporal shifts in methane seepage flux. Through massively parallel 16S rRNA gene sequencing and statistical analysis, native carbonates are shown to be reservoirs of distinct and highly diverse seep microbial assemblages. Unique coupled transplantation and colonization experiments on the seafloor demonstrated that carbonate-associated microbial assemblages are resilient to seep quiescence and reactive to seep activation over 13 months. Various rates of response to simulated seep quiescence and activation are observed among similar phylogenies (e.g., Chloroflexi operational taxonomic units) and similar metabolisms (e.g., putative S oxidizers), demonstrating the wide range of microbial sensitivity to changes in seepage flux. These results imply that carbonates do not passively record a time-integrated history of seep microorganisms but rather host distinct, diverse, and dynamic microbial assemblages. IMPORTANCE Since their discovery in 1984, the global distribution and importance of marine methane seeps have become increasingly clear. Much of our understanding of methane seep microorganisms-from metabolisms to community ecology-has stemmed from detailed studies of seep sediments. However, it has become apparent that carbonates represent a volumetrically significant habitat substrate at methane seeps. Through combined in situ characterization and incubation experiments, this study demonstrates that carbonates host microbial assemblages distinct from and more diverse than those of other seep habitats. This emphasizes the importance of seep carbonates as biodiversity locales. Furthermore, we demonstrate that carbonate-associated microbial assemblages are well adapted to withstand fluctuations in methane seepage, and we gain novel insight into particular taxa that are responsive (or recalcitrant) to changes in seep conditions.

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.

Pasulka, AL, Levin LA, Steele JA, Case DH, Landry MR, Orphan VJ.  2016.  Microbial eukaryotic distributions and diversity patterns in a deep-sea methane seep ecosystem. Environmental Microbiology. 18:3022-3043.   10.1111/1462-2920.13185   AbstractWebsite

Although chemosynthetic ecosystems are known to support diverse assemblages of microorganisms, the ecological and environmental factors that structure microbial eukaryotes (heterotrophic protists and fungi) are poorly characterized. In this study, we examined the geographic, geochemical and ecological factors that influence microbial eukaryotic composition and distribution patterns within Hydrate Ridge, a methane seep ecosystem off the coast of Oregon using a combination of high-throughput 18S rRNA tag sequencing, terminal restriction fragment length polymorphism fingerprinting, and cloning and sequencing of full-length 18S rRNA genes. Microbial eukaryotic composition and diversity varied as a function of substrate (carbonate versus sediment), activity (low activity versus active seep sites), sulfide concentration, and region (North versus South Hydrate Ridge). Sulfide concentration was correlated with changes in microbial eukaryotic composition and richness. This work also revealed the influence of oxygen content in the overlying water column and water depth on microbial eukaryotic composition and diversity, and identified distinct patterns from those previously observed for bacteria, archaea and macrofauna in methane seep ecosystems. Characterizing the structure of microbial eukaryotic communities in response to environmental variability is a key step towards understanding if and how microbial eukaryotes influence seep ecosystem structure and function.

Sapir, A, Dillman AR, Connon SA, Grupe BM, Ingels J, Mundo-Ocampo M, Levin LA, Baldwin JG, Orphan VJ, Sternberg PW.  2014.  Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Frontiers in Microbiology. 5   10.3389/fmicb.2014.00043   AbstractWebsite

The deep sea is Earth's largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over 2 years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes' intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. mansprofundi targets the host's body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep-sea biosphere.

Talley, TS, Levin LA.  2001.  Modification of sediments and macrofauna by an invasive marsh plant. Biological Invasions. 3:51-68.   10.1023/A:1011453003168   AbstractWebsite

Invasive grasses have recently altered salt marsh ecosystems throughout the northern hemisphere. On the eastern seaboard of the USA, Phragmites australis has invaded both brackish and salt marsh habitats. Phragmites australis influence on sediments and fauna was investigated along a salinity and invasion-age gradient in marshes of the lower Connecticut River estuary. Typical salinities were about 19-4 ppt in Site I, 9-10 ppt in Site II and 5-7 ppt in Site III. Strongest effects were evident in the least saline settings (II and III) where Phragmites has been present the longest and exists in monoculture. Limited influence was evident in the most saline region (I) where Phragmites and native salt marsh plants co-occur. The vegetation within Phragmites stands in tidal regions of the Connecticut River generally exhibits taller, but less dense shoots, higher above-ground biomass, and lower below-ground biomass than does the un-invaded marsh flora. There were lower sediment organic content, greater litter accumulation and higher sediment chlorophyll a concentrations in Phragmites-invaded than un-invaded marsh habitat. Epifaunal gastropods (Succinea wilsoni and Stagnicola catascopium) were less abundant in habitats where Phragmites had invaded than in un-invaded marsh habitat. Macro-infaunal densities were lower in the Phragmites-invaded than un-invaded habitats at the two least saline sites (II and III). Phragmites stands supported more podurid insects, sabellid polychaetes, and peracarid crustaceans, fewer arachnids, midges, tubificid and enchytraeid oligochaetes, and greater habitat-wide taxon richness as measured by rarefaction, than did the uninvaded stands. The magnitude and significance of the compositional differences varied with season and with site; differences were generally greatest at the oldest, least saline sites (II and III) and during May, when faunal densities were higher than in September. However, experimental design and the 1-year study period precluded clear separation of salinity, age, and seasonal effects. Although structural effects of Phragmites on salt marsh faunas are evident, further investigation is required to determine the consequences of these effects for ecosystem function.

Kayen, RE, Schwab WC, Lee HJ, Torresan ME, Hein JR, Quinterno PJ, Levin LA.  1989.  Morphology of sea-floor landslides on Horizon Guyot: application of steady-state geotechnical analysis. Deep-Sea Research Part a-Oceanographic Research Papers. 36:1817-1839.   10.1016/0198-0149(89)90114-3   AbstractWebsite

Mass movement and erosion have been identified on the pelagic sediment cap of Horizon Guyot, a seamount in the Mid-Pacific Mountains. Trends in the size, shape and preservation of bedforms and sediment textural trends on the pelagic cap indicate that bottom-current-generated sediment transport direction is upslope. Slumping of the sediment cap occurred on and that the net bedload transport direction is upslope. Slumping of the sediment cap occurred on the northwest side of the guyot on a 1.6° to 2.0° slope in the zone of enhanced bottom-current activity. Submersible investigations of these slump blocks show them to be discrete and to have a relief of 6–15 m, with nodular chert beds cropping out along the headwall of individual rotated blocks. An evaluation of the stability of the sediment cap suggests that the combination of the current-induced beveling of the sea floor and infrequent earthquake loading accompanied by cyclic strength reduction is responsible for the initiation of slumps. The sediment in the area of slumping moved short distances in relatively coherent masses, whereas sediment that has moved beyond the summit cap perimeter has fully mobilized into sediment gravity flows and traveled large distances. A steady-state geotechnical analysis of Horizon Guyot sediment indicates the predisposition of deeply buried sediment towards disintegrative flow failure on appropriately steep slopes. Thus, slope failure in this deeper zone would include large amounts of internal deformation. However, gravitational stress in the near-surface sediment of the summit cap (sub-bottom depth< 14 m) is insufficient to maintain downslope movement after initial failure occurs. The predicted morphology of coherent slump blocks displaced and rafted upon a weakened zone at depth corresponds well with seismic-reflection data and submersible observations.

Levin, LA.  1984.  Multiple patterns of development in Streblospio benedicti Webster (Spionidae) from three coasts of North America. Biological Bulletin. 166:494-508.   10.2307/1541157   AbstractWebsite

Streblospio benedicti Webster, a small tube-dwelling polychaete common in Pacific, Gulf of Mexico, and Atlantic estuaries of North America, exhibits both lecithotrophic and planktotrophic modes of larval development. In lecithotrophic forms females produce few (9-50) large ova (100-200 μm diam.). These develop in dorsal pouches into 9-12 setiger larvae, competent to settle at release. Females of planktotrophic forms produce large broods (100-548) of small ova (70-90 μm), brood larvae in dorsal pouches or beneath dorsal branchiae, and release 3-7 setiger larvae which bear long swimming setae and feed in the plankton for 1-5 weeks before settling. Lecithotrophy is reported for S. benedicti populations on all three coasts of N. America, planktotrophy from the Atlantic and Gulf coasts only. Reproductive differences observed in the field are maintained by laboratory cultures reared under constant (20°C) conditions, though individuals from planktotrophic and lecithotrophic populations are interfertile. Developmental variations observed in the field are believed to generate different patterns of dispersal, recruitment, population growth (r), and mortality. Poicilogony, the occurrence of multiple development modes, may account for the considerable success of S. benedicti in N. America.

Zhang, J, Gilbert D, Gooday AJ, Levin L, Naqvi SWA, Middelburg JJ, Scranton M, Ekau W, Pena A, Dewitte B.  2010.  Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences. 7:1443-1467., France: European Geosciences Union AbstractWebsite

Hypoxia has become a world-wide phenomenon in the global coastal ocean and causes a deterioration of the structure and function of ecosystems. Based on the collective contributions of members of SCOR Working Group #128, the present study provides an overview of the major aspects of coastal hypoxia in different biogeochemical provinces, including estuaries, coastal waters, upwelling areas, fjords and semi-enclosed basins, with various external forcings, ecosystem responses, feedbacks and potential impact on the sustainability of the fishery and economics. The obvious external forcings include freshwater runoff and other factors contributing to stratification, organic matter and nutrient loadings, as well as exchange between coastal and open ocean water masses. Their different interactions set up mechanisms that drive the system towards hypoxia. Coastal systems also vary in their relative susceptibility to hypoxia depending on their physical and geographic settings. It is understood that coastal hypoxia has a profound impact on the sustainability of ecosystems, which can be seen, for example, by the change in the food-web structure and system function; other influences include compression and loss of habitat, as well as changes in organism life cycles and reproduction. In most cases, the ecosystem responds to the low dissolved oxygen in non-linear ways with pronounced feedbacks to other compartments of the Earth System, including those that affect human society. Our knowledge and previous experiences illustrate that there is a need to develop new observational tools and models to support integrated research of biogeochemical dynamics and ecosystem behavior that will improve confidence in remediation management strategies for coastal hypoxia.

Levin, LA, Talley TS.  2002.  Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecological Applications. 12:1785-1802.   10.2307/3099938   AbstractWebsite

Ecosystem recovery following wetland restoration offers exceptional opportunities to study system structure, function, and successional processes in salt marshes. This study used observations of natural variation and large-scale manipulative experiments to test the influence of vascular vegetation and soil organic matter on the rate and trajectory of macrofaunal recovery in a southern California created salt marsh, the Crown Point Mitigation Site. During the first three years following marsh establishment, macrofaunal density and species richness recovered rapidly within the Spartina foliosa (cordgrass) zone; densities in the created marsh were 50% of those in the natural marsh after 16 mo and 97% after 28 mo. However, the early successional assemblage had a lower proportion of tubificid and enchytraeid oligochaetes, and a higher proportion of chironomids and other insect larvae than did the mature natural marsh. Most of the colonizers arrived by rafting on sea grass and algae rather than by larval dispersal. Initial planting of S. foliosa had no influence on macrofaunal recovery, perhaps because of variable transplant survival. However, subsequently, both positive and negative correlations were observed between densities of some macrofaunal taxa and shoot densities of S. foliosa or Salicornia spp. (pickleweed). Salinity and measures of soil organics (belowground biomass, combustible organic matter, and chlorophyll a) also were correlated with macrofaunal densities and taxon richness. Of foul added soil amendments (kelp, alfalfa, peat, and Milorganite), Milorganite (a sewage product) and kelp both promoted macrofaunal colonization during year 1, but effects were short lived. The most significant sources of heterogeneity in the recovering marsh were associated with site history and climate variation. Faunal recovery was most rapid in highly localized, organic-rich marsh sediments that were remnants of the historical wetland. Elevated sea level during the 1998 El Nino corresponded with similarity of macrofaunal communities in the created and natural marshes. The large spatial scale and multi-year duration of this study revealed that natural sources of spatial and temporal heterogeneity may exert stronger influence on faunal succession in California wetlands than manipulation of vegetation or soil properties.

Cook, AA, Lambshead PJD, Hawkins LE, Mitchell N, Levin LA.  2000.  Nematode abundance at the oxygen minimum zone in the Arabian Sea. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 47:75-85.   10.1016/s0967-0645(99)00097-1   AbstractWebsite

This paper supports the hypothesis that low oxygen does not influence deep-sea nematode abundance by investigating an oxygen minimum zone (OMZ) on the Oman slope in the Arabian Sea. Correlation with a number of environmental variables indicated that food quality (measured as the hydrogen index) rather than oxygen was the major predictor of nematode abundance. Nematode abundance was also positively correlated with abundance of total macrofauna, annelids, spionid polychaetes and macrofaunal tube builders. Comparison with published data showed Arabian Sea nematode abundance to be similar to that of the Porcupine Seabight and Bay of Biscay regions of the northeast Atlantic, which also receive significant quantities of phytodetritus but have no OMZ. (C) 1999 Elsevier Science Ltd. All rights reserved.

Neira, C, King I, Mendoza G, Sellanes J, De Ley P, Levin LA.  2013.  Nematode community structure along a central Chile margin transect influenced by the oxygen minimum zone. Deep Sea Research Part I: Oceanographic Research Papers. 78:1-15.   AbstractWebsite

Nematodes are among the metazoans most tolerant of low-oxygen conditions and play major roles in seafloor ecosystem processes. Nematode communities were studied in sediments off Concepción, Central Chile, spanning the outer shelf within the OMZ (122 m) to the mid-lower continental slope (972 m) beneath the OMZ. The total density and biomass of nematodes (core depth 0–10 cm) ranged from 677 to 2006 ind. 10 cm−2, and 168.4 to 506.5 µg DW 10 cm−2, respectively. Among metazoan meiofaunal taxa, nematodes predominated at all sites both in terms of relative abundance (83.7–99.4%) and biomass (53.8–88.1%), followed by copepods, nauplii and polychaetes. Nematodes were represented by 33 genera distributed among 17 families, with densities greatest at low oxygen sites (122–364 m; ~2000 ind. 10 cm−2). Nematode generic and trophic diversity, and individual biomass were lowest, and Rank 1 dominance was highest, at the most oxygen-depleted site (122 m), despite the fact that the organic carbon content of the sediment was maximal at this depth. At the most oxygenated slope sites (827 and 972 m), all of Wieser's nematode feeding groups were represented. In contrast, at the lowest-oxygen site, only selective deposit (bacterial) feeders (1A) were present, indicating a reduction in trophic complexity. A large percentage of nematodes inhabited subsurface sediment layers (>1 cm). At deeper, more oxygenated sites (827 and 972 m), nematode individual biomass increased downcore, while within the OMZ, nematode biomass was low and remained relatively uniform through the sediment column. The concentration of nematodes in deeper sediment layers, the vertical distribution of the feeding groups, as well as the high nutritional quality of the deeper layers, suggest a differential resource partitioning of the food available, which may reduce interspecific competition.

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.

Oliver, PG, Levin L.  2006.  A new species of the family Thyasiridae (Mollusca : Bivalvia) from the oxygen minimum zone of the Pakistan marcrin. Journal of the Marine Biological Association of the United Kingdom. 86:411-416.   10.1017/s0025315406013270   AbstractWebsite

A new species of Thyasiridae, 'Leptaxinus' indusarluni sp. nov. is described from the Indus margin, off Pakistan. The generic affinity is tentative and possible alternatives arc discussed. It occurs between 800 m and 1000 m water depth in a low oxygen environment, where it is relatively abundant. The ecological setting is described and data suggest that this species is not chemosymbiotic.

Dobretsov, S, Xiong HR, Xu Y, Levin LA, Qian PY.  2007.  Novel antifoulants: Inhibition of larval attachment by proteases. Marine Biotechnology. 9:388-397.   10.1007/s10126-007-7091-z   AbstractWebsite

We investigated the effect of commercially available enzymes (alpha-amylase, alpha-galactosidase, papain, trypsin, and lipase) as well as proteases from deep-sea bacteria on the larval attachment of the bryozoan Bugula neritina L. The 50% effective concentrations (EC50) of the commercial proteases were 10 times lower than those of other enzymes. Crude proteases from six deep-sea Psendoalteromonas species significantly decreased larval attachment at concentrations of 0.03 to 1 mIU ml(-1). The EC50 of the pure protease from the bacterium Pseudoalteromonas issachenkonii UST041101-043 was close to 1 ng ml(-1) (0.1 mrU ml(-1)). The protease and trypsin individually incorporated in a water-soluble paint matrix inhibited biofouling in a field experiment. There are certain correlations between production of proteases by bacterial films and inhibition of larval attachment. None of the bacteria with biofilms that induced attachment of B. neritina produced proteolytic enzymes, whereas most of the bacteria that formed inhibitive biofilms produced proteases. Our investigation demonstrated the potential use of proteolytic enzymes for antifouling defense.

Neira, C, Cossaboon J, Mendoza G, Hoh E, Levin LA.  2017.  Occurrence and distribution of polycyclic aromatic hydrocarbons in surface sediments of San Diego Bay marinas. Marine Pollution Bulletin. 114:466-479.   10.1016/j.marpolbul.2016.10.009   Abstract

Polycyclic aromatic hydrocarbons (PAHs) have garnered much attention due to their bioaccumulation, carcinogenic properties, and persistence in the environment. Investigation of the spatial distribution, composition, and sources of PAHs in sediments of three recreational marinas in San Diego Bay, California revealed significant differences among marinas, with concentrations in one site exceeding 16,000 ng g− 1. ‘Hotspots’ of PAH concentration suggest an association with stormwater outfalls draining into the basins. High-molecular weight PAHs (4–6 rings) were dominant (> 86%); the average percentage of potentially carcinogenic PAHs was high in all sites (61.4–70%) but ecotoxicological risks varied among marinas. Highly toxic benzo(a)pyrene (BaP) was the main contributor (> 90%) to the total toxic equivalent quantity (TEQ) in marinas. PAHs in San Diego Bay marina sediments appear to be derived largely from pyrogenic sources, potentially from combustion products that reach the basins by aerial deposition and stormwater drainage from nearby streets and parking lots.

Gallo, ND, Victor DG, Levin LA.  2017.  Ocean commitments under the Paris Agreement. Nature Climate Change. 7:833-+.   10.1038/nclimate3422   AbstractWebsite

Under the Paris Agreement nations made pledges known as nationally determined contributions (NDCs), which indicate how national governments are evaluating climate risks and policy opportunities. We find that NDCs reveal important systematic patterns reflecting national interests and capabilities. Because the ocean plays critical roles in climate mitigation and adaptation, we created a quantitative marine focus factor (MFF) to evaluate how governments address marine issues. In contrast to the past, when oceans received minimal attention in climate negotiations, 70% of 161 NDCs we analysed include marine issues. The percentage of the population living in low-lying areas-vulnerable to rising seas-positively influences the MFF, but negotiating group (Annex 1 or small island developing states) is equally important, suggesting political motivations are crucial to NDC development. The analysis reveals gaps between scientific and government attention, including on ocean deoxygenation, which is barely mentioned. Governments display a keen interest in expanding marine research on climate priorities.

Stramma, L, Schmidtko S, Levin LA, Johnson GC.  2010.  Ocean oxygen minima expansions and their biological impacts. Deep-Sea Research Part I-Oceanographic Research Papers. 57:587-595.   10.1016/j.dsr.2010.01.005   AbstractWebsite

Climate models with biogeochemical components predict declines in oceanic dissolved oxygen with global warming. In coastal regimes oxygen deficits represent acute ecosystem perturbations Here, we estimate dissolved oxygen differences across the global tropical and subtropical oceans within the oxygen minimum zone (200-700-dbar depth) between 1960-1974 (an early period with reliable data) and 1990-2008 (a recent period capturing ocean response to planetary warming) In most regions of the tropical Pacific. Atlantic, and Indian Oceans the oxygen content in the 200-700-dbar layer has declined. Furthermore, at 200 dbar, the area with O(2) < 70 mu mol kg(-1) where some large mobile macro-organisms are unable to abide, has increased by 4.5 million km(2) The tropical low oxygen zones have expanded horizontally and vertically Subsurface oxygen has decreased adjacent to most continental shelves However, oxygen has increased in sonic regions in the subtropical gyres at the depths analyzed According to literature discussed below, fishing pressure is strong in the open ocean, which may make it difficult to isolate the impact of declining oxygen on fisheries At shallower depths we predict habitat compression will occur for hypoxia-intolerant taxa, with eventual loss of biodiversity. Should past trends in observed oxygen differences continue into the future, shifts in animal distributions and changes in ecosystem structure could accelerate (C) 2010 Elsevier Ltd. All rights reserved

McCann, LD, Levin LA.  1989.  Oligochaete influence on settlement, growth and reproduction in a surface-deposit-feeding polychaete. Journal of Experimental Marine Biology and Ecology. 131:233-253.   10.1016/0022-0981(89)90115-9   AbstractWebsite

The functional-group hypothesis predicting that a mobile subsurface-deposit feeder would inhibit the recruitment and subsequent development of a more sedentary tubiculous surface-deposit feeder was tested through a series of laboratory and field manipulations of the oligochaete Monopylephorus evertus Brinkhurst and the polychaete Streblospio benedicti Webster. Laboratory and field studies indicated that settlement of S. benedicti was unaffected by the presence of M. evertus. Settlement of syllid, capitellid and other spionid polychaetes, gastropods and Gemma gemma Totten also appeared to be unaffected. In laboratory cultures, M. evertus caused decreased survivorship of S. benedicti from age 11 wk through senescence and decreased growth (addition of setigers) at age 6–11 wk. Growth of newly settled and older worms may be decreased by the presence of M. evertus, however, the experimental design had insufficient power to determine significance when treatment differences were small. Reduced growth of juveniles, leading to smaller size, was predicted to cause decreased reproductive output in S. benedicti although size-specific reproductive capacity of individual worms was unaffected. Results are consistent with functional-group theory predicting mobile burrowing forms to have negative effects on more stationary tubiculous forms. However, significant decreases in growth rate were limited to the juvenile (recruitment) stages of S. benedicti, emphasizing the importance of examining the entire life cycle of the species of interest. This study also highlights the need for future investigations to determine the role of marine oligochaetes in the dynamics of salt-marsh and estuarine communities.

Levin, LA, Whitcraft CR, Mendoza GF, Gonzalez JP, Cowie G.  2009.  Oxygen and organic matter thresholds for benthic faunal activity on the Pakistan margin oxygen minimum zone (700-1100 m). Deep-Sea Research Part Ii-Topical Studies in Oceanography. 56:449-471.   10.1016/j.dsr2.2008.05.032   AbstractWebsite

A transition from fully laminated to highly bioturbated sediments on continental margins is thought to derive from increased animal activity associated with increasing bottom-water oxygen concentration. We examined faunal community responses to oxygen and organic matter gradients across the lower oxygen minimum zone (OMZ) on the bathyal Pakistan margin, where sediments grade from fully laminated sediment at 700m (0.12 mLL(-1) O(2) [5 mu M]) to highly bioturbated sediment at 1100 m (0.23 mLL(-1) O(2) [10 mu M]). High-resolution sampling of the seafloor (every 50 m water depth) was conducted along a single transect during inter- and post-monsoon periods in 2003 to address (a) the existence of oxygen thresholds regulating macrofaunal abundance, composition, diversity and lifestyles, (b) the interactive effects of organic matter quantity and quality, (c) associated community effects on sediment structure, and (d) potential seasonality in these processes. Macrofaunal biomass and bioturbation depth were positively correlated with organic matter availability, which peaked at 850-950 m (3.39-3.53% Org. Q. In contrast, macrofaunal diversity (HI), dominance (RID), and burrow number exhibited threshold responses at oxygen concentrations of 0.12-0.20 mLL(-1) [5-9 mu M]), with few animals and highly laminated sediments present below this concentration and most taxa present in fully bioturbated sediments above it. The highly mobile, burrowing amphinomid polychaete Linopherus sp. exhibited almost complete dominance and high density at 750-850 m (0.12-0.14 mLL(-1) O(2) [5-6 mu M]), but despite its activity, sediment laminae remained faintly visible. Formation of permanent burrows and detritivory were dominant macrofaunal lifestyles within the OMZ, allowing laminae to persist at surprisingly high animal density and biomass. Results reflect a shift from organic matter to oxygen regulation of body size and biogenic structures following the monsoon. This study suggests that for assemblages evolving under permanent severe hypoxia, food availability remains a significant determinant of animal abundance and biogenic structure depth. Oxygen influences patterns of diversity and dominance and interacts with organic matter to generate abrupt faunal transitions on the Pakistan margin. (C) 2008 Elsevier Ltd. All rights reserved.

Woulds, C, Cowie GL, Levin LA, Andersson JH, Middelburg JJ, Vandewiele S, Lamont PA, Larkin KE, Gooday AJ, Schumacher S, Whitcraft C, Jeffreys RM, Schwartz M.  2007.  Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling. Limnology and Oceanography. 52:1698-1709.   10.4319/lo.2007.52.4.1698   AbstractWebsite

C-13 tracer experiments were conducted at sites spanning the steep oxygen, organic matter, and biological community gradients across the Arabian Sea oxygen minimum zone, in order to quantify the role that benthic fauna play in the short-term processing of organic matter (OM) and to determine how this varies among different environments. Metazoan macrofauna and macrofauna-sized foraminiferans took up as much as 56 +/- 13 mg of added C m(-2) (685 mg C m(-2) added) over 2-5 d, and at some sites this uptake was similar in magnitude to bacterial uptake and/or total respiration. Bottom-water dissolved oxygen concentrations exerted a strong control over metazoan macrofaunal OM processing. At oxygen concentrations > 7 mu mol L-1 (0.16 ml L-1), metazoan macrofauna were able to take advantage of abundant OM and to dominate OM uptake, while OM processing at O-2 concentrations of 5.0 mu mol L-1 (0.11 ml L-1) was dominated instead by (macrofaunal) foraminiferans. This led us to propose the hypothesis that oxygen controls the relative dominance of metazoan macrofauna and foraminifera in a threshold manner, with the threshold lying between 5 and 7 mu mol L-1 (0.11 to 0.16 ml L-1). Large metazoan macrofaunal biomass and high natural concentrations of OM were also associated with rapid processing of fresh OM by the benthic community. Where they were present, the polychaete Linopherus sp. and the calcareous foraminiferan Uvigerina ex gr. semiornata, dominated the uptake of OM above and below, respectively, the proposed threshold concentrations of bottom-water oxygen.