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Breitburg, DL, Salisbury J, Bernhard JM, Cai WJ, Dupont S, Doney SC, Kroeker KJ, Levin LA, Long WC, Milke LM, Miller SH, Phelan B, Passow U, Seibel BA, Todgham AE, Tarrant AM.  2015.  And on top of all that... Coping with ocean acidification in the midst of many stressors. Oceanography. 28:48-61.   10.5670/oceanog.2015.31   AbstractWebsite

Oceanic and coastal waters are acidifying due to processes dominated in the open ocean by increasing atmospheric CO2 and dominated in estuaries and some coastal waters by nutrient-fueled respiration. The patterns and severity of acidification, as well as its effects, are modified by the host of stressors related to human activities that also influence these habitats. Temperature, deoxygenation, and changes in food webs are particularly important co-stressors because they are pervasive, and both their causes and effects are often mechanistically linked to acidification. Development of a theoretical underpinning to multiple stressor research that considers physiological, ecological, and evolutionary perspectives is needed because testing all combinations of stressors and stressor intensities experimentally is impossible. Nevertheless, use of a wide variety of research approaches is a logical and promising strategy for improving understanding of acidification and its effects. Future research that focuses on spatial and temporal patterns of stressor interactions and on identifying mechanisms by which multiple stressors affect individuals, populations, and ecosystems is critical. It is also necessary to incorporate consideration of multiple stressors into management, mitigation, and adaptation to acidification and to increase public and policy recognition of the importance of addressing acidification in the context of the suite of other stressors with which it potentially interacts.

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Blair, NE, Levin LA, Demaster DJ, Plaia G, Martin C, Fornes W, Thomas C, Pope R.  2001.  The biogeochemistry of carbon in continental slope sediments. Organism-sediment Interactions. ( Aller JY, Woodin S, Aller RC, Belle W. Baruch Institute for Marine Biology and Coastal Research. , Eds.).:243-262., Columbia: Published for the Belle W. Baruch Insitute for Marine Biology and Coastal Research by the University of South Carolina Press Abstract
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Demaster, DJ, Pope RH, Levin LA, Blair NE.  1994.  Biological mixing intensity and rates of organic carbon accumulation in North Carolina slope sediments. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 41:735-753.   10.1016/0967-0645(94)90045-0   AbstractWebsite

Sediment accumulation rates and biological mixing intensities were determined at three sites on the North Carolina slope based on profiles of naturally occurring C-14, Pb-210 and(234) Th. The three sites all were at a water depth of 850 m with a spacing of 150-180 km between sites. Sediment accumulation rates increase from south to north from values of 7 cm ky(-1) at Site I, to 160 cm ky(-1) at Site II, to 1100 cm ky(-1) at Site III. The organic carbon burial rate at these sites also increases in the northward direction from 0.65 (Site I) to 20 (Site II) to less than or equal to 150 g C-org m(-2) year(-1) (Site III). These data indicate that continental margin environments can exhibit highly variable carbon fluxes over relatively small distances on the seafloor. The rate of organic carbon accumulation at Site III is one of the highest values reported for the marine environment. Based on these accumulation rates and dissolved inorganic carbon flux estimates from each site, the seabed organic carbon preservation efficiency (i.e. the ratio of C-org accumulation rate to C-org deposition rate times 100) was estimated to vary from 6.0% to 54% to 88% at Sites I, II and III, respectively. The C-14 age of organic matter in surface sediments was older at Site III (1800 years BP) than at Sites I and II (800 years BP), indicating that Site III receives a greater proportion of old sediment from either up-slope areas or from terrigenous sources. Inventories of excess Th-234 (half-life of 24 days) were used as a tracer for particle flux covering the 100 days prior to the October 1989, July-August 1990 and August 1991 cruises. The mean Th-234 inventories al the three sites were 4.7 +/- 1.9, 8.4 +/- 6.3 and 23.1 +/- 7.3 dpm cm(-2) for Sites I, II and III, respectively. Profiles of excess Th-234 activity reveal that the biological mixing intensity is greater at Site III (mean D-b = 19 +/- 11 cm(2) year(-1), n = 5) than at either Site I (mean D-b = 6.0 +/- 6.2 cm(2) year(-1) n = 6) or Site II (mean D-b = 4.6 +/- 5.2 cm(2) year(-1), n = 9). In addition to the trend in mixing coefficients, the depth of particle mixing on a 100-day time scale generally is greater at Site III than at the other two sites. These observations of particle mixing intensity are consistent with the northward increase in the mean abundance of macrofauna (>300 microns) from mean values of 9400 m(-2) at Site I, to 21,400 m(-2) at Site II, to 55,500 m(-2) at Site III. For the three study sites off North Carolina, a strong correlation (R(2) = 0.99,p = 0.06) exists between macrofaunal abundance and the organic carbon deposition rate. An equally strong correlation (R(2) = 0.99, P = 0.04) occurs between macrofaunal abundance and the Th-234 inventories (index of 100-day particle flux). Fine-sand size glass tracer beads were dispersed at these three sites by submersible and then the field plots were sampled similar to 1 year later. The vertical distributions of beads at the three sites are consistent with a higher mixing intensity at Site III than at the other two sites, but the estimated mixing coefficients generally are lower than those determined from the profiles of Th-234. The slower mixing of the glass beads may be the result of their low food value and/or their relatively large size (compared to the surrounding fine-grained sediments).

Buhl-Mortensen, L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, Buhl-Mortensen P, Gheerardyn H, King NJ, Raes M.  2010.  Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Marine Ecology-an Evolutionary Perspective. 31:21-50.   10.1111/j.1439-0485.2010.00359.x   AbstractWebsite

Biological structures exert a major influence on species diversity at both local and regional scales on deep continental margins. Some organisms use other species as substrates for attachment, shelter, feeding or parasitism, but there may also be Mutual benefits from the association. Here, we highlight the structural attributes and biotic effects of the habitats that corals, sea pens, sponges and xenophyophores offer other organisms. The environmental setting of the biological structures influences their species composition. The importance of benthic species as substrates seems to increase with depth as the complexity of the surrounding geological substrate and food supply decline. There are marked differences in the degree of mutualistic relationships between habitat-forming taxa. This is especially evident for scleractinian corals, which have high numbers of facultative associates (commensals) and few obligate associates (mutualists), and gorgonians, with their few commensals and many obligate associates. Size, flexibility and architectural complexity of the habitat-forming organism are positively related to species diversity for both sessile and mobile species. This is mainly evident for commensal species sharing a facultative relationship with their host. Habitat complexity is enhanced by the architecture of biological structures, as well as by biological interactions. Colony morphology has a great influence on feeding efficiency for suspension feeders. Suspension feeding, habitat-forming organisms modify the environment to optimize their food uptake. This environmental advantage is also passed on to associated filter-feeding species. These effects are poorly understood but represent key points for understanding ecosystems and biodiversity on continental margins. In this paper we explore the contributions of organisms and the biotic structures they create (rather than physical modifications) to habitat heterogeneity and diversity on the deep continental margins.

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Basak, C, Rathburn AE, Perez ME, Martin JB, Kluesner JW, Levin LA, De Deckker P, Gieskes JM, Abriani M.  2009.  Carbon and oxygen isotope geochemistry of live (stained) benthic foraminifera from the Aleutian Margin and the Southern Australian Margin. Marine Micropaleontology. 70:89-101.   10.1016/j.marmicro.2008.11.002   AbstractWebsite

Comparisons of ambient bottom-water geochemistry and stable isotopic values of the tests of living (stained) calcareous benthic foraminifera from the North Pacific (on the Aleutian Margin, water depth 1988 m) and Murray Canyons group in the Southern Indian Ocean (Australian Margin, water depths 2476 m and 1634 m) provide modem environmental analogs to calibrate paleoenvironmental assessments. Consistent with the hypothesis that microhabitat preferences influence foraminiferal isotopic values, benthic foraminifera from both margins were depleted in (13)C with respect to bottom-water dissolved inorganic carbon (DIC). The carbon isotope values of deep infaunal foraminifera (Chilostomella oolina, Globobulimina pacifica) showed greater differences from estimates of those of DIC than shallow benthic foraminifera (Bulimina mexicana, Bolivinita quadrilatera, Pullenia bulloides). This study provides new isotopic and ecological information for B. quadrilatera. The mean Delta delta(13)C value, defined as foraminiferal delta(13)C values minus estimated ambient delta(13)C values from the Aleutian Margin, is 0.97 parts per thousand higher for G. pacifica than the mean from the Murray Canyon. This difference may result either from genetic or biological differences between the populations or from differences in environmental isotopic influences (such as pore water differences) that were not accounted for in the equilibrium calculations. These analyses provide calibration information for the evaluation of bottom water conditions and circulation patterns of ancient oceans based on fossil foraminiferal geochemistry. (C) 2008 Elsevier B.V. All rights reserved.

Pasulka, AL, Goffredi SK, Tavormina PL, Dawson KS, Levin LA, Rouse GW, Orphan VJ.  2017.  Colonial tube-dwelling ciliates influence methane cycling and microbial diversity within methane seep ecosystems. Frontiers in Marine Science. 3   10.3389/fmars.2016.00276   Abstract

In a variety of marine ecosystems, microbial eukaryotes play important ecological roles; however, our knowledge of their importance in deep-sea methane seep ecosystems is limited. Microbial eukaryotes have the potential to influence microbial community composition and diversity by creating habitat heterogeneity, and may contribute to carbon cycling through grazing or symbiotic associations with microorganisms. In this study, we characterized the distribution, substrate variability and ecology of a particular group of microbial eukaryotes, known as folliculinid ciliates, at methane seeps along the eastern Pacific margin. Folliculinid ciliates were recently recognized as an abundant and ecologically important component of hydrothermal vent ecosystems, but their ecology in methane seeps has not been examined. Folliculinid ciliates inhabited methane seeps from Costa Rica to Oregon, suggesting a broad distribution in the eastern Pacific. Using phylogenetic analyses of the 18S rRNA gene, two different species of folliculinid were identified. Folliculinids occupied a range of physical substrates, including authigenic carbonate rocks, shells of dead vesicomyid clams, polychaete tubes and gastropod shells. Molecular analysis of folliculinid associated microorganisms (16S rRNA and particulate methane monooxygenase) revealed that these ciliates not only influence overall microbial diversity, but also and have a specific relationship with bacteria in the ‘Deep sea-2’ methanotroph clade. Natural δ13C isotope signatures of folliculinids (-35‰) and their 13C-enrichment patterns in shipboard 13CH4 stable isotope-probing experiments indicated these ciliates and their associated microbes are involved in cycling methane-derived carbon. Folliculinids were significantly enriched in 13C after the addition of 13CH4 over short-term (3-8 day) incubations. Together, these results suggest that folliculinid ciliates represent a previously overlooked contributor to the ecology and biogeochemical cycling of deep-sea methane seep ecosystems.

Burkett, AM, Rathburn AE, Perez ME, Levin LA, Martin JB.  2016.  Colonization of over a thousand Cibicidoides wuellerstorfi (foraminifera: Schwager, 1866) on artificial substrates in seep and adjacent off-seep locations in dysoxic, deep-sea environments. Deep-Sea Research Part I-Oceanographic Research Papers. 117:39-50.   10.1016/j.dsr.2016.08.011   AbstractWebsite

After-1 yr on the seafloor at water depths of similar to 700 m on Hydrate Ridge in the Pacific, eight colonization experiments composed primarily of a plastic mesh cube (from here on refered to as SEA(3), for Seafloor Epibenthic Attachment Cubes) were colonized by 1076 Cibicidoides wuellerstorfi on similar to 1841 cm(2) of experimental substrate. This species is typically considered an indicator of well-oxygenated conditions, and recruitment of such large numbers in bottom waters with low dissolved oxygen availability (0.24-0.37 mL/L) indicate that this taxon may not be as limited by oxygen as previously thought. Clues about substrate preferences were evident from the distribution, or lack thereof, of individuals among plastic mesh, coated steel frame, wooden dowels and reflective tape. Abundance, individual size distributions within cage populations and isotopic biogeochemistry of living foraminifera colonizing experimental substrates were compared between active seep and adjacent off seep experiment locations, revealing potential differences between these environments. Few studies have examined foraminiferal colonization of hard substrates in the deep-sea and to our knowledge no previous study has compared foraminiferal colonization of active seep and off-seep substrates from the same region. This study provides initial results of recruitment, colonization, geochemical and morphological aspects of the paleoceanographically significant species, C. wuellerstorfi, from dynamic deep-sea environments. Further experimental deployments of SEA(3)s will provide a means to assess relatively unknown ecologic dynamics of important foraminiferal deep-sea species.

Springer, AE, Stevens LE, Anderson DE, Partnell RA, Kreamer DK, Levin LA, Flora S.  2008.  A comprehensive springs classification system. Integrating geomorphic, hydrogeochemical, and ecological criteria. Aridland springs in North America: ecology and conservation. ( Stevens LE, Meretsky VJ, Eds.).:49-75., Tucson: University of Arizona Press and the Arizona-Sonora Desert Museum Abstract
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Breitburg, D, Levin LA, Oschlies A, Grégoire M, Chavez FP, Conley DJ, Garçon V, Gilbert D, Gutiérrez D, Isensee K, Jacinto GS, Limburg KE, Montes I, Naqvi SWA, Pitcher GC, Rabalais NN, Roman MR, Rose KA, Seibel BA, Telszewski M, Yasuhara M, Zhang J.  2018.  Declining oxygen in the global ocean and coastal waters. Science. 359   10.1126/science.aam7240   Abstract

As plastic waste pollutes the oceans and fish stocks decline, unseen below the surface another problem grows: deoxygenation. Breitburg et al. review the evidence for the downward trajectory of oxygen levels in increasing areas of the open ocean and coastal waters. Rising nutrient loads coupled with climate change—each resulting from human activities—are changing ocean biogeochemistry and increasing oxygen consumption. This results in destabilization of sediments and fundamental shifts in the availability of key nutrients. In the short term, some compensatory effects may result in improvements in local fisheries, such as in cases where stocks are squeezed between the surface and elevated oxygen minimum zones. In the longer term, these conditions are unsustainable and may result in ecosystem collapses, which ultimately will cause societal and economic harm.

Levin, L, Caswell H, Bridges T, Dibacco C, Cabrera D, Plaia G.  1996.  Demographic responses of estuarine polychaetes to pollutants: Life table response experiments. Ecological Applications. 6:1295-1313.   10.2307/2269608   AbstractWebsite

Capitella sp. I and Streblospio benedicti are infaunal, deposit-feeding polychaetes that occur in estuaries and littoral wetlands throughout much of the United States. Life table response experiments (sensu Caswell 1989a) were carried out in the laboratory to compare the demographic responses of these species to three common sources of estuarine contamination or enrichment: sewage (Milorganite), blue-green algae (Spirulina sp,), and hydrocarbons (No. 2 fuel oil). Life table data were used to generate two population projection models (a fully age-classified model and a simple two-stage model) for each species in each treatment and in a salt marsh sediment control. These models were used to quantify the effects of treatments on survival, reproduction, and age at maturity, and hence on population growth rate. For both species, survival was high in all treatments except the blue-green algae treatment, where oxygen depletion (to <1 mL/L) occurred. Treatments had dramatic effects on age at maturity, fertility, and generation time, which differed between species and among contaminants. Population growth rates (lambda) were higher in Capitella sp. I than in S. benedicti for all treatments, primarily due to earlier maturation and a fertility advantage exhibited by Capitella during the first few weeks of reproduction, In Capitella sp. I, explosive increases in lambda were seen in the sewage (lambda = 5.31) and algae (lambda = 2.81) enrichments relative to the control (lambda = 1.86) and the hydrocarbon treatments (lambda = 1.67), Reduced maturation time and increases in age-specific fertility associated with rapid growth and large body size were responsible, Hydrocarbons reduced lambda primarily through delayed maturation and reduced age-specific fertility. population growth rates of S. benedicti in the hydrocarbon treatment (lambda = 1.11) and algae treatment (lambda = 1.09) were reduced relative to the control (lambda = 1.46) and sewage treatments (lambda = 1.41), The hydrocarbon reduction resulted from delayed maturity and reduced fertility, whereas the algal effects were caused by reductions in both juvenile survival and fertility. Our analyses revealed that Capitella sp. I's population growth rate was less sensitive than that of S. benedicti to these three common forms of estuarine contamination, that different sources of organic enrichment (sewage and blue-green algae) introduced at the same C and N levels could have varying demographic effects, and that when two contaminants (hydrocarbons and blue-green algae) caused similar reductions in population growth rate in a species (Streblospio), the underlying mechanisms may have differed. For both species all demographically important effects of contaminants occurred early in life, suggesting a need to focus on juveniles and young adults in held and laboratory testing. The experiments performed here demonstrated the sensitivity of polychaete demographic properties to the condition of estuarine sediments, This sensitivity may be exploited to evaluate organic enrichment and hydrocarbon contamination in field settings.

Demaster, DJ, Thomas CJ, Blair NE, Fornes WL, Plaia G, Levin LA.  2002.  Deposition of bomb (14)C in continental slope sediments of the Mid-Atlantic Bight: assessing organic matter sources and burial rates. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 49:4667-4685.   10.1016/s0967-0645(02)00134-0   AbstractWebsite

As part of the Ocean Margins Program (OMP), organic carbon (14)C measurements have been made on benthic fauna and kasten core sediments from the North Carolina continental slope. These analyses are used to evaluate the nature and burial flux of organic matter in the OMP study area off Cape Hatteras. Despite the fact that surface sediment (14)C contents ranged from -41 to -215 per mil, the benthic fauna (primarily polychactes) all contained significant amounts of bomb-(14)C (body tissue (14)C contents ranging from + 20 to + 82 per mil). Bomb-(14)C clearly is reaching the seabed on the North Carolina slope, and the labile planktonic material carrying this signal is a primary source of nutrition to the benthic ecosystem. The enrichment of (14)C in benthic faunal tissue relative to the (14)C content of bulk surface-sediment organic matter (a difference of similar to 150 per mil) is attributed to a combination of particle selection and selective digestive processes. Organic carbon burial rates from 12 stations on the North Carolina slope varied from 0.02 to 1.7 mol of Cm(-2) yr(-1), with a mean value of 0.7 mol of C m(-2) yr(-1). The accumulation of organic matter on the upper slope accounts for < 1 % of the primary production in the entire continental margin system. The North Carolina margin was deliberately selected because of its potential for offshore transport and high sediment deposition rates, and even in this environment, burial of organic carbon accounts for a very small fraction of the primary production occurring in surface waters. (C) 2002 Elsevier Science Ltd. All rights reserved.

Navarro, MO, Kwan GT, Batalov O, Choi CY, Pierce NT, Levin LA.  2016.  Development of embryonic market squid, Doryteuthis opalescens, under chronic exposure to low environmental pH and O-2. Plos One. 11   10.1371/journal.pone.0167461   AbstractWebsite

The market squid, Doryteuthis opalescens, is an important forage species for the inshore ecosystems of the California Current System. Due to increased upwelling and expansion of the oxygen minimum zone in the California Current Ecosystem, the inshore environment is expected to experience lower pH and [O-2] conditions in the future, potentially impacting the development of seafloor-attached encapsulated embryos. To understand the consequences of this co-occurring environmental pH and [O-2] stress for D. opalescens encapsulated embryos, we performed two laboratory experiments. In Experiment 1, embryo capsules were chronically exposed to a treatment of higher (normal) pH (7.93) and [O-2] (242 mu M) or a treatment of low pH (7.57) and [O-2] (80 mu M), characteristic of upwelling events and/or La Nina conditions. The low pH and low [O-2] treatment extended embryo development duration by 5-7 days; embryos remained at less developed stages more often and had 54.7% smaller statolith area at a given embryo size. Importantly, the embryos that did develop to mature embryonic stages grew to sizes that were similar (non-distinct) to those exposed to the high pH and high [O-2] treatment. In Experiment 2, we exposed encapsulated embryos to a single stressor, low pH (7.56) or low [O-2] (85 mu M), to understand the importance of environmental pH and [O-2] rising and falling together for squid embryogenesis. Embryos in the low pH only treatment had smaller yolk reserves and bigger statoliths compared to those in low [O-2] only treatment. These results suggest that D. opalescens developmental duration and statolith size are impacted by exposure to environmental [O-2] and pH (pCO(2)) and provide insight into embryo resilience to these effects.

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Bridges, TS, Levin LA, Cabrera D, Plaia G.  1994.  Effects of sediment amended with sewage, algae, or hydrocarbons on growth and reproduction in two opportunistic polychaetes. Journal of Experimental Marine Biology and Ecology. 177:99-119.   10.1016/0022-0981(94)90146-5   AbstractWebsite

The effects of organic- (sewage and blue-green algae) and hydrocarbon- (no. 2 fuel oil) amended sediments on growth schedules, age and size at maturity, fecundity, and reproductive output were examined for the opportunistic polychaetes Streblospio benedicti Webster and Capitella sp. 1. The two species responded very differently to the amended sediments. For S. benedicti, asymptotic size was reduced and age at first reproduction occurred later in the algae and hydrocarbon treatments compared to the marsh mud only and sewage treatments. Organic- and hydrocarbon-amended sediments did not affect per brood measures of fecundity or C and N investment in S. benedicti. In contrast, Capitella sp. I exhibited strong, positive responses to the organically amended sediments; this was seen in terms of more rapid growth (2 x), younger age at first reproduction (50%), larger asymptotic size (6 x), and higher per brood fecundity and C and N investment (4 x). Reproductive output, a relative measure of reproductive investment, was not directly affected by treatments in either species. For Capitella sp. I in organically enriched settings, the benefits of larger body size appear to include higher per brood fecundity without increasing the relative cost (in terms of reproductive output) of producing a brood of young. The population explosions of Capitella sp. I in response to organic enrichment are the result of earlier reproduction and increased body size and fecundity. Positive population-level responses of S. benedicti to contaminated sediments may be the result of its ability to tolerate conditions that other members of a community do not.

Levin, LA, Etter RJ, Rex MA, Gooday AJ, Smith CR, Pineda J, Stuart CT, Hessler RR, Pawson D.  2001.  Environmental influences on regional deep-sea species diversity. Annual Review of Ecology and Systematics. 32:51-93.   10.1146/annurev.ecolsys.32.081501.114002   AbstractWebsite

Most of our knowledge of biodiversity and its causes in the deep-sea benthos derives from regional-scale sampling studies of the macrofauna. Improved sampling methods and the expansion of investigations into a wide variety of habitats have revolutionized our understanding of the deep sea. Local species diversity shows clear geographic variation on spatial scales of 100-1000 km. Recent sampling programs have revealed unexpected complexity in community structure at the landscape level that is associated with large-scale oceanographic processes and their environmental consequences. We review the relationships between variation in local species diversity and the regional-scale phenomena of boundary constraints, gradients of productivity, sediment heterogeneity, oxygen availability, hydrodynamic regimes, and catastrophic physical disturbance. We present a conceptual model of how these interdependent environmental factors shape regional-scale variation in local diversity. Local communities in the deep sea may be composed of species that exist as metapopulations whose regional distribution depends on a balance among global-scale, landscape-scale, and small-scale dynamics. Environmental gradients may form geographic patterns of diversity by influencing local processes such as predation, resource partitioning, competitive exclusion, and facilitation that determine species coexistence. The measurement of deep-sea species diversity remains a vital issue in comparing geographic patterns and evaluating their potential causes. Recent assessments of diversity using species accumulation curves with randomly pooled samples confirm the often-disputed claim that the deep sea supports higher diversity than the continental shelf. However, more intensive quantitative sampling is required to fully characterize the diversity of deep-sea sediments, the most extensive habitat on Earth. Once considered to be constant, spatially uniform, and isolated, deep-sea sediments are now recognized as a dynamic, richly textured environment that is inextricably linked to the global biosphere. Regional studies of the last two decades provide the empirical background necessary to formulate and test specific hypotheses of causality by controlled sampling designs and experimental approaches.

Navarro, MO, Parnell PE, Levin LA.  2018.  Essential market squid (Doryteuthis opalescens) embryo habitat: A baseline for anticipated ocean climate change. Journal of Shellfish Research. 37:601-614.   10.2983/035.037.0313   AbstractWebsite

The market squid Doryteuthis opalescens deposits embryo capsules onto the continental shelf from Baja California to southern Alaska, yet little is known about the environment of embryo habitat. This study provides a baseline of environmental data and insights on factors underlying site selection for embryo deposition off southern California, and defines current essential embryo habitat using (1) remotely operated vehicle-supported surveys of benthos and environmental variables, (2) SCUBA surveys, and (3) bottom measurements of T, S, pH, and O-2. Here, embryo habitat is defined using embryo capsule density, capsule bed area, consistent bed footprint, and association with [O-2] and pH (pCO(2)) on the shelf. Spatial variation in embryo capsule density and location appears dependent on environmental conditions, whereas the temporal pattern of year-round spawning is not. Embryos require [O-2] greater than 160 mu mol and pH(T) greater than 7.8. Temperature does not appear to be limiting (range: 9.9 degrees C-15.5 degrees C). Dense embryo beds were observed infrequently, whereas low-density cryptic aggregations were common. Observations of dense embryo aggregation in response to shoaling of low [O-2] and pH indicate habitat compression. Essential embryo habitat likely expands and contracts in space and time directly with regional occurrence of appropriate O-2 and pH exposure. Embryo habitat will likely be at future risk of compression given secular trends of deoxygenation and acidification within the Southern California Bight. Increasingly localized and dense spawning may become more common, resulting in potentially important changes in market squid ecology and management.

Sato, KN, Powell J, Rudie D, Levin LA.  2018.  Evaluating the promise and pitfalls of a potential climate change-tolerant sea urchin fishery in southern California. Ices Journal of Marine Science. 75:1029-1041.   10.1093/icesjms/fsx225   AbstractWebsite

Marine fishery stakeholders are beginning to consider and implement adaptation strategies in the face of growing consumer demand and potential deleterious climate change impacts such as ocean warming, ocean acidification, and deoxygenation. This study investigates the potential for development of a novel climate change-tolerant sea urchin fishery in southern California based on Strongylocentrotus fragilis (pink sea urchin), a deep-sea species whose peak density was found to coincide with a current trap-based spot prawn fishery (Pandalus platyceros) in the 200-300-m depth range. Here we outline potential criteria for a climate change-tolerant fishery by examining the distribution, life-history attributes, and marketable qualities of S. fragilis in southern California. We provide evidence of seasonality of gonad production and demonstrate that peak gonad production occurs in the winter season. S. fragilis likely spawns in the spring season as evidenced by consistent minimum gonad indices in the spring/summer seasons across 4 years of sampling (2012-2016). The resiliency of S. fragilis to predicted future increases in acidity and decreases in oxygen was supported by high species abundance, albeit reduced relative growth rate estimates at water depths (485-510 m) subject to low oxygen (11.7-16.9 mmol kg similar to 1) and pHTotal (< 7.44), which may provide assurances to stakeholders and managers regarding the suitability of this species for commercial exploitation. Some food quality properties of the S. fragilis roe (e. g. colour, texture) were comparable with those of the commercially exploited shallow-water red sea urchin (Mesocentrotus franciscanus), while other qualities (e. g. 80% reduced gonad size by weight) limit the potential future marketability of S. fragilis. This case study highlights the potential future challenges and drawbacks of climate-tolerant fishery development in an attempt to inform future urchin fishery stakeholders.

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Schander, C, Rapp HT, Kongsrud JA, Bakken T, Berge J, Cochrane S, Oug E, Byrkjedal I, Todt C, Cedhagen T, Fosshagen A, Gebruk A, Larsen K, Levin L, Obst M, Pleijel F, Stohr S, Waren A, Mikkelsen NT, Hadler-Jacobsen S, Keuning R, Petersen KH, Thorseth IH, Pedersen RB.  2010.  The fauna of hydrothermal vents on the Mohn Ridge (North Atlantic) *. Marine Biology Research. 6:155-171.: Taylor & Francis Group Ltd., 2 Park Square Oxford OX14 4RN UK   10.1080/17451000903147450   AbstractWebsite

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Askarizadeh, A, Rippy MA, Fletcher TD, Feldman DL, Peng J, Bowler P, Mehring AS, Winfrey BK, Vrugt JA, AghaKouchak A, Jiang SC, Sanders BF, Levin LA, Taylor S, Grant SB.  2015.  From rain tanks to catchments: Use of low-impact development to address hydrologic symptoms of the urban stream syndrome. Environmental Science & Technology. 49:11264-11280.   10.1021/acs.est.5b01635   AbstractWebsite

Catchment urbanization perturbs the water and sediment budgets of streams, degrades stream health and function, and causes a constellation of flow, water quality, and ecological symptoms collectively known as the urban stream syndrome. Low-impact development (LID) technologies address the hydrologic symptoms of the urban stream syndrome by mimicking natural flow paths and restoring a natural water balance. Over annual time scales, the volumes of stormwater that should be infiltrated and harvested can be estimated from a catchment-scale water-balance given local climate conditions and preurban land cover. For all but the wettest regions of the world, a much larger volume of stormwater runoff should be harvested than infiltrated to maintain stream hydrology in a preurban state. Efforts to prevent or reverse hydrologic symptoms associated with the urban stream syndrome will therefore require: (1) selecting the right mix of LID technologies that provide regionally tailored ratios of stormwater harvesting and infiltration; (2) integrating these LID technologies into next-generation drainage systems; (3) maximizing potential cobenefits including water supply augmentation, flood protection, improved water quality, and urban amenities; and (4) long-term hydrologic monitoring to evaluate the efficacy of LID interventions.

Levin, LA, Boesch DF, Covich A, Dahm C, Erseus C, Ewel KC, Kneib RT, Moldenke A, Palmer MA, Snelgrove P, Strayer D, Weslawski JM.  2001.  The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems. 4:430-451.   10.1007/s10021-001-0021-4   AbstractWebsite

Estuaries and coastal wetlands are critical transition zones (CTZs) that link land, freshwater habitats, and the sea. CTZs provide essential ecological functions, including decomposition, nutrient cycling, and nutrient production, as well as regulation of fluxes of nutrients, water, particles, and organisms to and from land, rivers, and the ocean. Sediment-associated biota are integral to these functions. Functional groups considered essential to CTZ processes include heterotrophic bacteria and fungi, as well as many benthic invertebrates. Key invertebrate functions include shredding, which breaks down and recycles organic matter; suspension feeding, which collects and transports sediments across the sediment-water interface; and bioturbating, which moves sediment into or out of the seabed. In addition, macrophytes regulate many aspects of nutrient, particle, and organism dynamics above- and belowground. Animals moving within or through CTZs are vectors that transport nutrients and organic matter across terrestrial, freshwater, and marine interfaces. Significant threats to biodiversity within CTZs are posed by anthropogenic influences; eutrophication, nonnutrient pollutants, species invasions, overfishing, habitat alteration, and climate change affect species richness or composition in many coastal environments. Because biotic diversity in marine CTZ sediments is inherently low whereas their functional significance is great, shifts in diversity are likely to be particularly important. Species introductions (from invasion) or loss (from overfishing or habitat alteration) provide evidence that single-species changes can have overt, sweeping effects on CTZ structure and function. Certain species may be critically important to the maintenance of ecosystem functions in CTZs even though at present there is limited empirical evidence that the number of species in CTZ sediments is critical. We hypothesized that diversity is indeed important to ecosystem function in marine CTZs because high diversity maintains positive interactions among species (facilitation and mutualism), promoting stability and resistance to invasion or other forms of disturbance. The complexity of interactions among species and feedbacks with ecosystem functions suggests that comparative (mensurative) and manipulative approaches will be required to elucidate the role of diversity in sustaining CTZ functions.

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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.

Levin, LA, Bett BJ, Gates AR, Heimbach P, Howe BM, Janssen F, McCurdy A, Ruhl HA, Snelgrove P, Stocks KI, Bailey D, Baumann-Pickering S, Beaverson C, Benfield MC, Booth DJ, Carreiro-Silva M, Colaco A, Eble MC, Fowler AM, Gjerde KM, Jones DOB, Katsumata K, Kelley D, Le Bris N, Leonardi AP, Lejzerowicz F, Macreadie PI, McLean D, Meitz F, Morato T, Netburn A, Pawlowski J, Smith CR, Sun S, Uchida H, Vardaro MF, Venkatesan R, Weller RA.  2019.  Global observing needs in the deep ocean. Frontiers in Marine Science. 6   10.3389/fmars.2019.00241   AbstractWebsite

The deep ocean below 200 m water depth is the least observed, but largest habitat on our planet by volume and area. Over 150 years of exploration has revealed that this dynamic system provides critical climate regulation, houses a wealth of energy, mineral, and biological resources, and represents a vast repository of biological diversity. A long history of deep-ocean exploration and observation led to the initial concept for the Deep-Ocean Observing Strategy (DOOS), under the auspices of the Global Ocean Observing System (GOOS). Here we discuss the scientific need for globally integrated deep-ocean observing, its status, and the key scientific questions and societal mandates driving observing requirements over the next decade. We consider the Essential Ocean Variables (EOVs) needed to address deep-ocean challenges within the physical, biogeochemical, and biological/ecosystem sciences according to the Framework for Ocean Observing (FOO), and map these onto scientific questions. Opportunities for new and expanded synergies among deep-ocean stakeholders are discussed, including academic-industry partnerships with the oil and gas, mining, cable and fishing industries, the ocean exploration and mapping community, and biodiversity conservation initiatives. Future deep-ocean observing will benefit from the greater integration across traditional disciplines and sectors, achieved through demonstration projects and facilitated reuse and repurposing of existing deep-sea data efforts. We highlight examples of existing and emerging deep-sea methods and technologies, noting key challenges associated with data volume, preservation, standardization, and accessibility. Emerging technologies relevant to deep-ocean sustainability and the blue economy include novel genomics approaches, imaging technologies, and ultra-deep hydrographic measurements. Capacity building will be necessary to integrate capabilities into programs and projects at a global scale. Progress can be facilitated by Open Science and Findable, Accessible, Interoperable, Reusable (FAIR) data principles and converge on agreed to data standards, practices, vocabularies, and registries. We envision expansion of the deep-ocean observing community to embrace the participation of academia, industry, NGOs, national governments, international governmental organizations, and the public at large in order to unlock critical knowledge contained in the deep ocean over coming decades, and to realize the mutual benefits of thoughtful deep-ocean observing for all elements of a sustainable ocean.

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Hofmann, GE, Smith JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR.  2011.  High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison. Plos One. 6   10.1371/journal.pone.0028983   AbstractWebsite

The effect of Ocean Acidification (OA) on marine biota is quasi-predictable at best. While perturbation studies, in the form of incubations under elevated pCO(2), reveal sensitivities and responses of individual species, one missing link in the OA story results from a chronic lack of pH data specific to a given species' natural habitat. Here, we present a compilation of continuous, high-resolution time series of upper ocean pH, collected using autonomous sensors, over a variety of ecosystems ranging from polar to tropical, open-ocean to coastal, kelp forest to coral reef. These observations reveal a continuum of month-long pH variability with standard deviations from 0.004 to 0.277 and ranges spanning 0.024 to 1.430 pH units. The nature of the observed variability was also highly site-dependent, with characteristic diel, semi-diurnal, and stochastic patterns of varying amplitudes. These biome-specific pH signatures disclose current levels of exposure to both high and low dissolved CO2, often demonstrating that resident organisms are already experiencing pH regimes that are not predicted until 2100. Our data provide a first step toward crystallizing the biophysical link between environmental history of pH exposure and physiological resilience of marine organisms to fluctuations in seawater CO2. Knowledge of this spatial and temporal variation in seawater chemistry allows us to improve the design of OA experiments: we can test organisms with a priori expectations of their tolerance guardrails, based on their natural range of exposure. Such hypothesis-testing will provide a deeper understanding of the effects of OA. Both intuitively simple to understand and powerfully informative, these and similar comparative time series can help guide management efforts to identify areas of marine habitat that can serve as refugia to acidification as well as areas that are particularly vulnerable to future ocean change.

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.

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Levin, LA, Gage J, Lamont P, Cammidge L, Patience A, Martin C.  1997.  Infaunal community structure in a low-oxygen organic rich habitat on the Oman Continental Slope, NW Arabian Sea. The responses of marine organisms to their environments : Proceedings of the 30th European Marine Biology Symposium, University of Southampton, Southampton, United Kingdom. ( Hawkins LE, Hutchinson S, Jensen AC, Sheader M, Williams JA, Eds.).:223-230., Southampton: Southampton Oceanography Centre, University of Southampton Abstract
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Levin, LA, Plaia G, Huggett CL.  1994.  The influence of natural organic enhancement on life histories and community structure of bathyal polychaetes. Reproduction, larval biology, and recruitment of the deep-sea benthos. ( Young CM, Eckelbarger KJ, Eds.).:261-283., New York: Columbia University Press Abstract
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