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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, LA, Gooday A.  2003.  The Deep Atlantic Ocean. Ecosystems of the deep oceans. ( Tyler PA, Ed.).:111-178., Amsterdam ; New York: Elsevier Abstract
Levin, LA, Le Bris N.  2015.  The deep ocean under climate change. Science. 350:766-768.   10.1126/science.aad0126   AbstractWebsite

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

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

The deep sea, the largest biome on Earth, has a series of characteristics that make this environment both distinct from other marine and land ecosystems and unique for the entire planet. This review describes these patterns and processes, from geological settings to biological processes, biodiversity and biogeographical patterns. It concludes with a brief discussion of current threats from anthropogenic activities to deep-sea habitats and their fauna. Investigations of deep-sea habitats and their fauna began in the late 19th century. In the intervening years, technological developments and stimulating discoveries have promoted deep-sea research and changed our way of understanding life on the planet. Nevertheless, the deep sea is still mostly unknown and current discovery rates of both habitats and species remain high. The geological, physical and geochemical settings of the deep-sea floor and the water column form a series of different habitats with unique characteristics that support specific faunal communities. Since 1840, 28 new habitats/ecosystems have been discovered from the shelf break to the deep trenches and discoveries of new habitats are still happening in the early 21st century. However, for most of these habitats the global area covered is unknown or has been only very roughly estimated; an even smaller - indeed, minimal - proportion has actually been sampled and investigated. We currently perceive most of the deep-sea ecosystems as heterotrophic, depending ultimately on the flux on organic matter produced in the overlying surface ocean through photosynthesis. The resulting strong food limitation thus shapes deep-sea biota and communities, with exceptions only in reducing ecosystems such as inter alia hydrothermal vents or cold seeps. Here, chemoautolithotrophic bacteria play the role of primary producers fuelled by chemical energy sources rather than sunlight. Other ecosystems, such as seamounts, canyons or cold-water corals have an increased productivity through specific physical processes, such as topographic modification of currents and enhanced transport of particles and detrital matter. Because of its unique abiotic attributes, the deep sea hosts a specialized fauna. Although there are no phyla unique to deep waters, at lower taxonomic levels the composition of the fauna is distinct from that found in the upper ocean. Amongst other characteristic patterns, deep-sea species may exhibit either gigantism or dwarfism, related to the decrease in food availability with depth. Food limitation on the seafloor and water column is also reflected in the trophic structure of heterotrophic deep-sea communities, which are adapted to low energy availability. In most of these heterotrophic habitats, the dominant megafauna is composed of detritivores, while filter feeders are abundant in habitats with hard substrata (e. g. mid-ocean ridges, seamounts, canyon walls and coral reefs). Chemoautotrophy through symbiotic relationships is dominant in reducing habitats. Deep-sea biodiversity is among of the highest on the planet, mainly composed of macro and meiofauna, with high evenness. This is true for most of the continental margins and abyssal plains with hot spots of diversity such as seamounts or cold-water corals. However, in some ecosystems with particularly "extreme" physicochemical processes (e.g. hydrothermal vents), biodiversity is low but abundance and biomass are high and the communities are dominated by a few species. Two large-scale diversity patterns have been discussed for deep-sea benthic communities. First, a unimodal relationship between diversity and depth is observed, with a peak at intermediate depths (2000-3000 m), although this is not universal and particular abiotic processes can modify the trend. Secondly, a poleward trend of decreasing diversity has been discussed, but this remains controversial and studies with larger and more robust data sets are needed. Because of the paucity in our knowledge of habitat coverage and species composition, biogeographic studies are mostly based on regional data or on specific taxonomic groups. Recently, global biogeographic provinces for the pelagic and benthic deep ocean have been described, using environmental and, where data were available, taxonomic information. This classification described 30 pelagic provinces and 38 benthic provinces divided into 4 depth ranges, as well as 10 hydrothermal vent provinces. One of the major issues faced by deep-sea biodiversity and biogeographical studies is related to the high number of species new to science that are collected regularly, together with the slow description rates for these new species. Taxonomic coordination at the global scale is particularly difficult, but is essential if we are to analyse large diversity and biogeographic trends. Because of their remoteness, anthropogenic impacts on deep-sea ecosystems have not been addressed very thoroughly until recently. The depletion of biological and mineral resources on land and in shallow waters, coupled with technological developments, are promoting the increased interest in services provided by deep-water resources. Although often largely unknown, evidence for the effects of human activities in deep-water ecosystems - such as deep-sea mining, hydrocarbon exploration and exploitation, fishing, dumping and littering - is already accumulating. Because of our limited knowledge of deep-sea biodiversity and ecosystem functioning and because of the specific life-history adaptations of many deep-sea species (e. g. slow growth and delayed maturity), it is essential that the scientific community works closely with industry, conservation organisations and policy makers to develop robust and efficient conservation and management options.

Smith, CR, Levin LA, Mullineaux LS.  1998.  Deep-sea biodiversity: a tribute to Robert R. Hessler. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 45:1-11.   10.1016/s0967-0645(97)00088-x   AbstractWebsite

Through extraordinary research and training of graduate students, Robert R. Hessler has profoundly influenced our knowledge of biodiversity in the deep sea. This special volume honors his contributions and presents recent advances in the study of deep-sea biodiversity on a broad range of topics. (C) 1998 Elsevier Science Ltd. All rights reserved.

Niner, HJ, Ardron JA, Escobar EG, Gianni M, Jaeckel A, Jones DOB, Levin LA, Smith CR, Thiele T, Turner PJ, Vandover CL, Watling L, Gjerde KM.  2018.  Deep-sea mining with no net loss of biodiversity-an impossible aim. Frontiers in Marine Science. 5   10.3389/fmars.2018.00053   AbstractWebsite

Deep-sea mining is likely to result in biodiversity loss, and the significance of this to ecosystem function is not known. "Out of kind" biodiversity offsets substituting one ecosystem type (e.g., coral reefs) for another (e.g., abyssal nodule fields) have been proposed to compensate for such loss. Here we consider a goal of no net loss (NNL) of biodiversity and explore the challenges of applying this aim to deep seabed mining, based on the associated mitigation hierarchy (avoid, minimize, remediate). We conclude that the industry cannot at present deliver an outcome of NNL. This results from the vulnerable nature of deep-sea environments to mining impacts, currently limited technological capacity to minimize harm, significant gaps in ecological knowledge, and uncertainties of recovery potential of deep-sea ecosystems. Avoidance and minimization of impacts are therefore the only presently viable means of reducing biodiversity losses from seabed mining. Because of these constraints, when and if deep-sea mining proceeds, it must be approached in a precautionary and step-wise manner to integrate new and developing knowledge. Each step should be subject to explicit environmental management goals, monitoring protocols, and binding standards to avoid serious environmental harm and minimize loss of biodiversity. "Out of kind" measures, an option for compensation currently proposed, cannot replicate biodiversity and ecosystem services lost through mining of the deep seabed and thus cannot be considered true offsets. The ecosystem functions provided by deep-sea biodiversity contribute to a wide range of provisioning services (e.g., the exploitation of fish, energy, pharmaceuticals, and cosmetics), play an essential role in regulatory services (e.g., carbon sequestration) and are important culturally. The level of "acceptable" biodiversity loss in the deep sea requires public, transparent, and well-informed consideration, as well as wide agreement. If accepted, further agreement on how to assess residual losses remaining after the robust implementation of the mitigation hierarchy is also imperative. To ameliorate some of the inter-generational inequity caused by mining-associated biodiversity losses, and only after all NNL measures have been used to the fullest extent, potential compensatory actions would need to be focused on measures to improve the knowledge and protection of the deep sea and to demonstrate benefits that will endure for future generations.

Levin, LA, Mengerink K, Gjerde KM, Rowden AA, Vandover CL, Clark MR, Ramirez-Llodra E, Currie B, Smith CR, Sato KN, Gallo N, Sweetman AK, Lily H, Armstrong CW, Brider J.  2016.  Defining "serious harm" to the marine environment in the context of deep-seabed mining. Marine Policy. 74:245-259.   10.1016/j.marpol.2016.09.032   AbstractWebsite

Increasing interest in deep-seabed mining has raised many questions surrounding its potential environmental impacts and how to assess the impacts' significance. Under the United Nations Convention on the Law of the Sea (UNCLOS), the International Seabed Authority (ISA) is charged with ensuring effective protection of the marine environment as part of its responsibilities for managing mining in seabed areas beyond national jurisdiction (the Area) on behalf of humankind. This paper examines the international legal context for protection of the marine environment and defining the significant adverse change that can cause "serious harm", a term used in the ISA Mining Code to indicate a level of harm that strong actions must be taken to avoid. It examines the thresholds and indicators that can reflect significant adverse change and considers the specific vulnerability of the four ecosystems associated with the minerals targeted for mining: (1) manganese (polymetallic) nodules, (2) seafloor massive (polymetallic) sulphides, (3) cobalt-rich (polymetallic) crusts and (4) phosphorites. The distributions and ecological setting, probable mining approaches and the potential environmental impacts of mining are examined for abyssal polymetallic nodule provinces, hydrothermal vents, seamounts and phosphorite-rich continental margins. Discussion focuses on the special features of the marine environment that affect the significance of the predicted environmental impacts and suggests actions that will advance understanding of these impacts.

Levin, LA, Caswell H, Depatra KD, Creed EL.  1987.  Demographic consequences of larval development mode: planktotrophy vs. lecithotrophy in Streblospio benedicti. Ecology. 68:1877-1886.   10.2307/1939879   AbstractWebsite

This paper examines the demographic consequences of planktotrophic and lecithotrophic development in an estuarine polychaete. Two strains of Streblospio benedicti (Spionidae) were reared in the laboratory from birth through death at 20⚬C and salinity 34 per mille. Survivorship and reproductive data were collected weekly and were used to construct life tables and population projection matrices for each development mode. Planktotrophic females reproduced earlier, and had higher fecundity and a shorter generation time than lecithotrophic females, but also exhibited higher mortality early in life. Despite the apparently opportunistic nature of the planktotrophic life history traits, the finite rate of increase (λ) in the lecithotrophic strain (1.319 wk-1) exceeded that of the planktotrophic strain (1.205 wk-1). Net reproductive rate (R0) was also higher for the lecithotrophs (93.4) than for the planktotrophs (17.6) Peak reproductive values were attained earlier in planktotrophs than in lecithotrophs. Sensitivity analyses indicate that λ is most sensitive to changes in larval and juvenile survivorship, and that the differences in λ were almost completely determined by life table differences during the first 15 wk of life. The potential population growth rates obtained in this study agree well with those estimated for other opportunistic polychaete species such as Capitella sp. I and Polydora ligni. Under uniform conditions the two strains of S. benedicti achieved similar growth rates with very different life history traits. We hypothesize that each combination of traits may be adaptive under different circumstances in the field.

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.

Vandover, CL, Smith CR, Ardron J, Dunn D, Gjerde K, Levin L, Smith S, Dinard Workshop C.  2012.  Designating networks of chemosynthetic ecosystem reserves in the deep sea. Marine Policy. 36:378-381.   10.1016/j.marpol.2011.07.002   AbstractWebsite

From the moment of their discovery, chemosynthetic ecosystems in the deep sea have held intrinsic scientific value. At the same time that the scientific community is studying chemosynthetic ecosystems other sectors are either engaged in, or planning for, activities that may adversely impact these ecosystems. There is a need and opportunity now to develop conservation strategies for networks of chemosynthetic ecosystem reserves in national and international waters through collaboration among concerned stakeholders. (C) 2011 Elsevier Ltd. All rights reserved.

Dibacco, C, Levin LA.  2000.  Development and application of elemental fingerprinting to track the dispersal of marine invertebrate larvae. Limnology and Oceanography. 45:871-880. AbstractWebsite

The early life history of many marine benthic invertebrate and fish species involves a planktonic larval stage that allows exchange of individuals among separated adult populations. Here, we demonstrate how natural and anthropogenic trace elements can be used to determine larval origins and assess bay-ocean exchange of invertebrate larvae. Trace elements can be effective site markers for estuaries because run-off and pollutant loading often impart distinct elemental signatures to bay habitats relative to nearshore coastal environments. Crab larvae originating from San Diego Bay (SDB) were distinguished from those originating in neighboring embayments and exposed coastal habitats by comparing multiple trace-element concentrations ("fingerprints") in individuals. Discriminant function analysis (DFA) was used to characterize stage I zoeae of the striped shore crab, Pachygrapsus crassipes, of known origin (reference larvae) via trace-elemental composition (i.e., Cu, Zn, Mn, Sr, Ca). Linear discriminant functions were used to identify the origin and characterize the exchange of stage I P. crassipes zoeae between SDB and the nearshore coastal environment during one spring tidal cycle. Elemental fingerprinting revealed that most (87%) of the stage I larvae collected at the bay entrance during the flood tide were larvae of SDB origin that were reentering the bay. Nearly one third of zoeae sampled (32%) at the entrance during ebb tide were coastal larvae leaving the bay and returning to open water. The observed bidirectional exchange contrasts with the unidirectional transport of zoeae out of the bay predicted from stage I vertical migratory behavior. Because P. crassipes zoeal survivorship is lower in SDB than in coastal waters, bay-ocean exchange has significant implications for the dynamics of P. crassipes populations. Trace-elemental fingerprinting of invertebrate larvae promises to facilitate investigations of many previously intractable questions about larval transport and dynamics.

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.

Bailey, JV, Salman V, Rouse GW, Schulz-Vogt HN, Levin LA, Orphan VJ.  2011.  Dimorphism in methane seep-dwelling ecotypes of the largest known bacteria. ISME Journal. 5:1926-1935.   10.1038/ismej.2011.66   AbstractWebsite

We present evidence for a dimorphic life cycle in the vacuolate sulfide-oxidizing bacteria that appears to involve the attachment of a spherical Thiomargarita-like cell to the exteriors of invertebrate integuments and other benthic substrates at methane seeps. The attached cell elongates to produce a stalk-like form before budding off spherical daughter cells resembling free-living Thiomargarita that are abundant in surrounding sulfidic seep sediments. The relationship between the attached parent cell and free-living daughter cell is reminiscent of the dimorphic life modes of the prosthecate Alphaproteobacteria, but on a grand scale, with individual elongate cells reaching nearly a millimeter in length. Abundant growth of attached Thiomargarita-like bacteria on the integuments of gastropods and other seep fauna provides not only a novel ecological niche for these giant bacteria, but also for animals that may benefit from epibiont colonization. The ISME Journal (2011) 5, 1926-1935; doi: 10.1038/ismej.2011.66; published online 23 June 2011

Levin, LA.  1981.  Dispersion, feeding behavior and competition in two spionid polychaetes. Journal of Marine Research. 39:99-117. AbstractWebsite

Spatial analysis, laboratory and field experiments, and feeding observations indicate contrasting patterns of aggression in the polychaetes Pseudopolydora paucibranchiata (Okuda) and Streblospio benedicti (Webster) and provide the 1st evidence of territoriality in a spionid polychaete (Pseudopolydora). On the intertidal mudflats of Mission Bay in San Diego, California, Pseudopolydora is spaced more evenly than expected from a random distribution; the dispersion of Streblospio does not depart significantly from random. Recruitment patterns in Pseudopolydora indicate that uniform spacing is initiated during settlement and enhanced by subsequent interactions between individuals. Field manipulations provide evidence for adult interactions with settling larvae which may also play a role in generating non-random dispersion in Pseudopolydora. Differences between Pseudopolydora and Streblospia in aggressive behavior (palp fighting and biting) and feeding mechanisms are correlated with different space requirements for feeding and tube building. Laboratory observations of surface deposit and suspension feeding indicate that Pseudopolydora is more aggressive and frequently uses its mouth and palps to acquire food particles. These species differ in their site of food particle selection. Streblospio relies primarily on lips and mouth to taste particles; Pseudopolydora more frequently uses its palps. Pseudopolydora defends palp territories necessary for the acquisition of food and tube building materials. The spatial analysis, in conjunction with experimental results and behavioral observations, suggest strong competition in Pseudopolydora but not in Streblospio.

Gooday, AJ, Levin LA, Thomas CL, Hecker B.  1992.  The distribution and ecology of Bathysiphon filiformis sars and B. major de folin (Protista, Foraminiferida) on the continental slope off North Carolina. Journal of Foraminiferal Research. 22:129-146. AbstractWebsite

Two large species of the agglutinated foraminifera genus Bathysiphon are common in samples and photographs from bathyal depths on the North Carolina continental slope: B. filiformis off Cape Hatteras (588-930 m bathymetric depth) and B. major off Cape Lookout (850-1950 m depth). The sampling area, and particularly the 850 m station where B. filiformis is abundant (mean densities of 59-154 per m2), is believed to receive large inputs of organic material from various sources. This is consistent with the previously observed occurrence of large Bathysiphon species in regions of high food supply. Ten camera sled transects across the eastern U.S. continental slope between 32-degrees-N and 41-degrees-N emphasize the abundance of B. filiformis in the Cape Hatteras area compared with its rarity or absence elsewhere along the continental slope. Box cores, bottom photographs, and direct submersible observations indicate that B. filiformis tubes project above the sediment in an arcuate curve with only the lower 1 cm or so buried. Bathysiphon major adopts a similar orientation but has a greater proportion (50-80%) of the tube buried. The voluminous, dense, granular protoplasm of both species contains biogenic particles (including diatoms, in B. filiformis only), dinoflagellate cysts, fungal remains, pollen grains, tintinnid loricae, polychaete jaws and setae, benthic foraminiferal tests, and fish tooth fragments), suggesting that they feed mainly on material derived from the sediment surface. Submersible observations indicate that B. filiformis is patchily distributed at 100 m scales. Smaller scale dispersion patterns (analyzed from photographs) are generally random but with a tendency to be aggregated at lower densities and uniform at higher densities. A variety of metazoans and foraminifers live epifaunally on the outer surfaces of B. filiformis tubes. The most frequently occurring metazoans were larvae and juveniles of an unidentified gastropod and a tubiculous terebellid polychaete Nicolea sp. The most common epifaunal foraminifers were Tritaxis conica and Trochammina sp. Tubes of B. major, however, are virtually devoid of epifauna. Our results support the view that large, agglutinated rhizopod tests may influence the structure of deep-water benthic communities. However, in the case of Bathysiphon on the North Carolina continental slope, the effect appears limited to taxa directly associated with the foraminiferal tubes.

Neira, C, Ingels J, Mendoza G, Hernandez-Lopez E, Levin LA.  2018.  Distribution of meiofauna in bathyal sediments influenced by the oxygen minimum zone off Costa Rica. Frontiers in Marine Science. 5   10.3389/fmars.2018.00448   AbstractWebsite

Ocean deoxygenation has become a topic of increasing concern because of its potential impacts on marine ecosystems, including oxygen minimum zone (OMZ) expansion and subsequent benthic effects. We investigated the influence of oxygen concentration and organic matter (OM) availability on metazoan meiofauna within and below an OMZ in bathyal sediments off Costa Rica, testing the hypothesis that oxygen and OM levels are reflected in meiofaunal community structures and distribution. Mean total densities in our sampling cores (400-1800 m water depth) were highest with 3688 ind. 10 cm(-2) at the OMZ core at 400 m water depth, decreasing rapidly downslope. Nematodes were overall dominant, with a maximum of 99.9% in the OMZ core, followed by copepods (13%), nauplii (4.8%), and polychaetes (3%). Relative copepod and nauplii abundance increased consistently with depth and increasing bottom-water O-2. Meiofaunal composition was significantly different among sites, with lower taxonomic diversity at OMZ sites relative to deeper, oxygenated sites. Vertical distribution patterns within sediments showed that in strongly oxygen-depleted sites less meiofauna was concentrated in the surface sediment than at deeper slope sites. Highest meiofaunal abundance and lowest diversity occurred under lowest oxygen and highest pigment levels, whereas highest diversity occurred under highest oxygen-concentrations and low pigments, as well as high quality of sedimentary pigment (chl a/phaeo) and organic carbon (C/N). The lower meiofaunal diversity, and lower structural and trophic complexity, at oxygen-depleted sites raises concerns about changes in the structure and function of benthic marine ecosystems in the face of OMZ expansions.

Moseman, SM, Zhang R, Qian PY, Levin LA.  2009.  Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biological Invasions. 11:225-239.   10.1007/s10530-008-9227-0   AbstractWebsite

Impacts of invasive species on microbial components of wetland ecosystems can reveal insights regarding functional consequences of biological invasions. Nitrogen fixation (acetylene reduction) rates and diversity of nitrogen fixers, determined by genetic fingerprinting (T-RFLP) of the nifH gene, were compared between native and invaded sediments in three systems. Variable responses of nitrogen fixing microbes to invasion by a non-native mussel, Musculista senhousia, and mangrove, Avicennia marina, in Kendall Frost-Northern Wildlife Preserve (Mission Bay) and salt cedar, Tamarisk (Tamarix spp.) in Tijuana Estuary suggest microbes respond to both species- and site-specific influences. Structurally similar invaders (the mangrove and salt cedar) produced different effects on activity and diversity of nitrogen fixers, reflecting distinct environmental contexts. Despite relative robustness of microbial community composition, subtle differences in total diversity or activity of nitrogen fixers reveal that microbes are not immune to impacts of biological invasions, and that functional redundancy of microbial diversity is limited, with significant consequences for functional dynamics of wetlands.

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

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

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

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

Tegner, MJ, Levin LA.  1982.  Do sea urchins and abalones compete in California kelp forest communities? Echinoderms, proceedings of the International Conference, Tampa Bay. ( Lawrence JM, Ed.).:265-271., RotterdamSalem, NH: A.A. Balkema ;Distributed in USA & Canada by MBS Abstract
Levin, LA, Gooday AJ, James DW.  2001.  Dressing up for the deep: agglutinated protists adorn an irregular urchin. Journal of the Marine Biological Association of the United Kingdom. 81:881-882.   10.1017/s0025315401004738   AbstractWebsite

A specimen of the deep-water, spatangoid urchin. Cystochinus loveni, wearing a costume of agglutinated protists, was collected from 3088 m in the Gulf of Alaska, north-east Pacific. Over 24 putative taxa of living and dead foraminiferans and xenophyophores, as well as a sipunculan.. polychaete tanaid, and two isopods, were collected from the dorsal surface of this single individual, This is the first report of a deep-sea urchin using rhizopod protists and it is proposed that the urchin acquires camouflage or benefits from increased specific gravity associated with the protistan cloak.

Levin, LA.  1983.  Drift tube studies of bay-ocean water exchange and implications for larval dispersal. Estuaries. 6:364-371.   10.2307/1351395   AbstractWebsite

Surface water transport and larval dispersal potential within Mission Bay, San Diego, California and along the southern California coast were studied with drift test tubes. Drift tubes, released once during each season at six sites inside Mission Bay, traveled up to 173 km north and 205 km south of Mission Bay at maximum rates of 36 cm per s (north) and 50 cm per s (south). These findings were used to estimate probability of larval transport out of Mission Bay for the intertidal spionid polychaete Pseudopolydora paucibranchiata (Okuda) which occurred in the back of the bay. Outer coast drift tube returns were used to determine potential for gene flow, via larval exchange, between populations in isolated bays along the California coast. Drift tube recoveries and larval abundances in the plankton indicate that few Pseudopolydora larvae leave Mission Bay, but that longshore currents can carry those which do to other suitable bay habitats.

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

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