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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.

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.

Gallo, ND, Levin LA.  2016.  Fish ecology and evolution in the world's oxygen minimum zones and implications of ocean deoxygenation. Advances in Marine Biology, Vol 74. 74( Curry BE, Ed.).:117-198., San Diego: Elsevier Academic Press Inc   10.1016/bs.amb.2016.04.001   Abstract

Oxygen minimum zones (OMZs) and oxygen limited zones (OLZs) are important oceanographic features in the Pacific, Atlantic, and Indian Ocean, and are characterized by hypoxic conditions that are physiologically challenging for demersal fish. Thickness, depth of the upper boundary, minimum oxygen levels, local temperatures, and diurnal, seasonal, and interannual oxycline variability differ regionally, with the thickest and shallowest OMZs occurring in the subtropics and tropics. Although most fish are not hypoxia-tolerant, at least 77 demersal fish species from 16 orders have evolved physiological, behavioural, and morphological adaptations that allow them to live under the severely hypoxic, hypercapnic, and at times sulphidic conditions found in OMZs. Tolerance to OMZ conditions has evolved multiple times in multiple groups with no single fish family or genus exploiting all OMZs globally. Severely hypoxic conditions in OMZs lead to decreased demersal fish diversity, but fish density trends are variable and dependent on region-specific thresholds. Some OMZ-adapted fish species are more hypoxiatolerant than most megafaunal invertebrates and are present even when most invertebrates are excluded. Expansions and contractions of OMZs in the past have affected fish evolution and diversity. Current patterns of ocean warming are leading to ocean deoxygenation, causing the expansion and shoaling of OMZs, which is expected to decrease demersal fish diversity and alter trophic pathways on affected margins. Habitat compression is expected for hypoxia-intolerant species, causing increased susceptibility to overfishing for fisheries species. Demersal fisheries are likely to be negatively impacted overall by the expansion of OMZs in a warming world.

Frieder, CA, Gonzalez JP, Bockmon EE, Navarro MO, Levin LA.  2014.  Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae? Global Change Biology. 20:754-764.   10.1111/gcb.12485   AbstractWebsite

Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2 ]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2 ], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2 ], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2 ] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2 ] reflective of their environment (80-260 ╬╝mol kg(-1) ). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.

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.

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

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

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.

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

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

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.