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

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

Talley, TS, Crooks JA, Levin LA.  2001.  Habitat utilization and alteration by the invasive burrowing isopod, Sphaeroma quoyanum, in California salt marshes. Marine Biology. 138:561-573.   10.1007/s002270000472   AbstractWebsite

In recent years the pace of exotic species introduction and invasion has accelerated, particularly in estuaries and wetlands. Species invasions may affect coastal ecosystems in many ways. Alteration of sedimentary environments, through structure formation and burrowing, has particularly dramatic effects on coastal habitats. This study examines modification of channel bank and marsh edge habitat by the burrowing Australasian isopod Sphaeroma quoyanum Milne Edwards, in created and natural salt marshes of San Diego Bay and San Francisco Bay. Abundance and distribution patterns of this isopod species, its relationships with habitat characteristics, and its effects on sediment properties and bank erosion were examined seasonally, and in several marsh microhabitats. Mean isopod densities were 1541 and 2936 individuals per 0.25 m(2) in San Francisco Bay, and 361 and 1153 individuals per 0.25 m(2) in San Diego Bay study sites during December and July 1998, respectively. This isopod forms dense, anastomosing burrow networks. S. quoyanum densities did not differ as a function of location within creeks or location in natural versus created marshes. Burrows, which are on average 6 mm wide and 2 cm long, were associated with firm sediments containing high detrital biomass. Although erosion is a natural process along salt marsh banks, enclosure experiments demonstrated that isopod activities can enhance sediment loss from banks. In areas infested with S. quoyanum, losses may exceed 100 cm of marsh edge per year. The effects of habitat alteration by this invading species are likely to increase in severity in the coastal zone as these ecosystems become degraded.

Fodrie, FJ, Levin LA, Rathburn AE.  2009.  High densities and depth-associated changes of epibenthic megafauna along the Aleutian margin from 2000-4200 m. Journal of the Marine Biological Association of the United Kingdom. 89:1517-1527.   10.1017/s0025315409000903   AbstractWebsite

The Aleutian margin is a dynamic environment underlying a productive coastal ocean and subject to frequent tectonic disturbance. In July 2004, We used over 500 individual bottom images from towed camera transects to investigate patterns of epibenthic megafaunal density and community composition on the contiguous Aleutian margin (53 degrees N 163 degrees W) at depths of 2000 m, 3200 m and 4200 M. We also examined the influence of vertical isolation on the megafaunal assemblage across a topographic rise at 3200 m, located 30 km from the main margin and elevated 800 m above the surrounding seafloor. In comparison to previous reports from bathyal and abyssal depths, megafaunal densities along the Aleutian margin were remarkably high, averaging 5.38 +/- 0.43 (mean +/- 1 standard error), 0.32 +/- 0.02 to 0.43 +/- 0.03 and 0.27 +/- 0.01 individuals m(-2) at 2000 m, 3200 m and 4200 m, respectively. Diversity at 2000 M Was elevated by 15-30% over the deeper sites (3200-4200 m) depending on the metric, while evenness was depressed by similar to 10%. Levels of richness and evenness were similar among the three deeper sites. Echinoderms were the most abundant phylum at each depth; ophiuroids accounted for 89% of individuals in photographs at 2000 m, echinoids were dominant at 3200 M (39%), and holothurians dominated at 4200 m (47%). We observed a 26% reduction in megafaunal density across the summit of the topographic rise relative to that documented on the continental slope at the same depth. However, the two communities at 3200 m were very similar in composition. Together, these data support the modified 'archibenthal zone of transition' framework for slope community patterns with distinct communities along the middle and lower slope (the upper slope was not evaluated here). This study fills a geographical gap by providing baseline information for a relatively pristine, high-latitude, deep-sea benthic ecosystem. As pressures grow for drilling, fishing and mining on high-latitude margins, such data can serve as a reference point for much-needed studies on the ecology, long-term dynamics, and anthropogenically induced change of these habitats.

Frieder, CA, Nam SH, Martz TR, Levin LA.  2012.  High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences. 9:3917-3930. AbstractWebsite

Predicting consequences of ocean deoxygenation and ocean acidification for nearshore marine ecosystems requires baseline dissolved oxygen (DO) and carbonate chemistry data that are both high-frequency and high-quality. Such data allow accurate assessment of environmental variability and present-day organism exposure regimes. In this study, scales of DO and pH variability were characterized over one year in a nearshore kelp forest ecosystem in the Southern California Bight. DO and pH were strongly, positively correlated, revealing that organisms on this upwelling shelf are not only exposed to low pH but also to low DO. The dominant scale of temporal DO and pH variability occurred on semi-diurnal, diurnal and event (days-weeks) time scales. Daily ranges in DO and pH at 7 m water depth (13 mab) could be as large as 220 mu mol kg(-1) and 0.36 units, respectively. Sources of pH and DO variation include photosynthesis within the kelp forest ecosystem, which can elevate DO and pH by up to 60 mu mol kg(-1) and 0.1 units over one week following the intrusion of high-density, nutrient-rich water. Accordingly, highly productive macrophyte-based ecosystems could serve as deoxygenation and acidification refugia by acting to elevate DO and pH relative to surrounding waters. DO and pH exhibited greater spatial variation over a 10 m increase in water depth (from 7 to 17 m) than along a 5 km stretch of shelf in a cross-shore or alongshore direction. Over a three-month time period, mean DO and pH at 17 m water depth were 168 mu mol kg(-1) and 7.87, respectively. These values represent a 35% decrease in mean DO and 37% increase in [H+] relative to near-surface waters. High-frequency variation was also reduced at depth. The mean daily range in DO and pH was 39% and 37% less, respectively, at 17m water depth relative to 7 m. As a consequence, the exposure history of an organism is largely a function of its depth of occurrence within the kelp forest. With knowledge of local alkalinity conditions and high-frequency temperature, salinity, and pH data, we estimated pCO(2) and calcium carbonate saturation states with respect to calcite and aragonite (Omega(calc) and Omega(arag)) for the La Jolla kelp forest at 7 m and 17 m water depth. pCO(2) ranged from 246 to 1016 mu atm, Omega(calc) was always supersaturated, and Omega(arag) was undersaturated at the beginning of March for five days when pH was less than 7.75 and DO was less than 115 mu mol kg(-1). These findings raise the possibility that the benthic communities along eastern boundary current systems are currently acclimatized and adapted to natural, variable, and low DO and pH. Still, future exposure of coastal California populations to even lower DO and pH may increase as upwelling intensifies and hypoxic boundaries shoal, compressing habitats and challenging the physiological capacity of intolerant species.

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.

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, 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.

Levin, LA, Baco AR, Bowden DA, Colaco A, Cordes EE, Cunha MR, Demopoulos AWJ, Gobin J, Grupe BM, Le J, Metaxas A, Netburn AN, Rouse GW, Thurber AR, Tunnicliffe V, Van Dover CL, Vanreusel A, Watling L.  2016.  Hydrothermal vents and methane seeps: Rethinking the sphere of influence. Frontiers in Marine Science. 3   10.3389/fmars.2016.00072   AbstractWebsite

Although initially viewed as oases within a barren deep ocean, hydrothermal vent and methane seep communities are now recognized to interact with surrounding ecosystems on the sea floor and in the water column, and to affect global geochemical cycles. The importance of understanding these interactions is growing as the potential rises for disturbance from oil and gas extraction, seabed mining and bottom trawling. Here we synthesize current knowledge of the nature, extent and time and space scales of vent and seep interactions with background systems. We document an expanded footprint beyond the site of local venting or seepage with respect to elemental cycling and energy flux, habitat use, trophic interactions, and connectivity. Heat and energy are released, global biogeochemical and elemental cycles are modified, and particulates are transported widely in plumes. Hard and biotic substrates produced at vents and seeps are used by “benthic background” fauna for attachment substrata, shelter, and access to food via grazing or through position in the current, while particulates and fluid fluxes modify planktonic microbial communities. Chemosynthetic production provides nutrition to a host of benthic and planktonic heterotrophic background species through multiple horizontal and vertical transfer pathways assisted by flow, gamete release, animal movements, and succession, but these pathways remain poorly known. Shared species, genera and families indicate that ecological and evolutionary connectivity exists among vents, seeps, organic falls and background communities in the deep sea; the genetic linkages with inactive vents and seeps and background assemblages however, are practically unstudied. The waning of venting or seepage activity generates major transitions in space and time that create links to surrounding ecosystems, often with identifiable ecotones or successional stages. The nature of all these interactions is dependent on water depth, as well as regional oceanography and biodiversity. Many ecosystem services are associated with the interactions and transitions between chemosynthetic and background ecosystems, for example carbon cycling and sequestration, fisheries production, and a host of non-market and cultural services. The quantification of the sphere of influence of vents and seeps could be beneficial to better management of deep-sea environments in the face of growing industrialization.