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Parker, EA, Rippy MA, Mehring AS, Winfrey BK, Ambrose RF, Levin LA, Grant SB.  2017.  Predictive power of clean bed filtration theory for fecal indicator bacteria removal in stormwater biofilters. Environmental Science & Technology. 51:5703-5712.   10.1021/acs.est.7b00752   AbstractWebsite

Green infrastructure (also referred to as low impact development, or LID) has the potential to transform urban stormwater runoff from an environmental threat to a valuable water resource. In this paper we focus on the removal of fecal indicator bacteria (FIB, a pollutant responsible for runoff associated inland and coastal beach closures) in stormwater biofilters (a common type of green infrastructure). Drawing on a combination of previously published and new laboratory studies of FIB removal in biofilters, we find that 66% of the variance in FIB removal rates can be explained by clean bed filtration theory (CBFT, 31%), antecedent dry period (14%), study effect (8%), biofilter age (7%), and the presence or absence of shrubs (6%). Our analysis suggests that, with the exception of shrubs, plants affect FIB removal indirectly by changing the infiltration rate, not directly by changing the FIB removal mechanisms or altering filtration rates in ways not already accounted for by CBFT. The analysis presented here represents a significant step forward in our understanding of how physicochemical theories (such as CBFT) can be melded with hydrology, engineering design, and ecology to improve the water quality benefits of green infrastructure.

Hansman, RL, Thurber AR, Levin LA, Aluwihare LI.  2017.  Methane fates in the benthos and water column at cold seep sites along the continental margin of Central and North America. Deep-Sea Research Part I-Oceanographic Research Papers. 120:122-131.   10.1016/j.dsr.2016.12.016   AbstractWebsite

The potential influence of methane seeps on carbon cycling is a key question for global assessments, but the study of carbon cycling in surface sediments and the water column of cold seep environments is complicated by the high temporal and spatial variability of fluid and gas fluxes at these sites. In this study we directly examined carbon sources supporting benthic and planktonic food webs at venting methane seeps using isotopic and molecular approaches that integrate this variability. At four seep environments located along North and Central America, microorganisms from two size fractions were collected over several days from 2800 to 90501 of seawater to provide a time-integrated measure of key microbial groups and the carbon sources supporting the overall planktonic microbial community. In addition to water column measurements, the extent of seafloor methane release was estimated at two of the sites by examining the stable carbon isotopic signature (delta C-13) of benthic metazoan infauna. This signature reveals carbon sources fueling the base of the food chain and thus provides a metric that represents a time-integrated view of the dominant microbial processes within the sediment. The stable carbon isotopic composition of microbial DNA (delta C-13-DNA), which had values between -17.0 and -19.5%(0), indicated that bulk planktonic microbial production was not ultimately linked to methane or other C-13-depleted seep-derived carbon sources. Instead these data support the importance of organic carbon derived from either photo- or chemoautotrophic CO2 fixation to the planktonic food web. Results of qPCR of microbial DNA sequences coding for a subunit of the particulate methane monooxygenase gene (pmoA) showed that only a small percentage of the planktonic microbial community were potential methane oxidizers possessing pmoA (< 5% of 16S rRNA gene copies). There was an overall decrease of C-13-depleted carbon fueling the benthic metazoan community from 3 to 5 cm below the seafloor to the sediment surface, reflecting limited use of isotopically depleted carbon at the sediment surface. Rare methane emission as indicated by limited aerobic methane oxidation acts to corroborate our findings for the planktonic microbial community.

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.

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

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

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.

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.

Mehring, AS, Hatt BE, Kraikittikun D, Orelo BD, Rippy MA, Grant SB, Gonzalez JP, Jiang SC, Ambrose RF, Levin LA.  2016.  Soil invertebrates in Australian rain gardens and their potential roles in storage and processing of nitrogen. Ecological Engineering. 97:138-143.   10.1016/j.ecoleng.2016.09.005   AbstractWebsite

Research on rain gardens generally focuses on hydrology, geochemistry, and vegetation. The role of soil invertebrates has largely been overlooked, despite their well-known impacts on soil nutrient storage, removal, and processing. Surveys of three rain gardens in Melbourne, Australia, revealed a soil invertebrate community structure that differed significantly among sites but was stable across sampling dates (July 2013 and April 2014). Megadrilacea (earthworms), Enchytraeidae (potworms), and Collembola (springtails) were abundant in all sites, and together accounted for a median of 80% of total soil invertebrate abundance. Earthworms were positively correlated to soil organic matter content, but the abundances of other taxonomic groups were not strongly related to organic matter content, plant cover, or root biomass across sites. While less than 5% of total soil N was estimated to be stored in the body tissues of these three taxa, and estimated N gas emissions from earthworms (N2O and N-2) were low, ingestion and processing of soil was high (e.g., up to 417% of the upper 5 cm of soil ingested by earthworms annually in one site), suggesting that the contribution of these organisms to N cycling in rain gardens may be substantial. Thus, invertebrate communities represent an overlooked feature of rain garden design that can play an important role in the structure and function of these systems. (C) 2016 Elsevier B.V. All rights reserved.

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.

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

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

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.

Moseman-Valtierra, S, Levin LA, Martin RM.  2016.  Anthropogenic impacts on nitrogen fixation rates between restored and natural Mediterranean salt marshes. Marine Ecology-an Evolutionary Perspective. 37:370-379.   10.1111/maec.12289   AbstractWebsite

To test the effects of site and successional stage on nitrogen fixation rates in salt marshes of the Venice Lagoon, Italy, acetylene reduction assays were performed with Salicornia veneta- and Spartina townsendii-vegetated sediments from three restored (6-14years) and two natural marshes. Average nitrogen fixation (acetylene reduction) rates ranged from 31 to 343 mu mol C2H4.m(-2.)h(-1) among all marshes, with the greatest average rates being from one natural marsh (Tezze Fonde). These high rates are up to six times greater than those reported from Southern California Spartina marshes of similar Mediterranean climate, but substantially lower than those found in moister climates of the Atlantic US coast. Nitrogen fixation rates did not consistently vary between natural and restored marshes within a site (Fossei Est, Tezze Fonde, Cenesa) but were negatively related to assayed plant biomass within the acetylene reduction samples collected among all marshes. Highest nitrogen fixation rates were found at Tezze Fonde, the location closest to the city of Venice, in both natural and restored marshes, suggesting possible site-specific impacts of anthropogenic stress on marsh succession.

Sperling, EA, Frieder CA, Levin LA.  2016.  Biodiversity response to natural gradients of multiple stressors on continental margins. Proceedings of the Royal Society of London B: Biological Sciences. 283   10.1098/rspb.2016.0637   Abstract

Sharp increases in atmospheric CO2 are resulting in ocean warming, acidification and deoxygenation that threaten marine organisms on continental margins and their ecological functions and resulting ecosystem services. The relative influence of these stressors on biodiversity remains unclear, as well as the threshold levels for change and when secondary stressors become important. One strategy to interpret adaptation potential and predict future faunal change is to examine ecological shifts along natural gradients in the modern ocean. Here, we assess the explanatory power of temperature, oxygen and the carbonate system for macrofaunal diversity and evenness along continental upwelling margins using variance partitioning techniques. Oxygen levels have the strongest explanatory capacity for variation in species diversity. Sharp drops in diversity are seen as O2 levels decline through the 0.5–0.15 ml l−1 (approx. 22–6 µM; approx. 21–5 matm) range, and as temperature increases through the 7–10°C range. pCO2 is the best explanatory variable in the Arabian Sea, but explains little of the variance in diversity in the eastern Pacific Ocean. By contrast, very little variation in evenness is explained by these three global change variables. The identification of sharp thresholds in ecological response are used here to predict areas of the seafloor where diversity is most at risk to future marine global change, noting that the existence of clear regional differences cautions against applying global thresholds.

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.

Neira, C, Mendoza G, Porrachia M, Stransky C, Levin LA.  2015.  Macrofaunal recolonization of copper-contaminated sediments in San Diego Bay. Marine Pollution Bulletin. 101:794-804.   10.1016/j.marpolbul.2015.09.023   AbstractWebsite

Effects of Cu-loading on macrofaunal recolonization were examined in Shelter Island Yacht Basin (San Diego Bay, California). Sediments with high and low Cu levels were defaunated and Cu-spiked, translocated, and then placed back into the environment These demonstrated that the alteration observed in benthic communities associated with Cu contamination occurs during initial recolonization. After a 3-month exposure to sediments with varying Cu levels, two primary colonizing communities were identified: (1) a "mouth assemblage" resembling adjacent background fauna associated with low-Cu levels that was more diverse and predominantly dominated by surface- and subsurface-deposit feeders, burrowers, and tube builders, and (2) a "head assemblage" resembling adjacent background fauna associated with high-Cu concentrations, with few dominant species and an increasing importance of carnivores and mobile epifauna. Cu loading can cause reduced biodiversity and lower structural complexity that may last several months if high concentrations persist, with a direct effect on community functioning. (C) 2015 Elsevier Ltd. All rights reserved.

Mehring, AS, Levin LA.  2015.  Potential roles of soil fauna in improving the efficiency of rain gardens used as natural stormwater treatment systems. Journal of Applied Ecology. 52:1445-1454.   10.1111/1365-2664.12525   AbstractWebsite

Natural treatment systems such as rain gardens aim to overcome the negative effects of urbanization on water quality, availability, and freshwater and marine ecosystem integrity by mimicking the natural water cycle in urban planning and design. While soils in these systems are inhabited by a diverse array of invertebrates, the soil macrofauna is ignored in the vast majority of studies on new or existing rain gardens. Here, we review the functional roles of invertebrates commonly found within soils of rain gardens. Soil fauna have the potential to substantially alter plant growth, water infiltration rates, and the retention and removal of pathogens, nutrients, heavy metals and other contaminants. Their lack of inclusion in controlled laboratory or greenhouse studies may contribute to differences in observed function in field and laboratory settings. Promising future research directions include the following: (i) the use of controlled experiments to study invertebrate effects on rain garden function; (ii) determining the factors affecting variability in organismal abundance among and within sites; and (iii) the design of rain gardens to facilitate development of fauna that promote desired functions.Synthesis and applications. Soil fauna may substantially alter the function of rain gardens as natural stormwater treatment systems in urban areas. Therefore, incorporat-ing animal effects into design and testing may better enable managers and researchers tounderstand and optimize rain garden functioning, and forecast the longevity of rain gardens. Soil fauna may substantially alter the function of rain gardens as natural stormwater treatment systems in urban areas. Therefore, incorporat-ing animal effects into design and testing may better enable managers and researchers tounderstand and optimize rain garden functioning, and forecast the longevity of rain gardens.

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.

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

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

Nordstrom, MC, Demopoulos AWJ, Whitcraft CR, Rismondo A, McMillan P, Gonzalez JP, Levin LA.  2015.  Food web heterogeneity and succession in created saltmarshes. Journal of Applied Ecology. 52:1343-1354.   10.1111/1365-2664.12473   AbstractWebsite

Ecological restoration must achieve functional as well as structural recovery. Functional metrics for re-establishment of trophic interactions can be used to complement traditional monitoring of structural attributes. In addition, topographic effects on food web structure provide added information within a restoration context; often, created sites may require spatial heterogeneity to effectively match structure and function of natural habitats. We addressed both of these issues in our study of successional development of benthic food web structure, with focus on bottom-up-driven changes in macroinvertebrate consumer assemblages in the saltmarshes of the Venice Lagoon, Italy. We combined quantified estimates of the changing community composition with stable isotope data (C-13:C-12 and N-15:N-14) to compare the general trophic structure between created (2-14years) marshes and reference sites and along topographic elevation gradients within saltmarshes. Macrofaunal invertebrate consumers exhibited local, habitat-specific trophic patterns. Stable isotope-based trophic structure changed with increasing marsh age, in particular with regard to mid-elevation (Salicornia) habitats. In young marshes, the mid-elevation consumer signatures resembled those of unvegetated ponds. The mid-elevation of older and natural marshes had a more distinct Salicornia zone food web, occasionally resembling that of the highest (Sarcocornia-dominated) elevation. In summary, this indicates that primary producers and availability of vascular plant detritus structure consumer trophic interactions and the flow of carbon. Functionally different consumers, subsurface-feeding detritivores (Oligochaeta) and surface grazers (Hydrobia sp.), showed distinct but converging trajectories of isotopic change over time, indicating that successional development may be asymmetric between brown' (detrital) guilds and green' (grazing) guilds in the food web.Synthesis and applications. Created marsh food webs converged into a natural state over about a decade, with successional shifts seen in both consumer community composition and stable isotope space. Strong spatial effects were noted, highlighting the utility of stable isotopes to evaluate functional equivalence in spatially heterogeneous systems. Understanding the recovery of functional properties such as food web support, and their inherent spatial variability, is key to planning and managing successful habitat restoration. Created marsh food webs converged into a natural state over about a decade, with successional shifts seen in both consumer community composition and stable isotope space. Strong spatial effects were noted, highlighting the utility of stable isotopes to evaluate functional equivalence in spatially heterogeneous systems. Understanding the recovery of functional properties such as food web support, and their inherent spatial variability, is key to planning and managing successful habitat restoration.

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.

Raman, AV, Damodaran R, Levin LA, Ganesh T, Rao YKV, Nanduri S, Madhusoodhanan R.  2015.  Macrobenthos relative to the oxygen minimum zone on the East Indian margin, Bay of Bengal. Marine Ecology-an Evolutionary Perspective. 36:679-700.   10.1111/maec.12176   AbstractWebsite

The Bay of Bengal remains one of the least studied of the world's oxygen minimum zones (OMZs). Here we offer a detailed investigation of the macrobenthos relative to oxygen minimum zone [OMZ - DO (dissolved oxygen), concentration <0.5ml1(-1)] at 110 stations off the North East Indian margin (16(0) and 20(0)N) featuring coastal, shelf and slope settings (10-1004m). Macrobenthos (>0.5mm) composition, abundance and diversity were studied in relation to variations in depth, dissolved oxygen, sediment texture and organic carbon. Using multivariate procedures powered by SIMPROF analysis we identified distinct OMZ core sites (depth 150-280m; DO 0.37ml1(-1)) that exhibited dense populations of surface-feeding polychaetes (mean 2188 ind. m(-2)) represented by spionids and cossurids (96%). Molluscs and crustaceans were poorly represented except for ampeliscid amphipods. The lower OMZ sites (DO>0.55mll(-1)) supported a different assemblage of polychaetes (cirratulids, amphinomids, eunicids, orbinids, paraonids), crustaceans and molluscs, albeit with low population densities (mean 343 ind. m(-2)). Species richness [E(S-100)], diversity (Margalef d; H') and evenness (J') were lower and dominance was higher within the OMZ core region. Multiple regression analysis showed that a combination of sand, clay, organic carbon, and dissolved oxygen explained 62-78% of the observed variance in macrobenthos species richness and diversity: E(S-100) and H'. For polychaetes, clay and oxygen proved important. At low oxygen sites (DO <1mll(-1)), depth accounted for most variance. Residual analysis (after removing depth effects) revealed that dissolved oxygen and sediment organic matter influenced 50-62% of residual variation in E(S-100), H' and d for total macrofauna. Of this, oxygen alone influenced up to similar to 50-62%. When only polychaetes were evaluated, oxygen and organic matter explained up to 58-63%. For low oxygen sites, organic matter alone had the explanatory power when dominance among polychaetes was considered. Overall, macrobenthic patterns in the Bay of Bengal were consistent with those reported for other upwelling margins. However, the compression of faunal gradients at shallower depths was most similar to the Chile/Peru margin, and different from the Arabian Sea, where the depth range of the OMZ is two times greater. The Bay of Bengal patterns may take on added significance as OMZs shoal globally.

Grupe, BM, Krach ML, Pasulka AL, Maloney JM, Levin LA, Frieder CA.  2015.  Methane seep ecosystem functions and services from a recently discovered southern California seep. Marine Ecology-an Evolutionary Perspective. 36:91-108.   10.1111/maec.12243   AbstractWebsite

The recent discovery of a methane seep with diverse microhabitats and abundant groundfish in the San Diego Trough (1020 m) off the coast of Del Mar, California raised questions about the role of seep ecosystem functions and services in relation to continental margins. We used multicorer and ROV grab samples and an ROV survey to characterize macrofaunal structure, diversity, and trophic patterns in soft sediments and authigenic carbonates; seep microhabitats and taxa observed; and the abundance and spatial patterns of fishery-relevant species. Biogenic microhabitats near the Del Mar Seep included microbially precipitated carbonate boulders, bacterial mats, vesicomyid clam beds, frenulate and ampharetid beds, vestimentiferan tubeworm clumps, and fields of Bathysiphon filiformis tubes. Macrofaunal abundance increased and mean faunal delta C-13 signatures decreased in multicorer samples nearer the seep, suggesting that chemosynthetic production enhanced animal densities outside the seep center. Polychaetes dominated sediments, and ampharetids became especially abundant near microbial mats, while gastropods, hydroids, and sponges dominated carbonate rocks. A wide range of stable isotopic signatures reflected the diversity of microhabitats, and methane-derived carbon was the most prevalent source of nutrition for several taxa, especially those associated with carbonates. Megafaunal species living near the seep included longspine thornyhead (Sebastolobus altivelis), Pacific dover sole (Microstomus pacificus), and lithodid crabs (Paralomis verrilli), which represent targets for demersal fisheries. Sebastolobus altivelis was especially abundant (6.5-8.2 fish.100 m(-2)) and appeared to aggregate near the most active seep microhabitats. The Del Mar Methane Seep, like many others along the world's continental margins, exhibits diverse ecosystem functions and enhances regional diversity. Seeps such as this one may also contribute ecosystem services if they provide habitat for fishery species, export production to support margin food webs, and serve as sinks for methane-derived carbon.

Ramirez-Llodra, E, Trannum HC, Evenset A, Levin LA, Andersson M, Finne TE, Hilario A, Flem B, Christensen G, Schaanning M, Vanreusel A.  2015.  Submarine and deep-sea mine tailing placements: A review of current practices, environmental issues, natural analogs and knowledge gaps in Norway and internationally. Marine Pollution Bulletin. 97:13-35.   10.1016/j.marpolbul.2015.05.062   AbstractWebsite

The mining sector is growing in parallel with societal demands for minerals. One of the most important environmental issues and economic burdens of industrial mining on land is the safe storage of the vast amounts of waste produced. Traditionally, tailings have been stored in land dams, but the lack of land availability, potential risk of dam failure and topography in coastal areas in certain countries results in increasing disposal of tailings into marine systems. This review describes the different submarine tailing disposal methods used in the world in general and in Norway in particular, their impact on the environment (e.g. hyper-sedimentation, toxicity, processes related to changes in grain shape and size, turbidity), current legislation and need for future research. Understanding these impacts on the habitat and biota is essential to assess potential ecosystem changes and to develop best available techniques and robust management plans. (C) 2015 Elsevier Ltd. All rights reserved.

Levin, LA, Mendoza GF, Grupe BM, Gonzalez JP, Jellison B, Rouse G, Thurber AR, Waren A.  2015.  Biodiversity on the rocks: Macrofauna inhabiting authigenic carbonate at Costa Rica methane seeps. PLoS ONE. 10:e0131080.: Public Library of Science   10.1371/journal.pone.0131080   Abstract

The activity of anaerobic methane oxidizing microbes facilitates precipitation of vast quantities of authigenic carbonate at methane seeps. Here we demonstrate the significant role of carbonate rocks in promoting diversity by providing unique habitat and food resources for macrofaunal assemblages at seeps on the Costa Rica margin (400–1850 m). The attendant fauna is surprisingly similar to that in rocky intertidal shores, with numerous grazing gastropods (limpets and snails) as dominant taxa. However, the community feeds upon seep-associated microbes. Macrofaunal density, composition, and diversity on carbonates vary as a function of seepage activity, biogenic habitat and location.

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.

Levin, LA, Honisch B, Frieder CA.  2015.  Geochemical proxies for estimating faunal exposure to ocean acidification. Oceanography. 28:62-73.   10.5670/oceanog.2015.32   AbstractWebsite

Growing concern over the impacts of modern ocean acidification (OA) and interest in historical pH excursions have intensified the development of geochemical proxies for organism exposure to acidification and other components of the carbonate system. The use of carbonate structures produced by foraminifers, coccolithophores, corals, mollusks, brachiopods, echinoderms, ostracods, and fish for paleoreconstructions is an active area of study, and the resulting proxy development offers new opportunities for studying modern faunal exposures. Here we review information from field studies and laboratory experiments on carbonate system geochemical proxies in protists and metazoa. Geochemical proxy development for foraminifers and corals is most advanced; studies of fish and echinoderms are in their infancy. The most promising geochemical proxies are those with a mechanistic link to changes in seawater carbonate chemistry, such as boron isotopes (delta B-11), B/Ca, and U/Ca ratios recorded in skeletal hard parts. We also discuss indirect geochemical proxies (other trace elements and carbonate polymorphs) along with their potential uses and limitations due to modification by physiological processes, precipitation rate, and degree of calcification. Proxy measurements in modern skeletal structures, otoliths, statoliths, and other hard parts could reveal environmental exposures of organisms from larval through adult stages, and could advance inferences about effects of OA (and other stressors) on survival, growth, population connectivity, and other ecological attributes. Use of geochemical proxies in live, field-collected organisms is an underutilized and underdeveloped approach to studying OA consequences, but it may offer a powerful, complementary approach to laboratory observations.