Publications

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

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

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

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

2017
Sweetman, AK, Thurber AR, Smith CR, Levin LA, Mora C, Wei CL, Gooday AJ, Jones DOB, Rex M, Yasuhara M, Ingels J, Ruhl HA, Frieder CA, Danovaro R, Wurzberg L, Baco A, Grupe BM, Pasulka A, Meyer KS, Dunlop KM, Henry LA, Roberts JM.  2017.  Major impacts of climate change on deep-sea benthic ecosystems. Elementa-Science of the Anthropocene. 5:1-23.   10.1525/elementa.203   AbstractWebsite

The deep sea encompasses the largest ecosystems on Earth. Although poorly known, deep seafloor ecosystems provide services that are vitally important to the entire ocean and biosphere. Rising atmospheric greenhouse gases are bringing about significant changes in the environmental properties of the ocean realm in terms of water column oxygenation, temperature, pH and food supply, with concomitant impacts on deep-sea ecosystems. Projections suggest that abyssal (3000-6000 m) ocean temperatures could increase by 1 degrees C over the next 84 years, while abyssal seafloor habitats under areas of deep-water formation may experience reductions in water column oxygen concentrations by as much as 0.03 mL L-1 by 2100. Bathyal depths (200-3000 m) worldwide will undergo the most significant reductions in pH in all oceans by the year 2100 (0.29 to 0.37 pH units). O-2 concentrations will also decline in the bathyal NE Pacific and Southern Oceans, with losses up to 3.7% or more, especially at intermediate depths. Another important environmental parameter, the flux of particulate organic matter to the seafloor, is likely to decline significantly in most oceans, most notably in the abyssal and bathyal Indian Ocean where it is predicted to decrease by 40-55% by the end of the century. Unfortunately, how these major changes will affect deep-seafloor ecosystems is, in some cases, very poorly understood. In this paper, we provide a detailed overview of the impacts of these changing environmental parameters on deep-seafloor ecosystems that will most likely be seen by 2100 in continental margin, abyssal and polar settings. We also consider how these changes may combine with other anthropogenic stressors (e.g., fishing, mineral mining, oil and gas extraction) to further impact deep-seafloor ecosystems and discuss the possible societal implications.

2015
Levin, LA, Liu KK, Emeis KC, Breitburg DL, Cloern J, Deutsch C, Giani M, Goffart A, Hofmann EE, Lachkar Z, Limburg K, Liu SM, Montes E, Naqvi W, Ragueneau O, Rabouille C, Sarkar SK, Swaney DP, Wassman P, Wishner KF.  2015.  Comparative biogeochemistry-ecosystem-human interactions on dynamic continental margins. Journal of Marine Systems. 141:3-17.   10.1016/j.jmarsys.2014.04.016   AbstractWebsite

The oceans' continental margins face strong and rapid change, forced by a combination of direct human activity, anthropogenic CO2-induced climate change, and natural variability. Stimulated by discussions in Goa, India at the IMBER IMBIZO III, we (1) provide an overview of the drivers of biogeochemical variation and change on margins, (2) compare temporal trends in hydrographic and biogeochemical data across different margins, (3) review ecosystem responses to these changes, (4) highlight the importance of margin time series for detecting and attributing change and (5) examine societal responses to changing margin biogeochemistry and ecosystems. We synthesize information over a wide range of margin settings in order to identify the commonalities and distinctions among continental margin ecosystems. Key drivers of biogeochemical variation include long-term climate cycles, CO2-induced warming, acidification, and deoxygenation, as well as sea level rise, eutrophication, hydrologic and water cycle alteration, changing land use, fishing, and species invasion. Ecosystem responses are complex and impact major margin services. These include primary production, fisheries production, nutrient cycling, shoreline protection, chemical buffering, and biodiversity. Despite regional differences, the societal consequences of these changes are unarguably large and mandate coherent actions to reduce, mitigate and adapt to multiple stressors on continental margins. (C) 2014 Elsevier BM. All rights reserved.

2014
Navarro, MO, Bockmon EE, Frieder CA, Gonzalez JP, Levin LA.  2014.  Environmental pH, O-2 and capsular effects on the geochemical composition of statoliths of embryonic squid Doryteuthis opalescens. Water. 6:2233-2254.   10.3390/w6082233   AbstractWebsite

Spawning market squid lay embryo capsules on the seafloor of the continental shelf of the California Current System (CCS), where ocean acidification, deoxygenation and intensified upwelling lower the pH and [O-2]. Squid statolith geochemistry has been shown to reflect the squid's environment (e. g., seawater temperature and elemental concentration). We used real-world environmental levels of pH and [O-2] observed on squid-embryo beds to test in the laboratory whether or not squid statolith geochemistry reflects environmental pH and [O-2]. We asked whether pH and [O-2] levels might affect the incorporation of element ratios (B:Ca, Mg:Ca, Sr:Ca, Ba:Ca, Pb:Ca, U:Ca) into squid embryonic statoliths as (1) individual elements and/or (2) multivariate elemental signatures, and consider future applications as proxies for pH and [O-2] exposure. Embryo exposure to high and low pH and [O-2] alone and together during development over four weeks only moderately affected elemental concentrations of the statoliths, and uranium was an important element driving these differences. Uranium: Ca was eight-times higher in statoliths exposed to low pHT (7.57-7.58) and low [O-2] (79-82 mu mol.kg(-1)) than those exposed to higher ambient pHT (7.92-7.94) and [O-2] (241-243 mu mol.kg(-1)). In a separate experiment, exposure to low pHT (7.55-7.56) or low [O-2] (83-86 mu mol.kg(-1)) yielded elevated U:Ca and Sr:Ca in the low [O-2] treatment only. We found capsular effects on multiple elements in statoliths of all treatments. The multivariate elemental signatures of embryonic statoliths were distinct among capsules, but did not reflect environmental factors (pH and/or [O-2]). We show that statoliths of squid embryos developing inside capsules have the potential to reflect environmental pH and [O-2], but that these "signals" are generated in concert with the physiological effects of the capsules and embryos themselves.

2012
Levin, LA, Sibuet M.  2012.  Understanding Continental Margin Biodiversity: A New Imperative. Annual Review of Marine Science, Vol 4. 4( Carlson CA, Giovannoni SJ, Eds.).:79-+., Palo Alto: Annual Reviews   10.1146/annurev-marine-120709-142714   Abstract

Until recently, the deep continental margins (200-4,000 m) were perceived as monotonous mud slopes of limited ecological or environmental concern. Progress in seafloor mapping and direct observation now reveals unexpected heterogeneity, with a mosaic of habitats and ecosystems linked to geomorphological, geochemical, and hydrographic features that influence biotic diversity. Interactions among water masses, terrestrial inputs, sediment diagenesis, and tectonic activity create a multitude of ecological settings supporting distinct communities that populate canyons and seamounts, high-stress oxygen minimum zones, and methane seeps, as well as vast reefs of cold corals and sponges. This high regional biodiversity is fundamental to the production of valuable fisheries, energy, and mineral resources, and performs critical ecological services (nutrient cycling, carbon sequestration, nursery and habitat support). It is under significant threat from climate change and human resource extraction activities. Serious actions are required to preserve the functions and services provided by the deep-sea settings we are just now getting to know.

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

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