Publications

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2018
Sato, KN, Andersson AJ, Day JMD, Taylor JRA, Frank MB, Jung JY, McKittrick J, Levin LA.  2018.  Response of sea urchin fitness traits to environmental gradients across the Southern California oxygen minimum zone. Frontiers in Marine Science. 5   10.3389/fmars.2018.00258   AbstractWebsite

Marine calcifiers are considered to be among the most vulnerable taxa to climate-forced environmental changes occurring on continental margins with effects hypothesized to occur on microstructural, biomechanical, and geochemical properties of carbonate structures. Natural gradients in temperature, salinity, oxygen, and pH on an upwelling margin combined with the broad depth distribution (100-1,100 m) of the pink fragile sea urchin, Strongylocentrotus (formerly Allocentrotus) fragilis, along the southern California shelf and slope provide an ideal system to evaluate potential effects of multiple climate variables on carbonate structures in situ. We measured, for the first time, trait variability across four distinct depth zones using natural gradients as analogues for species-specific implications of oxygen minimum zone (OMZ) expansion, deoxygenation and ocean acidification. Although S. fragilis may likely be tolerant of future oxygen and pH decreases predicted during the twenty-first century, we determine from adults collected across multiple depth zones that urchin size and potential reproductive fitness (gonad index) are drastically reduced in the OMZ core (450-900 m) compared to adjacent zones. Increases in porosity and mean pore size coupled with decreases in mechanical nanohardness and stiffness of the calcitic endoskeleton in individuals collected from lower pH(Total) (7.57-7.59) and lower dissolved oxygen (13-42 mu mol kg(-1)) environments suggest that S. fragilis may be potentially vulnerable to crushing predators if these conditions become more widespread in the future. In addition, elemental composition indicates that S. fragilis has a skeleton composed of the low Mg-calcite mineral phase of calcium carbonate (mean Mg/Ca = 0.02 mol mol(-1)), with Mg/Ca values measured in the lower end of values reported for sea urchins known to date. Together these findings suggest that ongoing declines in oxygen and pH will likely affect the ecology and fitness of a dominant echinoid on the California margin.

2017
McCormick, LR, Levin LA.  2017.  Physiological and ecological implications of ocean deoxygenation for vision in marine organisms. Philosophical Transactions of the Royal Society a-Mathematical Physical and Engineering Sciences. 375   10.1098/rsta.2016.0322   AbstractWebsite

Climate change has induced ocean deoxygenation and exacerbated eutrophication-driven hypoxia in recent decades, affecting the physiology, behaviour and ecology of marine organisms. The high oxygen demand of visual tissues and the known inhibitory effects of hypoxia on human vision raise the questions if and how ocean deoxygenation alters vision in marine organisms. This is particularly important given the rapid loss of oxygen and strong vertical gradients in oxygen concentration in many areas of the ocean. This review evaluates the potential effects of low oxygen (hypoxia) on visual function in marine animals and their implications for marine biota under current and future ocean deoxygenation based on evidence from terrestrial and a few marine organisms. Evolutionary history shows radiation of eye designs during a period of increasing ocean oxygenation. Physiological effects of hypoxia on photoreceptor function and light sensitivity, in combination with morphological changes that may occur throughout ontogeny, have the potential to alter visual behaviour and, subsequently, the ecology of marine organisms, particularly for fish, cephalopods and arthropods with `fast' vision. Visual responses to hypoxia, including greater light requirements, offer an alternative hypothesis for observed habitat compression and shoaling vertical distributions in visual marine species subject to ocean deoxygenation, which merits further investigation. This article is part of the themed issue 'Ocean ventilation and deoxygenation in a warming world'.

2016
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.

2015
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.

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, 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.

2011
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.

Ramirez-Llodra, E, Tyler PA, Baker MC, Bergstad OA, Clark MR, Escobar E, Levin LA, Menot L, Rowden AA, Smith CR, Vandover CL.  2011.  Man and the last great wilderness: human impact on the deep sea. Plos One. 6   10.1371/journal.pone.0022588   AbstractWebsite

The deep sea, the largest ecosystem on Earth and one of the least studied, harbours high biodiversity and provides a wealth of resources. Although humans have used the oceans for millennia, technological developments now allow exploitation of fisheries resources, hydrocarbons and minerals below 2000 m depth. The remoteness of the deep seafloor has promoted the disposal of residues and litter. Ocean acidification and climate change now bring a new dimension of global effects. Thus the challenges facing the deep sea are large and accelerating, providing a new imperative for the science community, industry and national and international organizations to work together to develop successful exploitation management and conservation of the deep-sea ecosystem. This paper provides scientific expert judgement and a semi-quantitative analysis of past, present and future impacts of human-related activities on global deep-sea habitats within three categories: disposal, exploitation and climate change. The analysis is the result of a Census of Marine Life - SYNDEEP workshop (September 2008). A detailed review of known impacts and their effects is provided. The analysis shows how, in recent decades, the most significant anthropogenic activities that affect the deep sea have evolved from mainly disposal (past) to exploitation (present). We predict that from now and into the future, increases in atmospheric CO(2) and facets and consequences of climate change will have the most impact on deep-sea habitats and their fauna. Synergies between different anthropogenic pressures and associated effects are discussed, indicating that most synergies are related to increased atmospheric CO(2) and climate change effects. We identify deep-sea ecosystems we believe are at higher risk from human impacts in the near future: benthic communities on sedimentary upper slopes, cold-water corals, canyon benthic communities and seamount pelagic and benthic communities. We finalise this review with a short discussion on protection and management methods.

2010
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

2009
Levin, LA, Dayton PK.  2009.  Ecological theory and continental margins: where shallow meets deep. Trends in Ecology & Evolution. 24:606-617.   10.1016/j.tree.2009.04.012   AbstractWebsite

Continental margins, where land becomes ocean and plunges to the deep sea, provide valuable food and energy resources, and perform essential functions such as carbon burial and nutrient cycling. They exhibit remarkably high species and habitat diversity, but this is threatened by our increasing reliance on the resources that margins provide, and by warming, expanding hypoxia and acidification associated with climate change. Continental margin ecosystems, with environments, constituents and processes that differ from those in shallow water, demand a new focus, in which ecological theory and experimental methods are brought to bear on management and conservation practices. Concepts of disturbance, diversity-function relationships, top-down versus bottom-up control, facilitation and meta-dynamics offer a framework for studying fundamental processes and understanding future change.