Elevated CO2 impairs olfactory-mediated neural and behavioral responses and gene expression in ocean-phase coho salmon (Oncorhynchus kisutch).

Elevated concentrations of CO2 in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal streams. We investigated the effects of elevated seawater CO2 on coho salmon (Oncorhynchus kisutch) olfactory-mediated behavior, neural signaling, and gene expression within the peripheral and central olfactory system. Ocean-phase coho salmon were exposed to three levels of CO2 , ranging from those currently found in ambient marine water to projected future levels. Juvenile coho salmon exposed to elevated CO2 levels for 2 weeks no longer avoided a skin extract odor that elicited avoidance responses in coho salmon maintained in ambient CO2 seawater. Exposure to these elevated CO2 levels did not alter odor signaling in the olfactory epithelium, but did induce significant changes in signaling within the olfactory bulb. RNA-Seq analysis of olfactory tissues revealed extensive disruption in expression of genes involved in neuronal signaling within the olfactory bulb of salmon exposed to elevated CO2 , with lesser impacts on gene expression in the olfactory rosettes. The disruption in olfactory bulb gene pathways included genes associated with GABA signaling and maintenance of ion balance within bulbar neurons. Our results indicate that ocean-phase coho salmon exposed to elevated CO2 can experience significant behavioral impairments likely driven by alteration in higher-order neural signal processing within the olfactory bulb. Our study demonstrates that anadromous fish such as salmon may share a sensitivity to rising CO2 levels with obligate marine species suggesting a more wide-scale ecological impact of ocean acidification.

Risks of ocean acidification in the California Current food web and fisheries: ecosystem model projections.

The benefits and ecosystem services that humans derive from the oceans are threatened by numerous global change stressors, one of which is ocean acidification. Here, we describe the effects of ocean acidification on an upwelling system that already experiences inherently low pH conditions, the California Current. We used an end-to-end ecosystem model (Atlantis), forced by downscaled global climate models and informed by a meta-analysis of the pH sensitivities of local taxa, to investigate the direct and indirect effects of future pH on biomass and fisheries revenues. Our model projects a 0.2-unit drop in pH during the summer upwelling season from 2013 to 2063, which results in wide-ranging magnitudes of effects across guilds and functional groups. The most dramatic direct effects of future pH may be expected on epibenthic invertebrates (crabs, shrimps, benthic grazers, benthic detritivores, bivalves), and strong indirect effects expected on some demersal fish, sharks, and epibenthic invertebrates (Dungeness crab) because they consume species known to be sensitive to changing pH. The model's pelagic community, including marine mammals and seabirds, was much less influenced by future pH. Some functional groups were less affected to changing pH in the model than might be expected from experimental studies in the empirical literature due to high population productivity (e.g., copepods, pteropods). Model results suggest strong effects of reduced pH on nearshore state-managed invertebrate fisheries, but modest effects on the groundfish fishery because individual groundfish species exhibited diverse responses to changing pH. Our results provide a set of projections that generally support and build upon previous findings and set the stage for hypotheses to guide future modeling and experimental analysis on the effects of OA on marine ecosystems and fisheries.

Incorporating climate and ocean change into extinction risk assessments for 82 coral species.

Many marine invertebrate species facing potential extinction have uncertain taxonomies and poorly known demographic and ecological traits. Uncertainties are compounded when potential extinction drivers are climate and ocean changes whose effects on even widespread and abundant species are only partially understood. The U.S. Endangered Species Act mandates conservation management decisions founded on the extinction risk to species based on the best available science at the time of consideration-requiring prompt action rather than awaiting better information. We developed an expert-opinion threat-based approach that entails a structured voting system to assess extinction risk from climate and ocean changes and other threats to 82 coral species for which population status and threat response information was limited. Such methods are urgently needed because constrained budgets and manpower will continue to hinder the availability of desired data for many potentially vulnerable marine species. Significant species-specific information gaps and uncertainties precluded quantitative assessments of habitat loss or population declines and necessitated increased reliance on demographic characteristics and threat vulnerabilities at genus or family levels. Adapting some methods (e.g., a structured voting system) used during other assessments and developing some new approaches (e.g., integrated assessment of threats and demographic characteristics), we rated the importance of threats contributing to coral extinction risk and assessed those threats against population status and trend information to evaluate each species' extinction risk over the 21st century. This qualitative assessment resulted in a ranking with an uncertainty range for each species according to their estimated likelihood of extinction. We offer guidance on approaches for future biological extinction risk assessments, especially in cases of data-limited species likely to be affected by global-scale threats. Incorporación del Cambio Climático y Oceánico en Estudios de Riesgo de Extinción para 82 Especies de Coral.

Human influence on the spatial structure of threatened Pacific salmon metapopulations.

To remain viable, populations must be resilient to both natural and human-caused environmental changes. We evaluated anthropogenic effects on spatial connections among populations of Chinook salmon (Oncorhynchus tshawytscha) and steelhead (O. mykiss) (designated as threatened under the U.S. Endangered Species Act) in the lower Columbia and Willamette rivers. For several anthropogenic-effects scenarios, we used graph theory to characterize the spatial relation among populations. We plotted variance in population size against connectivity among populations. In our scenarios, reduced habitat quality decreased the size of populations and hydropower dams on rivers led to the extirpation of several populations, both of which decreased connectivity. Operation of fish hatcheries increased connectivity among populations and led to patchy or panmictic populations. On the basis of our results, we believe recolonization of the upper Cowlitz River by fall and spring Chinook and winter steelhead would best restore metapopulation structure to near-historical conditions. Extant populations that would best conserve connectivity would be those inhabiting the Molalla (spring Chinook), lower Cowlitz, or Clackamas (fall Chinook) rivers and the south Santiam (winter steelhead) and north fork Lewis rivers (summer steelhead). Populations in these rivers were putative sources; however, they were not always the most abundant or centrally located populations. This result would not have been obvious if we had not considered relations among populations in a metapopulation context. Our results suggest that dispersal rate strongly controls interactions among the populations that comprise salmon metapopulations. Thus, monitoring efforts could lead to understanding of the true rates at which wild and hatchery fish disperse. Our application of graph theory allowed us to visualize how metapopulation structure might respond to human activity. The method could be easily extended to evaluations of anthropogenic effects on other stream-dwelling populations and communities and could help prioritize among competing conservation measures.

Dealing with uncertainty in ecosystem models: lessons from a complex salmon model.

Ecosystem models have been developed for assessment and management in a wide variety of environments. As model complexity increases, it becomes more difficult to trace how imperfect knowledge of internal model parameters, data inputs, or relationships among parameters might impact model results, affecting predictions and subsequent management decisions. Sensitivity analysis is an essential component of model evaluation, particularly when models are used to make management decisions. Results should be expressed as probabilities and should realistically account for uncertainty. When models are particularly complex, this can be difficult to do and to present in ways that do not obfuscate essential results. We conducted a sensitivity analysis of the Ecosystem Diagnosis and Treatment (EDT) model, which predicts salmon productivity and capacity as a function of ecosystem conditions. We used a novel "structured sensitivity analysis" approach that is particularly useful for very complex models or those with an abundance of interconnected parameters. We identified small, medium, and large plausible ranges for both input data and model parameters. Using a Monte Carlo approach, we explored the variation in output, prediction intervals, and sensitivity indices, given these plausible input distributions. The analyses indicated that, as a consequence of internal parameter uncertainty, EDT productivity and capacity predictions lack the precision needed for many management applications. However, EDT prioritization of reaches for preservation or restoration was more robust to given input uncertainties, indicating that EDT may be more useful as a relative measure of fish performance than as an absolute measure. Like all large models, if EDT output is to be used as input to other models or management tools it is important to explicitly incorporate the uncertainty and sensitivity analyses into such secondary analyses. Sensitivity analyses should become standard operating procedure for evaluation of ecosystem models.

Uncovering mechanisms of global ocean change effects on the Dungeness crab (Cancer magister) through metabolomics analysis.

The Dungeness crab is an economically and ecologically important species distributed along the North American Pacific coast. To predict how Dungeness crab may physiologically respond to future global ocean change on a molecular level, we performed untargeted metabolomic approaches on individual Dungeness crab juveniles reared in treatments that mimicked current and projected future pH and dissolved oxygen conditions. We found 94 metabolites and 127 lipids responded in a condition-specific manner, with a greater number of known compounds more strongly responding to low oxygen than low pH exposure. Pathway analysis of these compounds revealed that juveniles may respond to low oxygen through evolutionarily conserved processes including downregulating glutathione biosynthesis and upregulating glycogen storage, and may respond to low pH by increasing ATP production. Most interestingly, we found that the response of juveniles to combined low pH and low oxygen exposure was most similar to the low oxygen exposure response, indicating low oxygen may drive the physiology of juvenile crabs more than pH. Our study elucidates metabolic dynamics that expand our overall understanding of how the species might respond to future ocean conditions and provides a comprehensive dataset that could be used in future ocean acidification response studies.

Estimates of the Direct Effect of Seawater pH on the Survival Rate of Species Groups in the California Current Ecosystem.

Ocean acidification (OA) has the potential to restructure ecosystems due to variation in species sensitivity to the projected changes in ocean carbon chemistry. Ecological models can be forced with scenarios of OA to help scientists, managers, and other stakeholders understand how ecosystems might change. We present a novel methodology for developing estimates of species sensitivity to OA that are regionally specific, and applied the method to the California Current ecosystem. To do so, we built a database of all published literature on the sensitivity of temperate species to decreased pH. This database contains 393 papers on 285 species and 89 multi-species groups from temperate waters around the world. Research on urchins and oysters and on adult life stages dominates the literature. Almost a third of the temperate species studied to date occur in the California Current. However, most laboratory experiments use control pH conditions that are too high to represent average current chemistry conditions in the portion of the California Current water column where the majority of the species live. We developed estimates of sensitivity to OA for functional groups in the ecosystem, which can represent single species or taxonomically diverse groups of hundreds of species. We based these estimates on the amount of available evidence derived from published studies on species sensitivity, how well this evidence could inform species sensitivity in the California Current ecosystem, and the agreement of the available evidence for a species/species group. This approach is similar to that taken by the Intergovernmental Panel on Climate Change to characterize certainty when summarizing scientific findings. Most functional groups (26 of 34) responded negatively to OA conditions, but when uncertainty in sensitivity was considered, only 11 groups had relationships that were consistently negative. Thus, incorporating certainty about the sensitivity of species and functional groups to OA is an important part of developing robust scenarios for ecosystem projections.

Shell condition and survival of Puget Sound pteropods are impaired by ocean acidification conditions.

We tested whether the thecosome pteropod Limacina helicina from Puget Sound, an urbanized estuary in the northwest continental US, experiences shell dissolution and altered mortality rates when exposed to the high CO2, low aragonite saturation state (Ωa) conditions that occur in Puget Sound and the northeast Pacific Ocean. Five, week-long experiments were conducted in which we incubated pteropods collected from Puget Sound in four carbon chemistry conditions: current summer surface (∼460-500 µatm CO2, Ωa≈1.59), current deep water or surface conditions during upwelling (∼760 and ∼1600-1700 µatm CO2, Ωa≈1.17 and 0.56), and future deep water or surface conditions during upwelling (∼2800-3400 µatm CO2, Ωa≈0.28). We measured shell condition using a scoring regime of five shell characteristics that capture different aspects of shell dissolution. We characterized carbon chemistry conditions in statistical analyses with Ωa, and conducted analyses considering Ωa both as a continuous dataset and as discrete treatments. Shell dissolution increased linearly as aragonite saturation state decreased. Discrete treatment comparisons indicate that shell dissolution was greater in undersaturated treatments compared to oversaturated treatments. Survival increased linearly with aragonite saturation state, though discrete treatment comparisons indicated that survival was similar in all but the lowest saturation state treatment. These results indicate that, under starvation conditions, pteropod survival may not be greatly affected by current and expected near-future aragonite saturation state in the NE Pacific, but shell dissolution may. Given that subsurface waters in Puget Sound's main basin are undersaturated with respect to aragonite in the winter and can be undersaturated in the summer, the condition and persistence of the species in this estuary warrants further study.

Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: implications for the design of ocean acidification experiments.

Carbonate chemistry variability is often poorly characterized in coastal regions and patterns of covariation with other biologically important variables such as temperature, oxygen concentration, and salinity are rarely evaluated. This absence of information hampers the design and interpretation of ocean acidification experiments that aim to characterize biological responses to future pCO2 levels relative to contemporary conditions. Here, we analyzed a large carbonate chemistry data set from Puget Sound, a fjord estuary on the U.S. west coast, and included measurements from three seasons (winter, summer, and fall). pCO2 exceeded the 2008-2011 mean atmospheric level (392 µatm) at all depths and seasons sampled except for the near-surface waters (< 10 m) in the summer. Further, undersaturated conditions with respect to the biogenic carbonate mineral aragonite were widespread (Ωar<1). We show that pCO2 values were relatively uniform throughout the water column and across regions in winter, enriched in subsurface waters in summer, and in the fall some values exceeded 2500 µatm in near-surface waters. Carbonate chemistry covaried to differing levels with temperature and oxygen depending primarily on season and secondarily on region. Salinity, which varied little (27 to 31), was weakly correlated with carbonate chemistry. We illustrate potential high-frequency changes in carbonate chemistry, temperature, and oxygen conditions experienced simultaneously by organisms in Puget Sound that undergo diel vertical migrations under present-day conditions. We used simple calculations to estimate future pCO2 and Ωar values experienced by diel vertical migrators based on an increase in atmospheric CO2. Given the potential for non-linear interactions between pCO2 and other abiotic variables on physiological and ecological processes, our results provide a basis for identifying control conditions in ocean acidification experiments for this region, but also highlight the wide range of carbonate chemistry conditions organisms may currently experience in this and similar coastal ecosystems.