Smaller body size under warming is not due to gill-oxygen limitation in a cold-water salmonid.

Declining body size in fishes and other aquatic ectotherms associated with anthropogenic climate warming has significant implications for future fisheries yields, stock assessments and aquatic ecosystem stability. One proposed mechanism seeking to explain such body-size reductions, known as the gill oxygen limitation (GOL) hypothesis, has recently been used to model future impacts of climate warming on fisheries but has not been robustly empirically tested. We used brook trout (Salvelinus fontinalis), a fast-growing, cold-water salmonid species of broad economic, conservation and ecological value, to examine the GOL hypothesis in a long-term experiment quantifying effects of temperature on growth, resting metabolic rate (RMR), maximum metabolic rate (MMR) and gill surface area (GSA). Despite significantly reduced growth and body size at an elevated temperature, allometric slopes of GSA were not significantly different than 1.0 and were above those for RMR and MMR at both temperature treatments (15°C and 20°C), contrary to GOL expectations. We also found that the effect of temperature on RMR was time-dependent, contradicting the prediction that heightened temperatures increase metabolic rates and reinforcing the importance of longer-term exposures (e.g. >6 months) to fully understand the influence of acclimation on temperature-metabolic rate relationships. Our results indicate that although oxygen limitation may be important in some aspects of temperature-body size relationships and constraints on metabolic supply may contribute to reduced growth in some cases, it is unlikely that GOL is a universal mechanism explaining temperature-body size relationships in aquatic ectotherms. We suggest future research focus on alternative mechanisms underlying temperature-body size relationships, and that projections of climate change impacts on fisheries yields using models based on GOL assumptions be interpreted with caution.

Environment and phenology shape local adaptation in thermal performance.

Populations within species often exhibit variation in traits that reflect local adaptation and further shape existing adaptive potential for species to respond to climate change. However, our mechanistic understanding of how the environment shapes trait variation remains poor. Here, we used common garden experiments to quantify thermal performance in eight populations of the marine snail Urosalpinx cinerea across thermal gradients on the Atlantic and the Pacific coasts of North America. We then evaluated the relationship between thermal performance and environmental metrics derived from time-series data. Our results reveal a novel pattern of 'mixed' trait performance adaptation, where thermal optima were positively correlated with spawning temperature (cogradient variation), while maximum trait performance was negatively correlated with season length (countergradient variation). This counterintuitive pattern probably arises because of phenological shifts in the spawning season, whereby 'cold' populations delay spawning until later in the year when temperatures are warmer compared to 'warm' populations that spawn earlier in the year when temperatures are cooler. Our results show that variation in thermal performance can be shaped by multiple facets of the environment and are linked to organismal phenology and natural history. Understanding the impacts of climate change on organisms, therefore, requires the knowledge of how climate change will alter different aspects of the thermal environment.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Timing of stressors alters interactive effects on a coastal foundation species.

The effects of climate-driven stressors on organismal performance and ecosystem functioning have been investigated across many systems; however, manipulative experiments generally apply stressors as constant and simultaneous treatments, rather than accurately reflecting temporal patterns in the natural environment. Here, we assessed the effects of temporal patterns of high aerial temperature and low salinity on survival of Olympia oysters (Ostrea lurida), a foundation species of conservation and restoration concern. As single stressors, low salinity (5 and 10 psu) and the highest air temperature (40°C) resulted in oyster mortality of 55.8, 11.3, and 23.5%, respectively. When applied on the same day, low salinity and high air temperature had synergistic negative effects that increased oyster mortality. This was true even for stressor levels that were relatively mild when applied alone (10 psu and 35°C). However, recovery times of two or four weeks between stressors eliminated the synergistic effects. Given that most natural systems threatened by climate change are subject to multiple stressors that vary in the timing of their occurrence, our results suggest that it is important to examine temporal variation of stressors in order to more accurately understand the possible biological responses to global change.

Atmospheric rivers and the mass mortality of wild oysters: insight into an extreme future?

Climate change is predicted to increase the frequency and severity of extreme events. However, the biological consequences of extremes remain poorly resolved owing to their unpredictable nature and difficulty in quantifying their mechanisms and impacts. One key feature delivering precipitation extremes is an atmospheric river (AR), a long and narrow filament of enhanced water vapour transport. Despite recent attention, the biological impacts of ARs remain undocumented. Here, we use biological data coupled with remotely sensed and in situ environmental data to describe the role of ARs in the near 100% mass mortality of wild oysters in northern San Francisco Bay. In March 2011, a series of ARs made landfall within California, contributing an estimated 69.3% of the precipitation within the watershed and driving an extreme freshwater discharge into San Francisco Bay. This discharge caused sustained low salinities (less than 6.3) that almost perfectly matched the known oyster critical salinity tolerance and was coincident with a mass mortality of one of the most abundant populations throughout this species' range. This is a concern, because wild oysters remain a fraction of their historical abundance and have yet to recover. This study highlights a novel mechanism by which precipitation extremes may affect natural systems and the persistence of sensitive species in the face of environmental change.

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework.

Despite the abundance of literature on organismal responses to multiple environmental stressors, most studies have not matched the timing of experimental manipulations with the temporal pattern of stressors in nature. We test the interactive effects of diel-cycling hypoxia with both warming and decreased salinities using ecologically realistic exposures. Surprisingly, we found no evidence of negative synergistic effects on Olympia oyster growth; rather, we found only additive and opposing effects of hypoxia (detrimental) and warming (beneficial). We suspect that diel-cycling provided a temporal refuge that allowed physiological compensation. We also tested for latent effects of warming and hypoxia to low-salinity tolerance using a seasonal delay between stressor events. However, we did not find a latent effect, rather a threshold survival response to low salinity that was independent of early life-history exposure to warming or hypoxia. The absence of synergism is likely the result of stressor treatments that mirror the natural timing of environmental stressors. We provide environmental context for laboratory experimental data by examining field time series environmental data from four North American west coast estuaries and find heterogeneous environmental signals that characterize each estuary, suggesting that the potential stressor exposure to oysters will drastically differ over moderate spatial scales. This heterogeneity implies that efforts to conserve and restore oysters will require an adaptive approach that incorporates knowledge of local conditions. We conclude that studies of multiple environmental stressors can be greatly improved by integrating ecologically realistic exposure and timing of stressors found in nature with organismal life-history traits.

Biotic resistance in marine environments.

Biological invasions depend in part on the resistance of native communities. Meta-analyses of terrestrial experiments demonstrate that native primary producers and herbivores generally resist invasions of primary producers, and that resistance through competition strengthens with native producer diversity. To test the generality of these findings, we conducted a meta-analysis of marine experiments. We found that native marine producers generally failed to resist producer invasions through competition unless the native community was diverse, and this diversity effect was weaker in marine than in terrestrial systems. In contrast, native consumers equally resisted invasive producers in both ecosystems. Most marine experiments, however, tested invasive consumers and these invasions were resisted more strongly than were producer invasions. Given these differences between ecosystems and between marine trophic levels, we used a model-selection approach to assess if factors other than the resistance mechanism (i.e. competition vs. consumption) are more important for predicting marine biotic resistance. These results suggest that understanding marine biotic resistance depends on latitude, habitat and invader taxon, in addition to distinguishing between competition with and consumption by native species. By examining biotic resistance within and across ecosystems, our work provides a more complete understanding of the factors that underlie biological invasions.

Diminished warming tolerance and plasticity in low-latitude populations of a marine gastropod.

Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from native Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance - habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations.

Biotic resistance to invasion along an estuarine gradient.

Biotic resistance is the ability of native communities to repel the establishment of invasive species. Predation by native species may confer biotic resistance to communities, but the environmental context under which this form of biotic resistance occurs is not well understood. We evaluated several factors that influence the distribution of invasive Asian mussels (Musculista senhousia) in Mission Bay, a southern California estuary containing an extensive eelgrass (Zostera marina) habitat. Asian mussels exhibit a distinct spatial pattern of invasion, with extremely high densities towards the back of Mission Bay (up to 4,000 m(-2)) in contrast with near-complete absence at sites towards the front of the bay. We established that recruits arrived at sites where adult mussels were absent and found that dense eelgrass does not appear to preclude Asian mussel growth and survival. Mussel survival and growth were high in predator-exclusion plots throughout the bay, but mussel survival was low in the front of the bay when plots were open to predators. Additional experiments revealed that consumption by spiny lobsters (Panulirus interruptus) and a gastropod (Pteropurpura festiva) likely are the primary factors responsible for resistance to Asian mussel invasion. However, biotic resistance was dependent on location within the estuary (for both species) and also on the availability of a hard substratum (for P. festiva). Our findings indicate that biotic resistance in the form of predation may be conferred by higher order predators, but that the strength of resistance may strongly vary across estuarine gradients and depend on the nature of the locally available habitat.

Can marine reserves restore lost ecosystem functioning? A global synthesis.

Marine protected areas (MPAs) have grown exponentially, emerging as a widespread tool to conserve biodiversity and enhance fisheries production. Although numerous empirical studies and global syntheses have evaluated the effects of MPAs on community structure (e.g., biodiversity), no broad assessment concerning their capacity to influence ecological processes (e.g., species interactions) exists. Here, we present meta-analyses that compare rates of predation and herbivory on a combined 32 species across 30 MPAs spanning 85° of latitude. Our analyses synthesize the fate of 15,225 field experiment assays, and demonstrate that MPAs greatly increased predation intensity on animals but not herbivory on macroalgae or seagrass. Predation risk, quantified as the odds of prey being eaten, was largely determined by predator abundance and biomass within reserves. At MPAs with the greatest predator accumulation, the odds of predation increased to nearly 49:1, as opposed to 1:1 at MPAs where predators actually declined. Surprisingly, we also found evidence that predation risk declined with increased sea-surface temperature. Greater predation risk within MPAs was consistent with predator and prey population abundance estimates, where predators increased 4.4-fold within MPAs, whereas prey decreased 2.2-fold. For herbivory, the lack of change may have been driven by functional redundancy and the inability of reserves to increase herbivore abundance relative to fished zones in our sample. Overall, this work highlights the capacity of MPAs to restore a critical ecosystem function such as predation, which mediates energy flows and community assembly within natural systems. However, our review of the literature also uncovers relatively few studies that have quantified the effects of MPAs on ecosystem function, highlighting a key gap in our understanding of how protected areas may alter ecological processes and deliver ecosystem services. From a historical perspective, these findings suggest that modern levels of predation in the coastal oceans may currently only be a fraction of the baseline prior to human exploitation.