Metabolic plasticity drives mismatches in physiological traits between prey and predator.

Metabolic rate, the rate of energy use, underpins key ecological traits of organisms, from development and locomotion to interaction rates between individuals. In a warming world, the temperature-dependence of metabolic rate is anticipated to shift predator-prey dynamics. Yet, there is little real-world evidence on the effects of warming on trophic interactions. We measured the respiration rates of aquatic larvae of three insect species from populations experiencing a natural temperature gradient in a large-scale mesocosm experiment. Using a mechanistic model we predicted the effects of warming on these taxa's predator-prey interaction rates. We found that species-specific differences in metabolic plasticity lead to mismatches in the temperature-dependence of their relative velocities, resulting in altered predator-prey interaction rates. This study underscores the role of metabolic plasticity at the species level in modifying trophic interactions and proposes a mechanistic modelling approach that allows an efficient, high-throughput estimation of climate change threats across species pairs.

Regional impacts of warming on biodiversity and biomass in high latitude stream ecosystems across the Northern Hemisphere.

Warming can have profound impacts on ecological communities. However, explorations of how differences in biogeography and productivity might reshape the effect of warming have been limited to theoretical or proxy-based approaches: for instance, studies of latitudinal temperature gradients are often conflated with other drivers (e.g., species richness). Here, we overcome these limitations by using local geothermal temperature gradients across multiple high-latitude stream ecosystems. Each suite of streams (6-11 warmed by 1-15°C above ambient) is set within one of five regions (37 streams total); because the heating comes from the bedrock and is not confounded by changes in chemistry, we can isolate the effect of temperature. We found a negative overall relationship between diatom and invertebrate species richness and temperature, but the strength of the relationship varied regionally, declining more strongly in regions with low terrestrial productivity. Total invertebrate biomass increased with temperature in all regions. The latter pattern combined with the former suggests that the increased biomass of tolerant species might compensate for the loss of sensitive species. Our results show that the impact of warming can be dependent on regional conditions, demonstrating that local variation should be included in future climate projections rather than simply assuming universal relationships.

Warming indirectly simplifies food webs through effects on apex predators.

Warming alters ecosystems through direct physiological effects on organisms and indirect effects via biotic interactions, but their relative impacts in the wild are unknown due to the difficulty in warming natural environments. Here we bridge this gap by embedding manipulative field experiments within a natural stream temperature gradient to test whether warming and apex fish predators have interactive effects on freshwater ecosystems. Fish exerted cascading effects on algal production and microbial decomposition via both green and brown pathways in the food web, but only under warming. Neither temperature nor the presence of fish altered food web structure alone, but connectance and mean trophic level declined as consumer species were lost when both drivers acted together. A mechanistic model indicates that this temperature-induced trophic cascade is determined primarily by altered interactions, which cautions against extrapolating the impacts of warming from reductionist approaches that do not consider the wider food web.

Metabolic plasticity can amplify ecosystem responses to global warming.

Organisms have the capacity to alter their physiological response to warming through acclimation or adaptation, but the consequence of this metabolic plasticity for energy flow through food webs is currently unknown, and a generalisable framework does not exist for modelling its ecosystem-level effects. Here, using temperature-controlled experiments on stream invertebrates from a natural thermal gradient, we show that the ability of organisms to raise their metabolic rate following chronic exposure to warming decreases with increasing body size. Chronic exposure to higher temperatures also increases the acute thermal sensitivity of whole-organismal metabolic rate, independent of body size. A mathematical model parameterised with these findings shows that metabolic plasticity could account for 60% higher ecosystem energy flux with just +2 °C of warming than a traditional model based on ecological metabolic theory. This could explain why long-term warming amplifies ecosystem respiration rates through time in recent mesocosm experiments, and highlights the need to embed metabolic plasticity in predictive models of global warming impacts on ecosystems.

Thermal acclimation increases the stability of a predator-prey interaction in warmer environments.

Global warming over the next century is likely to alter the energy demands of consumers and thus the strengths of their interactions with their resources. The subsequent cascading effects on population biomasses could have profound effects on food web stability. One key mechanism by which organisms can cope with a changing environment is phenotypic plasticity, such as acclimation to warmer conditions through reversible changes in their physiology. Here, we measured metabolic rates and functional responses in laboratory experiments for a widespread predator-prey pair of freshwater invertebrates, sampled from across a natural stream temperature gradient in Iceland (4-18℃). This enabled us to parameterize a Rosenzweig-MacArthur population dynamical model to study the effect of thermal acclimation on the persistence of the predator-prey pairs in response to warming. Acclimation to higher temperatures either had neutral effects or reduced the thermal sensitivity of both metabolic and feeding rates for the predator, increasing its energetic efficiency. This resulted in greater stability of population dynamics, as acclimation to higher temperatures increased the biomass of both predator and prey populations with warming. These findings indicate that phenotypic plasticity can act as a buffer against the impacts of environmental warming. As a consequence, predator-prey interactions between ectotherms may be less sensitive to future warming than previously expected, but this requires further investigation across a broader range of interacting species.

Towards a unified study of multiple stressors: divisions and common goals across research disciplines.

Anthropogenic environmental changes, or 'stressors', increasingly threaten biodiversity and ecosystem functioning worldwide. Multiple-stressor research is a rapidly expanding field of science that seeks to understand and ultimately predict the interactions between stressors. Reviews and meta-analyses of the primary scientific literature have largely been specific to either freshwater, marine or terrestrial ecology, or ecotoxicology. In this cross-disciplinary study, we review the state of knowledge within and among these disciplines to highlight commonality and division in multiple-stressor research. Our review goes beyond a description of previous research by using quantitative bibliometric analysis to identify the division between disciplines and link previously disconnected research communities. Towards a unified research framework, we discuss the shared goal of increased realism through both ecological and temporal complexity, with the overarching aim of improving predictive power. In a rapidly changing world, advancing our understanding of the cumulative ecological impacts of multiple stressors is critical for biodiversity conservation and ecosystem management. Identifying and overcoming the barriers to interdisciplinary knowledge exchange is necessary in rising to this challenge. Division between ecosystem types and disciplines is largely a human creation. Species and stressors cross these borders and so should the scientists who study them.

Interactive effects of warming and microplastics on metabolism but not feeding rates of a key freshwater detritivore.

Microplastics are an emerging pollutant of high concern, with their prevalence in the environment linked to adverse impacts on aquatic organisms. However, our knowledge of these impacts on freshwater species is rudimentary, and there is almost no research directly testing how these effects can change under ongoing and future climate warming. Given the potential for multiple stressors to interact in nature, research on the combined impacts of microplastics and environmental temperature requires urgent attention. Thus, we experimentally manipulated environmentally realistic concentrations of microplastics and temperature to partition their independent and combined impacts on metabolic and feeding rates of a model freshwater detritivore. There was a significant increase in metabolic and feeding rates with increasing body mass and temperature, in line with metabolic and foraging theory. Experimental warming altered the effect of microplastics on metabolic rate, which increased with microplastic concentration at the lowest temperature, but decreased at the higher temperatures. The microplastics had no effect on the amount of litter consumed by the detritivores, therefore, did not result in altered feeding rates. These results show that the metabolism of important freshwater detritivores could be altered by short-term exposure to microplastics, with greater inhibition of metabolic rates at higher temperatures. The consequences of these metabolic changes may take longer to manifest than the duration of our experiments, requiring further investigation. Our results suggest little short-term impact of microplastics on litter breakdown by gammarid amphipods and highlight the importance of environmental context for a better understanding of microplastic pollution in freshwater ecosystems.

Consistent temperature dependence of functional response parameters and their use in predicting population abundance.

Global warming is one of the greatest threats to the persistence of populations: increased metabolic demands should strengthen pairwise species interactions, which could destabilize food webs at the higher organizational levels. Quantifying the temperature dependence of consumer-resource interactions is thus essential for predicting ecological responses to warming. We explored feeding interactions between different predator-prey pairs in controlled-temperature chambers and in a system of naturally heated streams. We found consistent temperature dependence of attack rates across experimental settings, though the magnitude and activation energy of attack rate were specific to each predator, which varied in mobility and foraging mode. We used these parameters along with metabolic rate measurements to estimate energetic efficiency and population abundance with warming. Energetic efficiency accurately estimated field abundance of a mobile predator that struggled to meet its metabolic demands, but was a poor predictor for a sedentary predator that operated well below its energetic limits. Temperature effects on population abundance may thus be strongly dependent on whether organisms are regulated by their own energy intake or interspecific interactions. Given the widespread use of functional response parameters in ecological modelling, reconciling outcomes from laboratory and field studies increases the confidence and precision with which we can predict warming impacts on natural systems.

Long-term exposure to higher temperature increases the thermal sensitivity of grazer metabolism and movement.

Ecological studies of global warming impacts have many constraints. Organisms are often exposed to higher temperatures for short periods of time, probably underestimating their ability to acclimate or adapt relative to slower but real rates of warming. Many studies also focus on a limited number of traits and miss the multifaceted effects that warming may have on organisms, from physiology to behaviour. Organisms exhibit different movement traits, some of which are primarily driven by metabolic processes and others by decision-making, which should influence the extent to which temperature affects them. We collected snails from streams that have been differentially heated by geothermal activity for decades to determine how long-term exposure to different temperatures affected their metabolism and movement. Additionally, we collected snails from a cold stream (5°C) and measured their metabolism and movement at higher temperatures (short-term exposure). We used respirometry to measure metabolic rates and automated in situ image-based tracking to quantify several movement traits from 5 to 21°C. Long-term exposure to higher temperatures resulted in a greater thermal sensitivity of metabolic rate compared to snails exposed for short durations, highlighting the need for caution when conducting acute temperature exposures in global warming research. Average speed, which is largely driven by metabolism, also increased more with temperature for long-term exposure compared to short-term exposure. Movement traits we interpret as more decision-based, such as time spent moving and trajectory shape, were less affected by temperature. Step length increased and step angle decreased at higher temperatures for both long- and short-term exposure, resulting in overall straighter trajectories. The power-law exponent of the step length distributions and fractal dimension of trajectories were independent of temperature, however, suggesting that snails retained the same movement strategy. The observed changes in snail movement at higher temperatures should lead to higher encounter rates and more efficient searching, providing a behavioural mechanism for stronger plant-herbivore interactions in warmer environments. Our research is among the first to show that temperature has contrasting effects on different movement traits, which may be determined by the metabolic contribution to those behaviours.

Herbivory enables marine communities to resist warming.

Climate change can influence ecosystems via both direct effects on individual organisms and indirect effects mediated by species interactions. However, we understand little about how these changes will ripple through ecosystems or whether there are particular ecological characteristics that might make ecosystems more susceptible-or more resistant-to warming. By combining in situ experimental warming with herbivore manipulations in a natural rocky intertidal community for over 16 months, we show that herbivory regulates the capacity of marine communities to resist warming. We found that limpet herbivores helped to preserve trophic and competitive interactions under experimental warming, dampening the impact of warming on overall community composition. The presence of limpets facilitated the survival of the main habitat modifier (barnacles) under warmer conditions, which, in turn, facilitated the presence of a consumer guild. When limpets were removed, environmental warming altered trophic, competitive, and facilitative interactions, with cascading impacts on community succession and stability. We conclude that conserving trophic structure and the integrity of interaction networks is vitally important as Earth continues to warm.

Embracing interactions in ocean acidification research: confronting multiple stressor scenarios and context dependence.

Changes in the Earth's environment are now sufficiently complex that our ability to forecast the emergent ecological consequences of ocean acidification (OA) is limited. Such projections are challenging because the effects of OA may be enhanced, reduced or even reversed by other environmental stressors or interactions among species. Despite an increasing emphasis on multifactor and multispecies studies in global change biology, our ability to forecast outcomes at higher levels of organization remains low. Much of our failure lies in a poor mechanistic understanding of nonlinear responses, a lack of specificity regarding the levels of organization at which interactions can arise, and an incomplete appreciation for linkages across these levels. To move forward, we need to fully embrace interactions. Mechanistic studies on physiological processes and individual performance in response to OA must be complemented by work on population and community dynamics. We must also increase our understanding of how linkages and feedback among multiple environmental stressors and levels of organization can generate nonlinear responses to OA. This will not be a simple undertaking, but advances are of the utmost importance as we attempt to mitigate the effects of ongoing global change.

Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming.

Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.

EFFECTS OF CLIMATE CHANGE ON GLOBAL SEAWEED COMMUNITIES.

Seaweeds are ecologically important primary producers, competitors, and ecosystem engineers that play a central role in coastal habitats ranging from kelp forests to coral reefs. Although seaweeds are known to be vulnerable to physical and chemical changes in the marine environment, the impacts of ongoing and future anthropogenic climate change in seaweed-dominated ecosystems remain poorly understood. In this review, we describe the ways in which changes in the environment directly affect seaweeds in terms of their physiology, growth, reproduction, and survival. We consider the extent to which seaweed species may be able to respond to these changes via adaptation or migration. We also examine the extensive reshuffling of communities that is occurring as the ecological balance between competing species changes, and as top-down control by herbivores becomes stronger or weaker. Finally, we delve into some of the ecosystem-level responses to these changes, including changes in primary productivity, diversity, and resilience. Although there are several key areas in which ecological insight is lacking, we suggest that reasonable climate-related hypotheses can be developed and tested based on current information. By strategically prioritizing research in the areas of complex environmental variation, multiple stressor effects, evolutionary adaptation, and population, community, and ecosystem-level responses, we can rapidly build upon our current understanding of seaweed biology and climate change ecology to more effectively conserve and manage coastal ecosystems.

Response to technical comment on `meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms'.

It has been proposed that crustaceans should be excluded from a comparison of biological responses to ocean acidification among organisms with different calcium carbonate (CaCO3 ) forms in their calcified structures. We re-analysed our data without crustaceans and found high variation in organismal responses within CaCO3 categories. We conclude that the CaCO3 polymorph alone does not predict sensitivity, and a consideration of functional differences among organisms is necessary for predicting variation in response to acidification.

Dynamics of species interaction strength in space, time and with developmental stage.

Quantifying species interaction strengths enhances prediction of community dynamics, but variability in the strength of species interactions in space and time complicates accurate prediction. Interaction strengths can vary in response to density, indirect effects, priority effects or a changing environment, but the mechanism(s) causing direction and magnitudes of change are often unclear. We designed an experiment to characterize how environmental factors influence the direction and the strength of priority effects between sessile species. We estimated per capita non-trophic effects of barnacles (Semibalanus balanoides) on newly settled germlings of the fucoid, Ascophyllum nodosum, in the presence and absence of consumers in experiments on rocky shores throughout the Gulf of Maine, USA. Per capita effects on germlings varied among environments and barnacle life stages, and these interaction strengths were largely unaltered by changing consumer abundance. Whereas previous evidence shows adult barnacles facilitate fucoids, here, we show that recent settlers and established juveniles initially compete with germlings. As barnacles mature, they switch to become facilitators of fucoids. Consumers caused variable mortality of germlings through time comparable to that from competition. Temporally variable effects of interactors (e.g. S. balanoides), or spatial variation in their population structure, in different regions differentially affect target populations (e.g. A. nodosum). This may affect abundance of critical stages and the resilience of target species to environmental change in different geographical regions.

Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms.

Ocean acidification is a pervasive stressor that could affect many marine organisms and cause profound ecological shifts. A variety of biological responses to ocean acidification have been measured across a range of taxa, but this information exists as case studies and has not been synthesized into meaningful comparisons amongst response variables and functional groups. We used meta-analytic techniques to explore the biological responses to ocean acidification, and found negative effects on survival, calcification, growth and reproduction. However, there was significant variation in the sensitivity of marine organisms. Calcifying organisms generally exhibited larger negative responses than non-calcifying organisms across numerous response variables, with the exception of crustaceans, which calcify but were not negatively affected. Calcification responses varied significantly amongst organisms using different mineral forms of calcium carbonate. Organisms using one of the more soluble forms of calcium carbonate (high-magnesium calcite) can be more resilient to ocean acidification than less soluble forms (calcite and aragonite). Additionally, there was variation in the sensitivities of different developmental stages, but this variation was dependent on the taxonomic group. Our analyses suggest that the biological effects of ocean acidification are generally large and negative, but the variation in sensitivity amongst organisms has important implications for ecosystem responses.

Modeling variation in interaction strength between barnacles and fucoids.

The strength by which species interact can vary throughout their ontogeny, as environments vary in space and time, and with the density of their populations. Characterizing strengths of interaction in situ for even a small number of species is logistically difficult and may apply only to those conditions under which the estimates were derived. We sought to combine data from field experiments estimating interaction strength of life stages of the barnacle, Semibalanus balanoides, on germlings of Ascophyllum nodosum, with a model that explored the consequences of variability at per capita and per population levels to the abundance of year-old algal recruits. We further simulated how this interaction affected fucoid germling abundance as the timing of their respective settlements varied relative to one another, as occurs regionally across the Gulf of Maine, USA. Juvenile S. balanoides have a weak estimated per capita effect on germlings. Germling populations are sensitive to variation in per capita effects of juvenile barnacles because of the typically large population sizes of the latter. However, high mortality of juvenile barnacles weakens the population interaction strength over time. Adult barnacles probably weakly facilitate fucoid germlings, but greater survival of adults sustains the strength of that interaction at the population level. Germling abundance is positively associated with densities of adult barnacles and negatively associated with that of juvenile barnacles. Metamorphosing cyprid larvae have the strongest per capita effect on germling abundance, but the interaction between the two stages is so short-lived that germling abundance is altered little. Variation in the timing of barnacle and A. nodosum settlement relative to one another had very little influence on the abundance of yearling germlings. Interactions between barnacles and germlings may influence the demographic structure of A. nodosum populations and the persistence of fucoid-dominated communities on sheltered rocky shores in New England.