Emergent effects of global change on consumption depend on consumers and their resources in marine systems.

A better understanding of how environmental change will affect species interactions would significantly aid efforts to scale up predictions of near-future responses to global change from individuals to ecosystems. To address this need, we used meta-analysis to quantify the individual and combined effects of ocean acidification (OA) and warming on consumption rates of predators and herbivores in marine ecosystems. Although the primary studies demonstrated that these environmental variables can have direct effects on consumers, our analyses highlight high variability in consumption rates in response to OA and warming. This variability likely reflects differences in local adaptation among species, as well as important methodological differences. For example, our results suggest that exposure of consumers to OA reduces consumption rates on average, yet consumption rates actually increase when both consumers and their resource(s) are concurrently exposed to the same conditions. We hypothesize that this disparity is due to increased vulnerability of prey or resource(s) in conditions of OA that offset declines in consumption. This hypothesis is supported by an analysis demonstrating clear declines in prey survival in studies that exposed only prey to future OA conditions. Our results illustrate how simultaneous OA and warming produce complex outcomes when species interact. Researchers should further explore other potential sources of variation in response, as well as the prey-driven component of any changes in consumption and the potential for interactive effects of OA and warming.

Southeast Alaskan kelp forests: inferences of process from large-scale patterns of variation in space and time.

Humans were considered external drivers in much foundational ecological research. A recognition that humans are embedded in the complex interaction networks we study can provide new insight into our ecological paradigms. Here, we use time-series data spanning three decades to explore the effects of human harvesting on otter-urchin-kelp trophic cascades in southeast Alaska. These effects were inferred from variation in sea urchin and kelp abundance following the post fur trade repatriation of otters and a subsequent localized reduction of otters by human harvest in one location. In an example of a classic trophic cascade, otter repatriation was followed by a 99% reduction in urchin biomass density and a greater than 99% increase in kelp density region wide. Recent spatially concentrated harvesting of otters was associated with a localized 70% decline in otter abundance in one location, with urchins increasing and kelps declining in accordance with the spatial pattern of otter occupancy within that region. While the otter-urchin-kelp trophic cascade has been associated with alternative community states at the regional scale, this research highlights how small-scale variability in otter occupancy, ostensibly due to spatial variability in harvesting or the risk landscape for otters, can result in within-region patchiness in these community states.

Upwelling-level acidification and pH/pCO2 variability moderate effects of ocean acidification on brain gene expression in the temperate surfperch, Embiotoca jacksoni.

Acidification-induced changes in neurological function have been documented in several tropical marine fishes. Here, we investigate whether similar patterns of neurological impacts are observed in a temperate Pacific fish that naturally experiences regular and often large shifts in environmental pH/pCO2 . In two laboratory experiments, we tested the effect of acidification, as well as pH/pCO2 variability, on gene expression in the brain tissue of a common temperate kelp forest/estuarine fish, Embiotoca jacksoni. Experiment 1 employed static pH treatments (target pH = 7.85/7.30), while Experiment 2 incorporated two variable treatments that oscillated around corresponding static treatments with the same mean (target pH = 7.85/7.70) in an eight-day cycle (amplitude ± 0.15). We found that patterns of global gene expression differed across pH level treatments. Additionally, we identified differential expression of specific genes and enrichment of specific gene sets (GSEA) in comparisons of static pH treatments and in comparisons of static and variable pH treatments of the same mean pH. Importantly, we found that pH/pCO2 variability decreased the number of differentially expressed genes detected between high and low pH treatments, and that interindividual variability in gene expression was greater in variable treatments than static treatments. These results provide important confirmation of neurological impacts of acidification in a temperate fish species and, critically, that natural environmental variability may mediate the impacts of ocean acidification.

Coupled changes in pH, temperature, and dissolved oxygen impact the physiology and ecology of herbivorous kelp forest grazers.

Understanding species' responses to upwelling may be especially important in light of ongoing environmental change. Upwelling frequency and intensity are expected to increase in the future, while ocean acidification and deoxygenation are expected to decrease the pH and dissolved oxygen (DO) of upwelled waters. However, the acute effects of a single upwelling event and the integrated effects of multiple upwelling events on marine organisms are poorly understood. Here, we use in situ measurements of pH, temperature, and DO to characterize the covariance of environmental conditions within upwelling-dominated kelp forest ecosystems. We then test the effects of acute (0-3 days) and chronic (1-3 months) upwelling on the performance of two species of kelp forest grazers, the echinoderm, Mesocentrotus franciscanus, and the gastropod, Promartynia pulligo. We exposed organisms to static conditions in a regression design to determine the shape of the relationship between upwelling and performance and provide insights into the potential effects in a variable environment. We found that respiration, grazing, growth, and net calcification decline linearly with increasing upwelling intensity for M. francicanus over both acute and chronic timescales. Promartynia pulligo exhibited decreased respiration, grazing, and net calcification with increased upwelling intensity after chronic exposure, but we did not detect an effect over acute timescales or on growth after chronic exposure. Given the highly correlated nature of pH, temperature, and DO in the California Current, our results suggest the relationship between upwelling intensity and growth in the 3-month trial could potentially be used to estimate growth integrated over long-term dynamic oceanographic conditions for M. franciscanus. Together, these results indicate current exposure to upwelling may reduce species performance and predicted future increases in upwelling frequency and intensity could affect ecosystem function by modifying the ecological roles of key species.

Resilient consumers accelerate the plant decomposition in a naturally acidified seagrass ecosystem.

Anthropogenic stressors are predicted to alter biodiversity and ecosystem functioning worldwide. However, scaling up from species to ecosystem responses poses a challenge, as species and functional groups can exhibit different capacities to adapt, acclimate, and compensate under changing environments. We used a naturally acidified seagrass ecosystem (the endemic Mediterranean Posidonia oceanica) as a model system to examine how ocean acidification (OA) modifies the community structure and functioning of plant detritivores, which play vital roles in the coastal nutrient cycling and food web dynamics. In seagrass beds associated with volcanic CO2 vents (Ischia, Italy), we quantified the effects of OA on seagrass decomposition by deploying litterbags in three distinct pH zones (i.e., ambient, low, extreme low pH), which differed in the mean and variability of seawater pH. We replicated the study in two discrete vents for 117 days (litterbags sampled on day 5, 10, 28, 55, and 117). Acidification reduced seagrass detritivore richness and diversity through the loss of less abundant, pH-sensitive species but increased the abundance of the dominant detritivore (amphipod Gammarella fucicola). Such compensatory shifts in species abundance caused more than a threefold increase in the total detritivore abundance in lower pH zones. These community changes were associated with increased consumption (52%-112%) and decay of seagrass detritus (up to 67% faster decomposition rate for the slow-decaying, refractory detrital pool) under acidification. Seagrass detritus deployed in acidified zones showed increased N content and decreased C:N ratio, indicating that altered microbial activities under OA may have affected the decay process. The findings suggest that OA could restructure consumer assemblages and modify plant decomposition in blue carbon ecosystems, which may have important implications for carbon sequestration, nutrient recycling, and trophic transfer. Our study highlights the importance of within-community response variability and compensatory processes in modulating ecosystem functions under extreme global change scenarios.

Standing Crop, Turnover, and Production Dynamics of Macrocystis pyrifera and Understory Species Hedophyllum nigripes and Neoagarum fimbriatum in High Latitude Giant Kelp Forests.

Production rates reported for canopy-forming kelps have highlighted the potential contributions of these foundational macroalgal species to carbon cycling and sequestration on a globally relevant scale. Yet, the production dynamics of many kelp species remain poorly resolved. For example, productivity estimates for the widely distributed giant kelp Macrocystis pyrifera are based on a few studies from the center of this species' range. To address this geospatial bias, we surveyed giant kelp beds in their high latitude fringe habitat in southeast Alaska to quantify foliar standing crop, growth and loss rates, and productivity of M. pyrifera and co-occurring understory kelps Hedophyllum nigripes and Neoagarum fimbriatum. We found that giant kelp beds at the poleward edge of their range produce ~150 g C · m-2 · year-1 from a standing biomass that turns over an estimated 2.1 times per year, substantially lower rates than have been observed at lower latitudes. Although the productivity of high latitude M. pyrifera dwarfs production by associated understory kelps in both winter and summer seasons, phenological differences in growth and relative carbon and nitrogen content among the three kelp species suggests their complementary value as nutritional resources to consumers. This work represents the highest latitude consideration of M. pyrifera forest production to date, providing a valuable quantification of kelp carbon cycling in this highly seasonal environment.

Coast-wide evidence of low pH amelioration by seagrass ecosystems.

Global-scale ocean acidification has spurred interest in the capacity of seagrass ecosystems to increase seawater pH within crucial shoreline habitats through photosynthetic activity. However, the dynamic variability of the coastal carbonate system has impeded generalization into whether seagrass aerobic metabolism ameliorates low pH on physiologically and ecologically relevant timescales. Here we present results of the most extensive study to date of pH modulation by seagrasses, spanning seven meadows (Zostera marina) and 1000 km of U.S. west coast over 6 years. Amelioration by seagrass ecosystems compared to non-vegetated areas occurred 65% of the time (mean increase 0.07 ± 0.008 SE). Events of continuous elevation in pH within seagrass ecosystems, indicating amelioration of low pH, were longer and of greater magnitude than opposing cases of reduced pH or exacerbation. Sustained elevations in pH of >0.1, comparable to a 30% decrease in [H+ ], were not restricted only to daylight hours but instead persisted for up to 21 days. Maximal pH elevations occurred in spring and summer during the seagrass growth season, with a tendency for stronger effects in higher latitude meadows. These results indicate that seagrass meadows can locally alleviate low pH conditions for extended periods of time with important implications for the conservation and management of coastal ecosystems.

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.

Windows of vulnerability: Seasonal mismatches in exposure and resource identity determine ocean acidification's effect on a primary consumer at high latitude.

It is well understood that differences in the cues used by consumers and their resources in fluctuating environments can give rise to trophic mismatches governing the emergent effects of global change. Trophic mismatches caused by changes in consumer energetics during periods of low resource availability have received far less attention, although this may be common for consumers during winter when primary producers are limited by light. Even less is understood about these dynamics in marine ecosystems, where consumers must cope with energetically costly changes in CO2 -driven carbonate chemistry that will be most pronounced in cold temperatures. This may be especially important for calcified marine herbivores, such as the pinto abalone (Haliotis kamschatkana). H. kamschatkana are of high management concern in the North Pacific due to the active recreational fishery and their importance among traditional cultures, and research suggests they may require more energy to maintain their calcified shells and acid/base balance with ocean acidification. Here we use field surveys to demonstrate seasonal mismatches in the exposure of marine consumers to low pH and algal resource identity during winter in a subpolar, marine ecosystem. We then use these data to test how the effects of exposure to seasonally relevant pH conditions on H. kamschatkana are mediated by seasonal resource identity. We find that exposure to projected future winter pH conditions decreases metabolism and growth, and this effect on growth is pronounced when their diet is limited to the algal species available during winter. Our results suggest that increases in the energetic demands of pinto abalone caused by ocean acidification during winter will be exacerbated by seasonal shifts in their resources. These findings have profound implications for other marine consumers and highlight the importance of considering fluctuations in exposure and resources when inferring the emergent effects of global change.

Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology.

The environmental conditions in the ocean have long been considered relatively more stable through time compared to the conditions on land. Advances in sensing technologies, however, are increasingly revealing substantial fluctuations in abiotic factors over ecologically and evolutionarily relevant timescales in the ocean, leading to a growing recognition of the dynamism of the marine environment as well as new questions about how this dynamism may influence species' vulnerability to global environmental change. In some instances, the diurnal or seasonal variability in major environmental change drivers, such as temperature, pH and seawater carbonate chemistry, and dissolved oxygen, can exceed the changes expected with continued anthropogenic global change. While ocean global change biologists have begun to experimentally test how variability in environmental conditions mediates species' responses to changes in the mean, the extensive literature on species' adaptations to temporal variability in their environment and the implications of this variability for their evolutionary responses has not been well integrated into the field. Here, we review the physiological mechanisms underlying species' responses to changes in temperature, pCO2 /pH (and other carbonate parameters), and dissolved oxygen, and discuss what is known about behavioral, plastic, and evolutionary strategies for dealing with variable environments. In addition, we discuss how exposure to variability may influence species' responses to changes in the mean conditions and highlight key research needs for ocean global change biology.

Geographic variation in responses of kelp forest communities of the California Current to recent climatic changes.

The changing global climate is having profound effects on coastal marine ecosystems around the world. Structure, functioning, and resilience, however, can vary geographically, depending on species composition, local oceanographic forcing, and other pressures from human activities and use. Understanding ecological responses to environmental change and predicting changes in the structure and functioning of whole ecosystems require large-scale, long-term studies, yet most studies trade spatial extent for temporal duration. We address this shortfall by integrating multiple long-term kelp forest monitoring datasets to evaluate biogeographic patterns and rates of change of key functional groups (FG) along the west coast of North America. Analysis of data from 469 sites spanning Alaska, USA, to Baja California, Mexico, and 373 species (assigned to 18 FG) reveals regional variation in responses to both long-term (2006-2016) change and a recent marine heatwave (2014-2016) associated with two atmospheric and oceanographic anomalies, the "Blob" and extreme El Niño Southern Oscillation (ENSO). Canopy-forming kelps appeared most sensitive to warming throughout their range. Other FGs varied in their responses among trophic levels, ecoregions, and in their sensitivity to heatwaves. Changes in community structure were most evident within the southern and northern California ecoregions, while communities in the center of the range were more resilient. We report a poleward shift in abundance of some key FGs. These results reveal major, ongoing region-wide changes in productive coastal marine ecosystems in response to large-scale climate variability, and the potential loss of foundation species. In particular, our results suggest that coastal communities that are dependent on kelp forests will be more impacted in the southern portion of the California Current region, highlighting the urgency of implementing adaptive strategies to sustain livelihoods and ensure food security. The results also highlight the value of multiregional integration and coordination of monitoring programs for improving our understanding of marine ecosystems, with the goal of informing policy and resource management in the future.

Opportunities for behavioral rescue under rapid environmental change.

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

Unexpected resilience of a seagrass system exposed to global stressors.

Despite a growing interest in identifying tipping points in response to environmental change, our understanding of the ecological mechanisms underlying nonlinear ecosystem dynamics is limited. Ecosystems governed by strong species interactions can provide important insight into how nonlinear relationships between organisms and their environment propagate through ecosystems, and the potential for environmentally mediated species interactions to drive or protect against sudden ecosystem shifts. Here, we experimentally determine the functional relationships (i.e., the shapes of the relationships between predictor and response variables) of a seagrass assemblage with well-defined species interactions to ocean acidification (enrichment of CO2 ) in isolation and in combination with nutrient loading. We demonstrate that the effect of ocean acidification on grazer biomass (Phyllaplysia taylori and Idotea resecata) was quadratic, with the peak of grazer biomass at mid-pH levels. Algal grazing was negatively affected by nutrients, potentially due to low grazer affinity for macroalgae (Ulva intestinalis), as recruitment of both macroalgae and diatoms were favored in elevated nutrient conditions. This led to an exponential increase in macroalgal and epiphyte biomass with ocean acidification, regardless of nutrient concentration. When left unchecked, algae can cause declines in seagrass productivity and persistence through shading and competition. Despite quadratic and exponential functional relationships to stressors that could cause a nonlinear decrease in seagrass biomass, productivity of our model seagrass-the eelgrass (Zostera marina)- remained highly resilient to increasing acidification. These results suggest that important species interactions governing ecosystem dynamics may shift with environmental change, and ecosystem state may be decoupled from ecological responses at lower levels of organization.

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.

Does sex really matter? Explaining intraspecies variation in ocean acidification responses.

Ocean acidification (OA) poses a major threat to marine ecosystems globally, having significant ecological and economic importance. The number and complexity of experiments examining the effects of OA has substantially increased over the past decade, in an attempt to address multi-stressor interactions and long-term responses in an increasing range of aquatic organisms. However, differences in the response of males and females to elevated pCO2 have been investigated in fewer than 4% of studies to date, often being precluded by the difficulty of determining sex non-destructively, particularly in early life stages. Here we highlight that sex can significantly impact organism responses to OA, differentially affecting physiology, reproduction, biochemistry and ultimately survival. What is more, these impacts do not always conform to ecological theory based on differential resource allocation towards reproduction, which would predict females to be more sensitive to OA owing to the higher production cost of eggs compared with sperm. Therefore, non-sex-specific studies may overlook subtle but ecologically significant differences in the responses of males and females to OA, with consequences for forecasting the fate of natural populations in a near-future ocean.

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.

Community dynamics and ecosystem simplification in a high-CO2 ocean.

Disturbances are natural features of ecosystems that promote variability in the community and ultimately maintain diversity. Although it is recognized that global change will affect environmental disturbance regimes, our understanding of the community dynamics governing ecosystem recovery and the maintenance of functional diversity in future scenarios is very limited. Here, we use one of the few ecosystems naturally exposed to future scenarios of environmental change to examine disturbance and recovery dynamics. We examine the recovery patterns of marine species from a physical disturbance across different acidification regimes caused by volcanic CO2 vents. Plots of shallow rocky reef were cleared of all species in areas of ambient, low, and extreme low pH that correspond to near-future and extreme scenarios for ocean acidification. Our results illustrate how acidification decreases the variability of communities, resulting in homogenization and reduced functional diversity at a landscape scale. Whereas the recovery trajectories in ambient pH were highly variable and resulted in a diverse range of assemblages, recovery was more predictable with acidification and consistently resulted in very similar algal-dominated assemblages. Furthermore, low pH zones had fewer signs of biological disturbance (primarily sea urchin grazing) and increased recovery rates of the dominant taxa (primarily fleshy algae). Together, our results highlight how environmental change can cause ecosystem simplification via environmentally mediated changes in community dynamics in the near future, with cascading impacts on functional diversity and ecosystem function.

Ocean acidification through the lens of ecological theory.

Ocean acidification, chemical changes to the carbonate system of seawater, is emerging as a key environmental challenge accompanying global warming and other human-induced perturbations. Considerable research seeks to define the scope and character of potential outcomes from this phenomenon, but a crucial impediment persists. Ecological theory, despite its power and utility, has been only peripherally applied to the problem. Here we sketch in broad strokes several areas where fundamental principles of ecology have the capacity to generate insight into ocean acidification's consequences. We focus on conceptual models that, when considered in the context of acidification, yield explicit predictions regarding a spectrum of population- and community-level effects, from narrowing of species ranges and shifts in patterns of demographic connectivity, to modified consumer-resource relationships, to ascendance of weedy taxa and loss of species diversity. Although our coverage represents only a small fraction of the breadth of possible insights achievable from the application of theory, our hope is that this initial foray will spur expanded efforts to blend experiments with theoretical approaches. The result promises to be a deeper and more nuanced understanding of ocean acidification'and the ecological changes it portends.

Divergent ecosystem responses within a benthic marine community to ocean acidification.

Ocean acidification is predicted to impact all areas of the oceans and affect a diversity of marine organisms. However, the diversity of responses among species prevents clear predictions about the impact of acidification at the ecosystem level. Here, we used shallow water CO(2) vents in the Mediterranean Sea as a model system to examine emergent ecosystem responses to ocean acidification in rocky reef communities. We assessed in situ benthic invertebrate communities in three distinct pH zones (ambient, low, and extreme low), which differed in both the mean and variability of seawater pH along a continuous gradient. We found fewer taxa, reduced taxonomic evenness, and lower biomass in the extreme low pH zones. However, the number of individuals did not differ among pH zones, suggesting that there is density compensation through population blooms of small acidification-tolerant taxa. Furthermore, the trophic structure of the invertebrate community shifted to fewer trophic groups and dominance by generalists in extreme low pH, suggesting that there may be a simplification of food webs with ocean acidification. Despite high variation in individual species' responses, our findings indicate that ocean acidification decreases the diversity, biomass, and trophic complexity of benthic marine communities. These results suggest that a loss of biodiversity and ecosystem function is expected under extreme acidification scenarios.