Kristy J. Kroeker

Interactive and cumulative effects of multiple human stressors in marine systems

Humans impact natural systems in a multitude of ways, yet the cumulative effect of multiple stressors on ecological communities remains largely unknown. Here we synthesized 171 studies that manipulated two or more stressors in marine and coastal systems and found that cumulative effects in individual studies were additive (26%), synergistic (36%), and antagonistic (38%). The overall interaction effect across all studies was synergistic, but interaction type varied by response level (community: antagonistic, population: synergistic), trophic level (autotrophs: antagonistic, heterotrophs: synergistic), and specific stressor pair (seven pairs additive, three pairs each synergistic and antagonistic). Addition of a third stressor changed interaction effects significantly in two-thirds of all cases and doubled the number of synergistic interactions. Given that most studies were performed in laboratories where stressor effects can be carefully isolated, these three-stressor results suggest that synergies may be quite common in nature where more than two stressors almost always coexist. While significant gaps exist in multiple stressor research, our results suggest an immediate need to account for stressor interactions in ecological studies and conservation planning.

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.

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 CO2 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.

The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO2) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks direct and indirect effects of CO2 on non-calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We present the model that future atmospheric [CO2] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO2 experiments and data from ‘natural’ volcanic CO2 vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO2 conditions both in temperate and tropical conditions. The benefits of CO2 are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO2 world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO2 as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.

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.

Predicting the Effects of Ocean Acidification on Predator-Prey Interactions: A Conceptual Framework Based on Coastal Molluscs

The influence of environmental change on species interactions will affect population dynamics and community structure in the future, but our current understanding of the outcomes of species interactions in a high-CO2 world is limited. Here, we draw upon emerging experimental research examining the effects of ocean acidification on coastal molluscs to provide hypotheses of the potential impacts of high-CO2 on predator-prey interactions. Coastal molluscs, such as oysters, mussels, and snails, allocate energy among defenses, growth, and reproduction. Ocean acidification increases the energetic costs of physiological processes such as acid-base regulation and calcification. Impacted molluscs can display complex and divergent patterns of energy allocation to defenses and growth that may influence predator-prey interactions; these include changes in shell properties, body size, tissue mass, immune function, or reproductive output. Ocean acidification has also been shown to induce complex changes in chemoreception, behavior, and inducible defenses, including altered cue detection and predator avoidance behaviors. Each of these responses may ultimately alter the susceptibility of coastal molluscs to predation through effects on predator handling time, satiation, and search time. While many of these effects may manifest as increases in per capita predation rates on coastal molluscs, the ultimate outcome of predator-prey interactions will also depend on how ocean acidification affects the specified predators, which also exhibit complex responses to ocean acidification. Changes in predator-prey interactions could have profound and unexplored consequences for the population dynamics of coastal molluscs in a high-CO2 ocean.

Taking Action Against Ocean Acidification: A Review of Management and Policy Options

Ocean acidification has emerged over the last two decades as one of the largest threats to marine organisms and ecosystems. However, most research efforts on ocean acidification have so far neglected management and related policy issues to focus instead on understanding its ecological and biogeochemical implications. This shortfall is addressed here with a systematic, international and critical review of management and policy options. In particular, we investigate the assumption that fighting acidification is mainly, but not only, about reducing CO2 emissions, and explore the leeway that this emerging problem may open in old environmental issues. We review nine types of management responses, initially grouped under four categories: preventing ocean acidification; strengthening ecosystem resilience; adapting human activities; and repairing damages. Connecting and comparing options leads to classifying them, in a qualitative way, according to their potential and feasibility. While reducing CO2 emissions is confirmed as the key action that must be taken against acidification, some of the other options appear to have the potential to buy time, e.g. by relieving the pressure of other stressors, and help marine life face unavoidable acidification. Although the existing legal basis to take action shows few gaps, policy challenges are significant: tackling them will mean succeeding in various areas of environmental management where we failed to a large extent so far.

Preparing to manage coral reefs for ocean acidification: lessons from coral bleaching

Ocean acidification is a direct consequence of increasing atmospheric carbon dioxide concentrations and is expected to compromise the structure and function of coral reefs within this century. Research into the effects of ocean acidification on coral reefs has focused primarily on measuring and predicting changes in seawater carbon (C) chemistry and the biological and geochemical responses of reef organisms to such changes. To date, few ocean acidification studies have been designed to address conservation planning and management priorities. Here, we discuss how existing marine protected area design principles developed to address coral bleaching may be modified to address ocean acidification. We also identify five research priorities needed to incorporate ocean acidification into conservation planning and management: (1) establishing an ocean C chemistry baseline, (2) establishing ecological baselines, (3) determining species/habitat/community sensitivity to ocean acidification, (4) projecting changes in...

Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification

Anthropogenic emissions of carbon dioxide (CO2) are causing ocean acidification, lowering seawater aragonite (CaCO3) saturation state (Ωarag), with potentially substantial impacts on marine ecosystems over the 21st Century. Calcifying organisms have exhibited reduced calcification under lower saturation state conditions in aquaria. However, the in situ sensitivity of calcifying ecosystems to future ocean acidification remains unknown. Here we assess the community level sensitivity of calcification to local CO2-induced acidification caused by natural respiration in an unperturbed, biodiverse, temperate intertidal ecosystem. We find that on hourly timescales nighttime community calcification is strongly influenced by Ωarag, with greater net calcium carbonate dissolution under more acidic conditions. Daytime calcification however, is not detectably affected by Ωarag. If the short-term sensitivity of community calcification to Ωarag is representative of the long-term sensitivity to ocean acidification, nighttime dissolution in these intertidal ecosystems could more than double by 2050, with significant ecological and economic consequences.

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

Changes in the Earths 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.