Additive impacts of deoxygenation and acidification threaten marine biota

Deoxygenation in coastal and open‐ocean ecosystems rarely exists in isolation but occurs concomitantly with acidification. Here, we first combine meta‐data of experimental assessments from across the globe to investigate the potential interactive impacts of deoxygenation and acidification on a broad range of marine taxa. We then characterize the differing degrees of deoxygenation and acidification tested in our dataset using a ratio between the partial pressure of oxygen and carbon dioxide (pO₂/pCO₂) to assess how biological processes change under an extensive, yet diverse range of pO₂ and pCO₂ conditions. The dataset comprised 375 experimental comparisons and revealed predominantly additive but variable effects (91.7%, additive; 6.0%, synergistic; and 2.3%, antagonistic) of the dual stressors, yielding negative impacts across almost all responses examined. Our data indicate that the pO₂/pCO₂‐ratio offers a simplified metric to characterize the extremity of the concurrent stressors and shows that more severe impacts occurred when ratios represented more extreme deoxygenation and acidification conditions. Importantly, our analysis highlights the need to assess the concurrent impacts of deoxygenation and acidification on marine taxa and that assessments considering the impact of O₂ depletion alone will likely underestimate the impacts of deoxygenation events and their ecosystem‐wide consequences.     

Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system

Metabolic rate determines the physiological and life-history performances of ectotherms. Thus, the extent to which such rates are sensitive and plastic to environmental perturbation is central to an organism''s ability to function in a changing environment. Little is known of long-term metabolic plasticity and potential for metabolic adaptation in marine ectotherms exposed to elevated pCO₂. Consequently, we carried out a series of in situ transplant experiments using a number of tolerant and sensitive polychaete species living around a natural CO₂ vent system. Here, we show that a marine metazoan (i.e. Platynereis dumerilii) was able to adapt to chronic and elevated levels of pCO₂. The vent population of P. dumerilii was physiologically and genetically different from nearby populations that experience low pCO₂, as well as smaller in body size. By contrast, different populations of Amphiglena mediterranea showed marked physiological plasticity indicating that adaptation or acclimatization are both viable strategies for the successful colonization of elevated pCO₂ environments. In addition, sensitive species showed either a reduced or increased metabolism when exposed acutely to elevated pCO₂. Our findings may help explain, from a metabolic perspective, the occurrence of past mass extinction, as well as shed light on alternative pathways of resilience in species facing ongoing ocean acidification.     

Meta‐analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels

Elevated pCO₂ and warming may promote algal growth and toxin production, and thereby possibly support the proliferation and toxicity of harmful algal blooms (HABs). Here, we tested whether empirical data support this hypothesis using a meta‐analytic approach and investigated the responses of growth rate and toxin content or toxicity of numerous marine and estuarine HAB species to elevated pCO₂ and warming. Most of the available data on HAB responses towards the two tested climate change variables concern dinoflagellates, as many members of this phytoplankton group are known to cause HAB outbreaks. Toxin content and toxicity did not reveal a consistent response towards both tested climate change variables, while growth rate increased consistently with elevated pCO₂. Warming also led to higher growth rates, but only for species isolated at higher latitudes. The observed gradient in temperature growth responses shows the potential for enhanced development of HABs at higher latitudes. Increases in growth rates with more CO₂ may present an additional competitive advantage for HAB species, particularly as CO₂ was not shown to enhance growth rate of other non‐HAB phytoplankton species. However, this may also be related to the difference in representation of dinoflagellate and diatom species in the respective HAB and non‐HAB phytoplankton groups. Since the proliferation of HAB species may strongly depend on their growth rates, our results warn for a greater potential of dinoflagellate HAB development in future coastal waters, particularly in temperate regions.     

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO(2) treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6-7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO(2), and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.     

Modified future diurnal variability of the global surface ocean CO2 system

Our understanding of how increasing atmospheric CO₂ and climate change influences the marine CO₂ system and in turn ecosystems has increasingly focused on perturbations to carbonate chemistry variability. This variability can affect ocean-climate feedbacks and has been shown to influence marine ecosystems. The seasonal variability of the ocean CO₂ system has already changed, with enhanced seasonal variations in the surface ocean pCO₂ over recent decades and further amplification projected by models over the 21st century. Mesocosm studies and CO₂ vent sites indicate that diurnal variability of the CO₂ system, the amplitude of which in extreme events can exceed that of mean seasonal variability, is also likely to be altered by climate change. Here, we modified a global ocean biogeochemical model to resolve physically and biologically driven diurnal variability of the ocean CO₂ system. Forcing the model with 3-h atmospheric outputs derived from an Earth system model, we explore how surface ocean diurnal variability responds to historical changes and project how it changes under two contrasting 21st-century emission scenarios. Compared to preindustrial values, the global mean diurnal amplitude of pCO₂ increases by 4.8 μatm (+226%) in the high-emission scenario but only 1.2 μatm (+55%) in the high-mitigation scenario. The probability of extreme diurnal amplitudes of pCO₂ and [H⁺] is also affected, with 30- to 60-fold increases relative to the preindustrial under high 21st-century emissions. The main driver of heightened pCO₂ diurnal variability is the enhanced sensitivity of pCO₂ to changes in temperature as the ocean absorbs atmospheric CO₂. Our projections suggest that organisms in the future ocean will be exposed to enhanced diurnal variability in pCO₂ and [H⁺], with likely increases in the associated metabolic cost that such variability imposes.     

The effects of elevated temperature and dissolved ρCO2 on a marine foundation species

Understanding how climate change and other environmental stressors will affect species is a fundamental concern of modern ecology. Indeed, numerous studies have documented how climate stressors affect species distributions and population persistence. However, relatively few studies have investigated how multiple climate stressors might affect species. In this study, we investigate the impacts of how two climate change factors affect an important foundation species. Specifically, we tested how ocean acidification from dissolution of CO₂ and increased sea surface temperatures affect multiple characteristics of juvenile eastern oysters (Crassostrea virginica). We found strong impacts of each stressor, but no interaction between the two. Simulated warming to mimic heat stressed summers reduced oyster growth, survival, and filtration rates. Additionally, we found that CO₂‐induced acidification reduced strength of oyster shells, which could potentially facilitate crab predation. As past studies have detected few impacts of these stressors on adult oysters, these results indicate that early life stages of calcareous marine organisms may be more susceptible to effects of ocean acidification and global warming. Overall, these data show that predicted changes in temperature and CO₂ can differentially influence direct effects on individual species, which could have important implications for the nature of their trophic interactions.     

Organism activity levels predict marine invertebrate survival during ancient global change extinctions

Multistressor global change, the combined influence of ocean warming, acidification, and deoxygenation, poses a serious threat to marine organisms. Experimental studies imply that organisms with higher levels of activity should be more resilient, but testing this prediction and understanding organism vulnerability at a global scale, over evolutionary timescales, and in natural ecosystems remain challenging. The fossil record, which contains multiple extinctions triggered by multistressor global change, is ideally suited for testing hypotheses at broad geographic, taxonomic, and temporal scales. Here, I assess the importance of activity level for survival of well‐skeletonized benthic marine invertebrates over a 100‐million‐year‐long interval (Permian to Jurassic periods) containing four global change extinctions, including the end‐Permian and end‐Triassic mass extinctions. More active organisms, based on a semiquantitative score incorporating feeding and motility, were significantly more likely to survive during three of the four extinction events (Guadalupian, end‐Permian, and end‐Triassic). In contrast, activity was not an important control on survival during nonextinction intervals. Both the end‐Permian and end‐Triassic mass extinctions also triggered abrupt shifts to increased dominance by more active organisms. Although mean activity gradually returned toward pre‐extinction values, the net result was a permanent ratcheting of ecosystem‐wide activity to higher levels. Selectivity patterns during ancient global change extinctions confirm the hypothesis that higher activity, a proxy for respiratory physiology, is a fundamental control on survival, although the roles of specific physiological traits (such as extracellular pCO₂ or aerobic scope) cannot be distinguished. Modern marine ecosystems are dominated by more active organisms, in part because of selectivity ratcheting during these ancient extinctions, so on average may be less vulnerable to global change stressors than ancient counterparts. However, ancient extinctions demonstrate that even active organisms can suffer major extinction when the intensity of environmental disruption is intense.     

Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis

For many aquatic organisms, olfactory-mediated behaviour is essential to the maintenance of numerous fitness-enhancing activities, including foraging, reproduction and predator avoidance. Studies in both freshwater and marine ecosystems have demonstrated significant impacts of anthropogenic acidification on olfactory abilities of fish and macroinvertebrates, leading to impaired behavioural responses, with potentially far-reaching consequences to population dynamics and community structure. Whereas the ecological impacts of impaired olfactory-mediated behaviour may be similar between freshwater and marine ecosystems, the underlying mechanisms are quite distinct. In acidified freshwater, molecular change to chemical cues along with reduced olfaction sensitivity appear to be the primary causes of olfactory-mediated behavioural impairment. By contrast, experiments simulating future ocean acidification suggest that interference of high CO₂ with brain neurotransmitter function is the primary cause for olfactory-mediated behavioural impairment in fish. Different physico-chemical characteristics between marine and freshwater systems are probably responsible for these distinct mechanisms of impairment, which, under globally rising CO₂ levels, may lead to strikingly different consequences to olfaction. While fluctuations in pH may occur in both freshwater and marine ecosystems, marine habitat will remain alkaline despite future ocean acidification caused by globally rising CO₂ levels. In this synthesis, we argue that ecosystem-specific mechanisms affecting olfaction need to be considered for effective management and conservation practices.     

Temperate and tropical brown macroalgae thrive,despite decalcification,along natural CO2 gradients

Predicting the impacts of ocean acidification on coastal ecosystems requires an understanding of the effects on macroalgae and their grazers, as these underpin the ecology of rocky shores. Whilst calcified coralline algae (Rhodophyta) appear to be especially vulnerable to ocean acidification, there is a lack of information concerning calcified brown algae (Phaeophyta), which are not obligate calcifiers but are still important producers of calcium carbonate and organic matter in shallow coastal waters. Here, we compare ecological shifts in subtidal rocky shore systems along CO₂ gradients created by volcanic seeps in the Mediterranean and Papua New Guinea, focussing on abundant macroalgae and grazing sea urchins. In both the temperate and tropical systems the abundances of grazing sea urchins declined dramatically along CO₂ gradients. Temperate and tropical species of the calcifying macroalgal genus Padina (Dictyoaceae, Phaeophyta) showed reductions in CaCO₃ content with CO₂ enrichment. In contrast to other studies of calcified macroalgae, however, we observed an increase in the abundance of Padina spp. in acidified conditions. Reduced sea urchin grazing pressure and significant increases in photosynthetic rates may explain the unexpected success of decalcified Padina spp. at elevated levels of CO₂. This is the first study to provide a comparison of ecological changes along CO₂ gradients between temperate and tropical rocky shores. The similarities we found in the responses of Padina spp. and sea urchin abundance at several vent systems increases confidence in predictions of the ecological impacts of ocean acidification over a large geographical range .     

Silent oceans: ocean acidification impoverishes natural soundscapes by altering sound production of the world's noisiest marine invertebrate

Soundscapes are multidimensional spaces that carry meaningful information for many species about the location and quality of nearby and distant resources. Because soundscapes are the sum of the acoustic signals produced by individual organisms and their interactions, they can be used as a proxy for the condition of whole ecosystems and their occupants. Ocean acidification resulting from anthropogenic CO₂ emissions is known to have profound effects on marine life. However, despite the increasingly recognized ecological importance of soundscapes, there is no empirical test of whether ocean acidification can affect biological sound production. Using field recordings obtained from three geographically separated natural CO₂ vents, we show that forecasted end-of-century ocean acidification conditions can profoundly reduce the biological sound level and frequency of snapping shrimp snaps. Snapping shrimp were among the noisiest marine organisms and the suppression of their sound production at vents was responsible for the vast majority of the soundscape alteration observed. To assess mechanisms that could account for these observations, we tested whether long-term exposure (two to three months) to elevated CO₂ induced a similar reduction in the snapping behaviour (loudness and frequency) of snapping shrimp. The results indicated that the soniferous behaviour of these animals was substantially reduced in both frequency (snaps per minute) and sound level of snaps produced. As coastal marine soundscapes are dominated by biological sounds produced by snapping shrimp, the observed suppression of this component of soundscapes could have important and possibly pervasive ecological consequences for organisms that use soundscapes as a source of information. This trend towards silence could be of particular importance for those species whose larval stages use sound for orientation towards settlement habitats.     

The stunting effect of a high CO2 ocean on calcification and development in sea urchin larvae,a synthesis from the tropics to the poles

The stunting effect of ocean acidification on development of calcifying invertebrate larvae has emerged as a significant effect of global change. We assessed the arm growth response of sea urchin echinoplutei, here used as a proxy of larval calcification, to increased seawater acidity/pCO₂ and decreased carbonate mineral saturation in a global synthesis of data from 15 species. Phylogenetic relatedness did not influence the observed patterns. Regardless of habitat or latitude, ocean acidification impedes larval growth with a negative relationship between arm length and increased acidity/pCO₂ and decreased carbonate mineral saturation. In multiple linear regression models incorporating these highly correlated parameters, pCO₂ exerted the greatest influence on decreased arm growth in the global dataset and also in the data subsets for polar and subtidal species. Thus, reduced growth appears largely driven by organism hypercapnia. For tropical species, decreased carbonate mineral saturation was most important. No single parameter played a dominant role in arm size reduction in the temperate species. For intertidal species, the models were equivocal. Levels of acidification causing a significant (approx. 10–20+%) reduction in arm growth varied between species. In 13 species, reduction in length of arms and supporting skeletal rods was evident in larvae reared in near-future (pCO₂ 800+ µatm) conditions, whereas greater acidification (pCO₂ 1000+ µatm) reduced growth in all species. Although multi-stressor studies are few, when temperature is added to the stressor mix, near-future warming can reduce the negative effect of acidification on larval growth. Broadly speaking, responses of larvae from across world regions showed similar trends despite disparate phylogeny, environments and ecology. Larval success may be the bottleneck for species success with flow-on effects for sea urchin populations and marine ecosystems.     

Lessons from two high CO2 worlds – future oceans and intensive aquaculture

Exponentially rising CO₂ (currently ~400 μatm) is driving climate change and causing acidification of both marine and freshwater environments. Physiologists have long known that CO₂ directly affects acid–base and ion regulation, respiratory function and aerobic performance in aquatic animals. More recently, many studies have demonstrated that elevated CO₂ projected for end of this century (e.g. 800–1000 μatm) can also impact physiology, and have substantial effects on behaviours linked to sensory stimuli (smell, hearing and vision) both having negative implications for fitness and survival. In contrast, the aquaculture industry was farming aquatic animals at CO₂ levels that far exceed end‐of‐century climate change projections (sometimes >10 000 μatm) long before the term ‘ocean acidification’ was coined, with limited detrimental effects reported. It is therefore vital to understand the reasons behind this apparent discrepancy. Potential explanations include 1) the use of ‘control’ CO₂ levels in aquaculture studies that go beyond 2100 projections in an ocean acidification context; 2) the relatively benign environment in aquaculture (abundant food, disease protection, absence of predators) compared to the wild; 3) aquaculture species having been chosen due to their natural tolerance to the intensive conditions, including CO₂ levels; or 4) the breeding of species within intensive aquaculture having further selected traits that confer tolerance to elevated CO₂. We highlight this issue and outline the insights that climate change and aquaculture science can offer for both marine and freshwater settings. Integrating these two fields will stimulate discussion on the direction of future cross‐disciplinary research. In doing so, this article aimed to optimize future research efforts and elucidate effective mitigation strategies for managing the negative impacts of elevated CO₂ on future aquatic ecosystems and the sustainability of fish and shellfish aquaculture.     

Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.     

Adaptation strategies to climate change in marine systems

The world's oceans are highly impacted by climate change and other human pressures, with significant implications for marine ecosystems and the livelihoods that they support. Adaptation for both natural and human systems is increasingly important as a coping strategy due to the rate and scale of ongoing and potential future change. Here, we conduct a review of literature concerning specific case studies of adaptation in marine systems, and discuss associated characteristics and influencing factors, including drivers, strategy, timeline, costs, and limitations. We found ample evidence in the literature that shows that marine species are adapting to climate change through shifting distributions and timing of biological events, while evidence for adaptation through evolutionary processes is limited. For human systems, existing studies focus on frameworks and principles of adaptation planning, but examples of implemented adaptation actions and evaluation of outcomes are scarce. These findings highlight potentially useful strategies given specific social–ecological contexts, as well as key barriers and specific information gaps requiring further research and actions.     

Climate change and ocean acidification effects on seagrasses and marine macroalgae

Although seagrasses and marine macroalgae (macro‐autotrophs) play critical ecological roles in reef, lagoon, coastal and open‐water ecosystems, their response to ocean acidification (OA) and climate change is not well understood. In this review, we examine marine macro‐autotroph biochemistry and physiology relevant to their response to elevated dissolved inorganic carbon [DIC], carbon dioxide [CO₂], and lower carbonate [CO₃^2?] and pH. We also explore the effects of increasing temperature under climate change and the interactions of elevated temperature and [CO₂]. Finally, recommendations are made for future research based on this synthesis. A literature review of >100 species revealed that marine macro‐autotroph photosynthesis is overwhelmingly C₃ (≥ 85%) with most species capable of utilizing HCO₃^?; however, most are not saturated at current ocean [DIC]. These results, and the presence of CO₂‐only users, lead us to conclude that photosynthetic and growth rates of marine macro‐autotrophs are likely to increase under elevated [CO₂] similar to terrestrial C₃ species. In the tropics, many species live close to their thermal limits and will have to up‐regulate stress‐response systems to tolerate sublethal temperature exposures with climate change, whereas elevated [CO₂] effects on thermal acclimation are unknown. Fundamental linkages between elevated [CO₂] and temperature on photorespiration, enzyme systems, carbohydrate production, and calcification dictate the need to consider these two parameters simultaneously. Relevant to calcifiers, elevated [CO₂] lowers net calcification and this effect is amplified by high temperature. Although the mechanisms are not clear, OA likely disrupts diffusion and transport systems of H⁺ and DIC. These fluxes control micro‐environments that promote calcification over dissolution and may be more important than CaCO₃ mineralogy in predicting macroalgal responses to OA. Calcareous macroalgae are highly vulnerable to OA, and it is likely that fleshy macroalgae will dominate in a higher CO₂ ocean; therefore, it is critical to elucidate the research gaps identified in this review.     

Phenotypic plasticity of coralline algae in a High CO2 world

It is important to understand how marine calcifying organisms may acclimatize to ocean acidification to assess their survival over the coming century. We cultured the cold water coralline algae, Lithothamnion glaciale, under elevated pCO₂ (408, 566, 770, and 1024 μatm) for 10 months. The results show that the cell (inter and intra) wall thickness is maintained, but there is a reduction in growth rate (linear extension) at all elevated pCO₂. Furthermore a decrease in Mg content at the two highest CO₂ treatments was observed. Comparison between our data and that at 3 months from the same long‐term experiment shows that the acclimation differs over time since at 3 months, the samples cultured under high pCO₂ showed a reduction in the cell (inter and intra) wall thickness but a maintained growth rate. This suggests a reallocation of the energy budget between 3 and 10 months and highlights the high degree plasticity that is present. This might provide a selective advantage in future high CO₂ world.     

Climate change–contaminant interactions in marine food webs: Toward a conceptual framework

Climate change is reshaping the way in which contaminants move through the global environment, in large part by changing the chemistry of the oceans and affecting the physiology, health, and feeding ecology of marine biota. Climate change‐associated impacts on structure and function of marine food webs, with consequent changes in contaminant transport, fate, and effects, are likely to have significant repercussions to those human populations that rely on fisheries resources for food, recreation, or culture. Published studies on climate change–contaminant interactions with a focus on food web bioaccumulation were systematically reviewed to explore how climate change and ocean acidification may impact contaminant levels in marine food webs. We propose here a conceptual framework to illustrate the impacts of climate change on contaminant accumulation in marine food webs, as well as the downstream consequences for ecosystem goods and services. The potential impacts on social and economic security for coastal communities that depend on fisheries for food are discussed. Climate change–contaminant interactions may alter the bioaccumulation of two priority contaminant classes: the fat‐soluble persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), as well as the protein‐binding methylmercury (MeHg). These interactions include phenomena deemed to be either climate change dominant (i.e., climate change leads to an increase in contaminant exposure) or contaminant dominant (i.e., contamination leads to an increase in climate change susceptibility). We illustrate the pathways of climate change–contaminant interactions using case studies in the Northeastern Pacific Ocean. The important role of ecological and food web modeling to inform decision‐making in managing ecological and human health risks of chemical pollutants contamination under climate change is also highlighted. Finally, we identify the need to develop integrated policies that manage the ecological and socioeconomic risk of greenhouse gases and marine pollutants.