Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—A review

Marine life is controlled by multiple physical and chemical drivers and by diverse ecological processes. Many of these oceanic properties are being altered by climate change and other anthropogenic pressures. Hence, identifying the influences of multifaceted ocean change, from local to global scales, is a complex task. To guide policy‐making and make projections of the future of the marine biosphere, it is essential to understand biological responses at physiological, evolutionary and ecological levels. Here, we contrast and compare different approaches to multiple driver experiments that aim to elucidate biological responses to a complex matrix of ocean global change. We present the benefits and the challenges of each approach with a focus on marine research, and guidelines to navigate through these different categories to help identify strategies that might best address research questions in fundamental physiology, experimental evolutionary biology and community ecology. Our review reveals that the field of multiple driver research is being pulled in complementary directions: the need for reductionist approaches to obtain process‐oriented, mechanistic understanding and a requirement to quantify responses to projected future scenarios of ocean change. We conclude the review with recommendations on how best to align different experimental approaches to contribute fundamental information needed for science‐based policy formulation.     

Modelling climate‐change‐induced nonlinear thresholds in cephalopod population dynamics

A significant global challenge lies in our current inability to anticipate, and therefore prepare for, critical ecological thresholds (i.e. tipping points in ecosystems). This deficit stems largely from an inadequate understanding of the many complex interactions between species and the environment at the ecosystem level, and the paucity of mechanistic models relating environment to population dynamics at the species level. In marine ecosystems, abundant, short‐lived and fast‐growing species such as anchovies or squids, consistently function as ‘keystone’ groups whose population dynamics affect entire ecosystems. Increasing exploitation coupled with climate change impacts has the potential to affect these ecological groups and consequently, the entire marine ecosystem. There are currently very few models that predict the impact of climate change on these keystone groups. Here we use a combination of individual‐based bioenergetics and stage‐structured population models to characterize the fundamental capacity of cephalopods to respond to climate change. We demonstrate the potential for, and mechanisms behind, two unfavourable climate‐change‐induced thresholds in future population dynamics. Although one threshold was the direct consequence of a decrease in incubation time caused by ocean warming, the other threshold was linked to survivorship, implying the possibility of management through a modification of fishing mortality. Additional substantive changes in phenology were also predicted, with a possible loss in population resilience. Our results demonstrate the feasibility of predicting complex nonlinear dynamics with a reasonably simplistic mechanistic model, and highlight the necessity of developing such approaches for other species if attempts to moderate the impact of climate change on natural resources are to be effective.     

Climate change does not affect the seafood quality of a commonly targeted fish

Climate change can affect marine and estuarine fish via alterations to their distributions, abundances, sizes, physiology and ecological interactions, threatening the provision of ecosystem goods and services. While we have an emerging understanding of such ecological impacts to fish, we know little about the potential influence of climate change on the provision of nutritional seafood to sustain human populations. In particular, the quantity, quality and/or taste of seafood may be altered by future environmental changes with implications for the economic viability of fisheries. In an orthogonal mesocosm experiment, we tested the influence of near‐future ocean warming and acidification on the growth, health and seafood quality of a recreationally and commercially important fish, yellowfin bream (Acanthopagrus australis). The growth of yellowfin bream significantly increased under near‐future temperature conditions (but not acidification), with little change in health (blood glucose and haematocrit) or tissue biochemistry and nutritional properties (fatty acids, lipids, macro‐ and micronutrients, moisture, ash and total N). Yellowfin bream appear to be highly resilient to predicted near‐future ocean climate change, which might be facilitated by their wide spatio‐temporal distribution across habitats and broad diet. Moreover, an increase in growth, but little change in tissue quality, suggests that near‐future ocean conditions will benefit fisheries and fishers that target yellowfin bream. The data reiterate the inherent resilience of yellowfin bream as an evolutionary consequence of their euryhaline status in often environmentally challenging habitats and imply their sustainable and viable fisheries into the future. We contend that widely distributed species that span large geographic areas and habitats can be “climate winners” by being resilient to the negative direct impacts of near‐future oceanic and estuarine climate change.     

Physiological ecology meets climate change

In this article, we pointed out that understanding the physiology of differential climate change effects on organisms is one of the many urgent challenges faced in ecology and evolutionary biology. We explore how physiological ecology can contribute to a holistic view of climate change impacts on organisms and ecosystems and their evolutionary responses. We suggest that theoretical and experimental efforts not only need to improve our understanding of thermal limits to organisms, but also to consider multiple stressors both on land and in the oceans. As an example, we discuss recent efforts to understand the effects of various global change drivers on aquatic ectotherms in the field that led to the development of the concept of oxygen and capacity limited thermal tolerance (OCLTT) as a framework integrating various drivers and linking organisational levels from ecosystem to organism, tissue, cell, and molecules. We suggest seven core objectives of a comprehensive research program comprising the interplay among physiological, ecological, and evolutionary approaches for both aquatic and terrestrial organisms. While studies of individual aspects are already underway in many laboratories worldwide, integration of these findings into conceptual frameworks is needed not only within one organism group such as animals but also across organism domains such as Archaea, Bacteria, and Eukarya. Indeed, development of unifying concepts is relevant for interpreting existing and future findings in a coherent way and for projecting the future ecological and evolutionary effects of climate change on functional biodiversity. We also suggest that OCLTT may in the end and from an evolutionary point of view, be able to explain the limited thermal tolerance of metazoans when compared to other organisms.     

Dynamic energy budget modeling reveals the potential of future growth and calcification for the coccolithophore Emiliania huxleyi in an acidified ocean

Ocean acidification is likely to impact the calcification potential of marine organisms. In part due to the covarying nature of the ocean carbonate system components, including pH and CO₂ and CO₃^2? levels, it remains largely unclear how each of these components may affect calcification rates quantitatively. We develop a process‐based bioenergetic model that explains how several components of the ocean carbonate system collectively affect growth and calcification rates in Emiliania huxleyi, which plays a major role in marine primary production and biogeochemical carbon cycling. The model predicts that under the IPCC A2 emission scenario, its growth and calcification potential will have decreased by the end of the century, although those reductions are relatively modest. We anticipate that our model will be relevant for many other marine calcifying organisms, and that it can be used to improve our understanding of the impact of climate change on marine systems.     

Projecting marine species range shifts from only temperature can mask climate vulnerability

Climate change is causing range shifts in many marine species, with implications for biodiversity and fisheries. Previous research has mainly focused on how species' ranges will respond to changing ocean temperatures, without accounting for other environmental covariates that could affect future distribution patterns. Here, we integrate habitat suitability modeling approaches, a high‐resolution global climate model projection, and detailed fishery‐independent and ‐dependent faunal datasets from one of the most extensively monitored marine ecosystems—the U.S. Northeast Shelf. We project the responses of 125 species in this region to climate‐driven changes in multiple oceanographic factors (e.g., ocean temperature, salinity, sea surface height) and seabed characteristics (i.e., rugosity and depth). Comparing model outputs based on ocean temperature and seabed characteristics to those that also incorporated salinity and sea surface height (proxies for primary productivity and ocean circulation features), we explored how an emphasis on ocean temperature in projecting species' range shifts can impact assessments of species' climate vulnerability. We found that multifactor habitat suitability models performed better in explaining and predicting species historical distribution patterns than temperature‐based models. We also found that multifactor models provided more concerning assessments of species' future distribution patterns than temperature‐based models, projecting that species' ranges will largely shift northward and become more contracted and fragmented over time. Our results suggest that using ocean temperature as a primary determinant of range shifts can significantly alter projections, masking species' climate vulnerability, and potentially forestalling proactive management.     

Strengthened currents override the effect of warming on lobster larval dispersal and survival

Human‐induced climate change is projected to increase ocean temperature and modify circulation patterns, with potential widespread implications for the transport and survival of planktonic larvae of marine organisms. Circulation affects the dispersal of larvae, whereas temperature impacts larval development and survival. However, the combined effect of changes in circulation and temperature on larval dispersal and survival has rarely been studied in a future climate scenario. Such understanding is crucial to predict future species distributions, anticipate ecosystem shifts and design effective management strategies. We simulate contemporary (1990s) and future (2060s) dispersal of lobster larvae using an eddy‐resolving ocean model in south‐eastern Australia, a region of rapid ocean warming. Here we show that the effects of changes in circulation and temperature can counter each other: ocean warming favours the survival of lobster larvae, whereas a strengthened western boundary current diminishes the supply of larvae to the coast by restricting cross‐current larval dispersal. Furthermore, we find that changes in circulation have a stronger effect on connectivity patterns of lobster larvae along south‐eastern Australia than ocean warming in the future climate so that the supply of larvae to the coast reduces by ~4% and the settlement peak shifts poleward by ~270 km in the model simulation. Thus, ocean circulation may be one of the dominant factors contributing to climate‐induced changes of species ranges.     

From global to regional and back again: common climate stressors of marine ecosystems relevant for adaptation across five ocean warming hotspots

Ocean warming ‘hotspots’ are regions characterized by above‐average temperature increases over recent years, for which there are significant consequences for both living marine resources and the societies that depend on them. As such, they represent early warning systems for understanding the impacts of marine climate change, and test‐beds for developing adaptation options for coping with those impacts. Here, we examine five hotspots off the coasts of eastern Australia, South Africa, Madagascar, India and Brazil. These particular hotspots have underpinned a large international partnership that is working towards improving community adaptation by characterizing, assessing and projecting the likely future of coastal‐marine food resources through the provision and sharing of knowledge. To inform this effort, we employ a high‐resolution global ocean model forced by Representative Concentration Pathway 8.5 and simulated to year 2099. In addition to the sea surface temperature, we analyse projected stratification, nutrient supply, primary production, anthropogenic CO₂‐driven ocean acidification, deoxygenation and ocean circulation. Our simulation finds that the temperature‐defined hotspots studied here will continue to experience warming but, with the exception of eastern Australia, may not remain the fastest warming ocean areas over the next century as the strongest warming is projected to occur in the subpolar and polar areas of the Northern Hemisphere. Additionally, we find that recent rapid change in SST is not necessarily an indicator that these areas are also hotspots of the other climatic stressors examined. However, a consistent facet of the hotspots studied here is that they are all strongly influenced by ocean circulation, which has already shown changes in the recent past and is projected to undergo further strong change into the future. In addition to the fast warming, change in local ocean circulation represents a distinct feature of present and future climate change impacting marine ecosystems in these areas.     

Transgenerational plasticity and climate change experiments: Where do we go from here?

Phenotypic plasticity, both within and across generations, is an important mechanism that organisms use to cope with rapid climate change. While an increasing number of studies show that plasticity across generations (transgenerational plasticity or TGP) may occur, we have limited understanding of key aspects of TGP, such as the environmental conditions that may promote it, its relationship to within‐generation plasticity (WGP) and its role in evolutionary potential. In this review, we consider how the detection of TGP in climate change experiments is affected by the predictability of environmental variation, as well as the timing and magnitude of environmental change cues applied. We also discuss the need to design experiments that are able to distinguish TGP from selection and TGP from WGP in multigenerational experiments. We conclude by suggesting future research directions that build on the knowledge to date and admit the limitations that exist, which will depend on the way environmental change is simulated and the type of experimental design used. Such an approach will open up this burgeoning area of research to a wider variety of organisms and allow better predictive capacity of the role of TGP in the response of organisms to future climate change.     

Pelagic food webs: Responses to environmental processes and effects on the environment

Changes in both the environment and environmental research have led to the development of new protocols and approaches. These new approaches consider both the effects of changes in the global environment on living organisms (i.e. the responses of ecosystems to environmental processes) and the feedback responses of these organisms and ecosystems (i.e. the effects of living organisms on the environment). The present paper focuses on pelagic food webs in aquatic ecosystems. We examine three major effects of global environmental changes on aquatic organisms: (i) the release of pollutants and biological agents in lakes and nearshore marine waters; (ii) the loss of biodiversity and the collapse of commercially exploited resources that were heretofore renewable. We develop detailed examples of the effects of human activities on marine organisms (i.e. the effects of nutrient supply on the structure of pelagic food webs in marine systems. Finally, we examine (iii) the food-web-controlled exchanges of CO₂ between the atmosphere and the ocean, as a feedback effect of pelagic ecosystems on the global environment with respect to the ongoing climate change.     

Solutions for ecosystem‐level protection of ocean systems under climate change

The Paris Conference of Parties (COP21) agreement renewed momentum for action against climate change, creating the space for solutions for conservation of the ocean addressing two of its largest threats: climate change and ocean acidification (CCOA). Recent arguments that ocean policies disregard a mature conservation research field and that protected areas cannot address climate change may be oversimplistic at this time when dynamic solutions for the management of changing oceans are needed. We propose a novel approach, based on spatial meta‐analysis of climate impact models, to improve the positioning of marine protected areas to limit CCOA impacts. We do this by estimating the vulnerability of ocean ecosystems to CCOA in a spatially explicit manner and then co‐mapping human activities such as the placement of renewable energy developments and the distribution of marine protected areas. We test this approach in the NE Atlantic considering also how CCOA impacts the base of the food web which supports protected species, an aspect often neglected in conservation studies. We found that, in this case, current regional conservation plans protect areas with low ecosystem‐level vulnerability to CCOA, but disregard how species may redistribute to new, suitable and productive habitats. Under current plans, these areas remain open to commercial extraction and other uses. Here, and worldwide, ocean conservation strategies under CCOA must recognize the long‐term importance of these habitat refuges, and studies such as this one are needed to identify them. Protecting these areas creates adaptive, climate‐ready and ecosystem‐level policy options for conservation, suitable for changing oceans.     

A decade of climate change experiments on marine organisms: procedures,patterns and problems

The first decade of the new millennium saw a flurry of experiments to establish a mechanistic understanding of how climate change might transform the global biota, including marine organisms. However, the biophysical properties of the marine environment impose challenges to experiments, which can weaken their inference space. To facilitate strengthening the experimental evidence for possible ecological consequences of climate change, we reviewed the physical, biological and procedural scope of 110 marine climate change experiments published between 2000 and 2009. We found that 65% of these experiments only tested a single climate change factor (warming or acidification), 54% targeted temperate organisms, 58% were restricted to a single species and 73% to benthic invertebrates. In addition, 49% of the reviewed experiments had issues with the experimental design, principally related to replication of the main test‐factors (temperature or pH), and only 11% included field assessments of processes or associated patterns. Guiding future research by this inventory of current strengths and weaknesses will expand the overall inference space of marine climate change experiments. Specifically, increased effort is required in five areas: (i) the combined effects of concurrent climate and non‐climate stressors; (ii) responses of a broader range of species, particularly from tropical and polar regions as well as primary producers, pelagic invertebrates, and fish; (iii) species interactions and responses of species assemblages, (iv) reducing pseudo‐replication in controlled experiments; and (v) increasing realism in experiments through broad‐scale observations and field experiments. Attention in these areas will improve the generality and accuracy of our understanding of climate change as a driver of biological change in marine ecosystems.     

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.     

Characterizing the multivariate physiogenomic response to environmental change

Global change is altering the climate that species have historically adapted to – in some cases at a pace not recently experienced in their evolutionary history – with cascading effects on all taxa. A central aim in global change biology is to understand how specific populations may be “primed” for global change, either through acclimation or adaptive standing genetic variation. It is therefore an important goal to link physiological measurements to the degree of stress a population experiences (Annual Review of Marine Science, 2012, 4, 39). Although “omic” approaches such as gene expression are often used as a proxy for the amount of stress experienced, we still have a poor understanding of how gene expression affects ecologically and physiologically relevant traits in non‐model organisms. In a From the Cover paper in this issue of Molecular Ecology, Griffiths, Pan and Kelley (Molecular Ecology, 2019, 28) link gene expression to physiological traits in a temperate marine coral. They discover population‐specific responses to ocean acidification for two populations that originated from locations with different histories of exposure to acidification. By integrating physiological and gene expression data, they were able to elucidate the mechanisms that explain these population‐specific responses. Their results give insight into the physiogenomic feedbacks that may prime organisms or make them unfit for ocean global change.     

Ecosystem dynamics based on plankton functional types for global ocean biogeochemistry models

Ecosystem processes are important determinants of the biogeochemistry of the ocean, and they can be profoundly affected by changes in climate. Ocean models currently express ecosystem processes through empirically derived parameterizations that tightly link key geochemical tracers to ocean physics. The explicit inclusion of ecosystem processes in models will permit ecological changes to be taken into account, and will allow us to address several important questions, including the causes of observed glacial–interglacial changes in atmospheric trace gases and aerosols, and how the oceanic uptake of CO₂ is likely to change in the future. There is an urgent need to assess our mechanistic understanding of the environmental factors that exert control over marine ecosystems, and to represent their natural complexity based on theoretical understanding. We present a prototype design for a Dynamic Green Ocean Model (DGOM) based on the identification of (a) key plankton functional types that need to be simulated explicitly to capture important biogeochemical processes in the ocean; (b) key processes controlling the growth and mortality of these functional types and hence their interactions; and (c) sources of information necessary to parameterize each of these processes within a modeling framework. We also develop a strategy for model evaluation, based on simulation of both past and present mean state and variability, and identify potential sources of validation data for each. Finally, we present a DGOM-based strategy for addressing key questions in ocean biogeochemistry. This paper thus presents ongoing work in ocean biogeochemical modeling, which, it is hoped will motivate international collaborations to improve our understanding of the role of the ocean in the climate system.     

Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses

Biological communities are shaped by complex interactions between organisms and their environment as well as interactions with other species. Humans are rapidly changing the marine environment through increasing greenhouse gas emissions, resulting in ocean warming and acidification. The first response by animals to environmental change is predominantly through modification of their behaviour, which in turn affects species interactions and ecological processes. Yet, many climate change studies ignore animal behaviour. Furthermore, our current knowledge of how global change alters animal behaviour is mostly restricted to single species, life phases and stressors, leading to an incomplete view of how coinciding climate stressors can affect the ecological interactions that structure biological communities. Here, we first review studies on the effects of warming and acidification on the behaviour of marine animals. We demonstrate how pervasive the effects of global change are on a wide range of critical behaviours that determine the persistence of species and their success in ecological communities. We then evaluate several approaches to studying the ecological effects of warming and acidification, and identify knowledge gaps that need to be filled, to better understand how global change will affect marine populations and communities through altered animal behaviours. Our review provides a synthesis of the far‐reaching consequences that behavioural changes could have for marine ecosystems in a rapidly changing environment. Without considering the pervasive effects of climate change on animal behaviour we will limit our ability to forecast the impacts of ocean change and provide insights that can aid management strategies.     

Predicting population consequences of ocean climate change for an ecosystem sentinel,the seabird Cassin's auklet

Forecasting the ecological effects of climate change on marine species is critical for informing greenhouse gas mitigation targets and developing marine conservation strategies that remain effective and increase species' resilience under changing climate conditions. Highly productive coastal upwelling systems are predicted to experience substantial effects from climate change, making them priorities for ecological forecasting. We used a population modeling approach to examine the consequences of ocean climate change in the California Current upwelling ecosystem on the population growth rate of the planktivorous seabird Cassin's auklet (Ptychoramphus aleuticus), a demographically sensitive indicator of marine climate change. We use future climate projections for sea surface temperature and upwelling intensity from a regional climate model to forecast changes in the population growth rate of the auklet population at the important Farallon Island colony in central California. Our study projected that the auklet population growth rate will experience an absolute decline of 11–45% by the end of the century, placing this population on a trajectory toward extinction. In addition, future changes in upwelling intensity and timing of peak upwelling are likely to vary across auklet foraging regions in the California Current Ecosystem (CCE), producing a mosaic of climate conditions and ecological impacts across the auklet range. Overall, the Farallon Island Cassin's auklet population has been declining during recent decades, and ocean climate change in this century under a mid‐level emissions scenario is projected to accelerate this decline, leading toward population extinction. Because our study species has proven to be a sensitive indicator of oceanographic conditions in the CCE and a powerful predictor of the abundance of other important predators (i.e. salmon), the significant impacts we predicted for the Cassin's auklet provide insights into the consequences that ocean climate change may have for other plankton predators in this system.     

Coralline algae (Rhodophyta) in a changing world: integrating ecological,physiological, and geochemical responses to global change

Coralline algae are globally distributed benthic primary producers that secrete calcium carbonate skeletons. In the context of ocean acidification, they have received much recent attention due to the potential vulnerability of their high‐Mg calcite skeletons and their many important ecological roles. Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including ocean acidification, rising temperatures, and pollution, on coralline algal growth and calcification. We also assess the ongoing use of coralline algae as marine climate proxies via calibration of skeletal morphology and geochemistry to environmental conditions. Finally, we indicate critical gaps in our understanding of coralline algal calcification and physiology and highlight key areas for future research. These include analytical areas that recently have become more accessible, such as resolving phylogenetic relationships at all taxonomic ranks, elucidating the genes regulating algal photosynthesis and calcification, and calibrating skeletal geochemical metrics, as well as research directions that are broadly applicable to global change ecology, such as the importance of community‐scale and long‐term experiments in stress response.