Ecosystem‐based management of coral reefs under climate change

Coral reefs provide food and livelihoods for hundreds of millions of people as well as harbour some of the highest regions of biodiversity in the ocean. However, overexploitation, land‐use change and other local anthropogenic threats to coral reefs have left many degraded. Additionally, coral reefs are faced with the dual emerging threats of ocean warming and acidification due to rising CO₂ emissions, with dire predictions that they will not survive the century. This review evaluates the impacts of climate change on coral reef organisms, communities and ecosystems, focusing on the interactions between climate change factors and local anthropogenic stressors. It then explores the shortcomings of existing management and the move towards ecosystem‐based management and resilience thinking, before highlighting the need for climate change‐ready marine protected areas (MPAs), reduction in local anthropogenic stressors, novel approaches such as human‐assisted evolution and the importance of sustainable socialecological systems. It concludes that designation of climate change‐ready MPAs, integrated with other management strategies involving stakeholders and participation at multiple scales such as marine spatial planning, will be required to maximise coral reef resilience under climate change. However, efforts to reduce carbon emissions are critical if the long‐term efficacy of local management actions is to be maintained and coral reefs are to survive.     

Incorporating climate change adaptation into marine protected area planning

Climate change is increasingly impacting marine protected areas (MPAs) and MPA networks, yet adaptation strategies are rarely incorporated into MPA design and management plans according to the primary scientific literature. Here we review the state of knowledge for adapting existing and future MPAs to climate change and synthesize case studies (n = 27) of how marine conservation planning can respond to shifting environmental conditions. First, we derive a generalized conservation planning framework based on five published frameworks that incorporate climate change adaptation to inform MPA design. We then summarize examples from the scientific literature to assess how conservation goals were defined, vulnerability assessments performed and adaptation strategies incorporated into the design and management of existing or new MPAs. Our analysis revealed that 82% of real‐world examples of climate change adaptation in MPA planning derive from tropical reefs, highlighting the need for research in other ecosystems and habitat types. We found contrasting recommendations for adaptation strategies at the planning stage, either focusing only on climate refugia, or aiming for representative protection of areas encompassing the full range of expected climate change impacts. Recommendations for MPA management were more unified and focused on adaptative management approaches. Lastly, we evaluate common barriers to adopting climate change adaptation strategies based on reviewing studies which conducted interviews with MPA managers and other conservation practitioners. This highlights a lack of scientific studies evaluating different adaptation strategies and shortcomings in current governance structures as two major barriers, and we discuss how these could be overcome. Our review provides a comprehensive synthesis of planning frameworks, case studies, adaptation strategies and management actions which can inform a more coordinated global effort to adapt existing and future MPA networks to continued climate change.     

Effects of high latitude protected areas on bird communities under rapid climate change

Anthropogenic climate change is rapidly becoming one of the main threats to biodiversity, along with other threats triggered by human‐driven land‐use change. Species are already responding to climate change by shifting their distributions polewards. This shift may create a spatial mismatch between dynamic species distributions and static protected areas (PAs). As protected areas represent one of the main pillars for preserving biodiversity today and in the future, it is important to assess their contribution in sheltering the biodiversity communities, they were designated to protect. A recent development to investigate climate‐driven impacts on biological communities is represented by the community temperature index (CTI). CTI provides a measure of the relative temperature average of a community in a specific assemblage. CTI value will be higher for assemblages dominated by warm species compared with those dominated by cold‐dwelling species. We here model changes in the CTI of Finnish bird assemblages, as well as changes in species densities, within and outside of PAs during the past four decades in a large boreal landscape under rapid change. We show that CTI has markedly increased over time across Finland, with this change being similar within and outside PAs and five to seven times slower than the temperature increase. Moreover, CTI has been constantly lower within than outside of PAs, and PAs still support communities, which show colder thermal index than those outside of PAs in the 1970s and 1980s. This result can be explained by the higher relative density of northern species within PAs than outside. Overall, our results provide some, albeit inconclusive, evidence that PAs may play a role in supporting the community of northern species. Results also suggest that communities are, however, shifting rapidly, both inside and outside of PAs, highlighting the need for adjusting conservation measures before it is too late.     

Forecasted coral reef decline in marine biodiversity hotspots under climate change

Coral bleaching events threaten coral reef habitats globally and cause severe declines of local biodiversity and productivity. Related to high sea surface temperatures (SST), bleaching events are expected to increase as a consequence of future global warming. However, response to climate change is still uncertain as future low‐latitude climatic conditions have no present‐day analogue. Sea surface temperatures during the Eocene epoch were warmer than forecasted changes for the coming century, and distributions of corals during the Eocene may help to inform models forecasting the future of coral reefs. We coupled contemporary and Eocene coral occurrences with information on their respective climatic conditions to model the thermal niche of coral reefs and its potential response to projected climate change. We found that under the RCP8.5 climate change scenario, the global suitability for coral reefs may increase up to 16% by 2100, mostly due to improved suitability of higher latitudes. In contrast, in its current range, coral reef suitability may decrease up to 46% by 2100. Reduction in thermal suitability will be most severe in biodiversity hotspots, especially in the Indo‐Australian Archipelago. Our results suggest that many contemporary hotspots for coral reefs, including those that have been refugia in the past, spatially mismatch with future suitable areas for coral reefs posing challenges to conservation actions under climate change.     

Non-climatic constraints on upper elevational plant range expansion under climate change

We are limited in our ability to predict climate-change-induced range shifts by our inadequate understanding of how non-climatic factors contribute to determining range limits along putatively climatic gradients. Here, we present a unique combination of observations and experiments demonstrating that seed predation and soil properties strongly limit regeneration beyond the upper elevational range limit of sugar maple, a tree species of major economic importance. Most strikingly, regeneration beyond the range limit occurred almost exclusively when seeds were experimentally protected from predators. Regeneration from seed was depressed on soil from beyond the range edge when this soil was transplanted to sites within the range, with indirect evidence suggesting that fungal pathogens play a role. Non-climatic factors are clearly in need of careful attention when attempting to predict the biotic consequences of climate change. At minimum, we can expect non-climatic factors to create substantial time lags between the creation of more favourable climatic conditions and range expansion.     

Temperature‐driven coral decline: the role of marine protected areas

Warming ocean temperatures are considered to be an important cause of the degradation of the world's coral reefs. Marine protected areas (MPAs) have been proposed as one tool to increase coral reef ecosystem resistance and resilience (i.e. recovery) to the negative effects of climate change, yet few studies have evaluated their efficacy in achieving these goals. We used a high resolution 4 km global temperature anomaly database from 1985–2005 and 8040 live coral cover surveys on protected and unprotected reefs to determine whether or not MPAs have been effective in mitigating temperature‐driven coral loss. Generally, protection in MPAs did not reduce the effect of warm temperature anomalies on coral cover declines. Shortcomings in MPA design, including size and placement, may have contributed to the lack of an MPA effect. Empirical studies suggest that corals that have been previously exposed to moderate levels of thermal stress have greater adaptive capacity and resistance to future thermal stress events. Existing MPAs protect relatively fewer reefs with moderate anomaly frequencies, potentially reducing their effectiveness. However, our results also suggest that the benefits from MPAs may not be great enough to offset the magnitude of losses from acute thermal stress events. Although MPAs are important conservation tools, their limitations in mitigating coral loss from acute thermal stress events suggest that they need to be complemented with policies aimed at reducing the activities responsible for climate change.     

Refugia under threat: Mass bleaching of coral assemblages in high‐latitude eastern Australia

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high‐latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage‐scale and genus‐level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long‐term mean temperatures during the hottest month of each year (SST_LTMAX), and annual fluctuations in water temperature (SST_VAR) and solar irradiance (PARZ_VAR). The most severely‐bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SST_LTMAX was low or PARZ_VAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally‐abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage‐scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage‐scale bleaching was associated with local differences in species abundance and taxon‐specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high‐latitude endemics, point to climate‐driven simplification of assemblage structures and progressive homogenisation of reef functions at these high‐latitude locations.     

The potential impacts of global climate change on marine protected areas

The potential effects of global climate changeon marine protected areas do not appear to havebeen addressed in the literature. This paperexamines the literature on protected areas,conservation biology, marine ecology,oceanography, and climate change, and reviewssome of the relevant differences between marineand terrestrial environments. Frameworks andclassifications systems used in protected areadesign are discussed. Finally, a frameworkthat summarizes some of the importantoceanographic processes and their links to thefood chain are reviewed. Species abundance anddistribution are expected to change as a resultof global climate change, potentiallycompromising the efficacy of marine protectedareas as biodiversity conservation tools. Thisreview suggests the need for: furtherinterdisciplinary research and the use oflinked models; an increase in marine protectedareas for biodiversity conservation and asresearch sites for teasing apart fishingeffects from climate effects; a temporallyresponsive approach to siting new marineprotected areas, shifting their locations ifnecessary; and large-scale ecosystem/integratedmanagement approaches to address the competinguses of the oceans and boundary-less threatssuch as global climate change and pollution.     

Model‐based conservation planning of the genetic diversity of Phellodendron amurense Rupr due to climate change

Climate change affects both habitat suitability and the genetic diversity of wild plants. Therefore, predicting and establishing the most effective and coherent conservation areas is essential for the conservation of genetic diversity in response to climate change. This is because genetic variance is a product not only of habitat suitability in conservation areas but also of efficient protection and management. Phellodendron amurense Rupr. is a tree species (family Rutaceae) that is endangered due to excessive and illegal harvesting for use in Chinese medicine. Here, we test a general computational method for the prediction of priority conservation areas (PCAs) by measuring the genetic diversity of P. amurense across the entirety of northeast China using a single strand repeat analysis of twenty microsatellite markers. Using computational modeling, we evaluated the geographical distribution of the species, both now and in different future climate change scenarios. Different populations were analyzed according to genetic diversity, and PCAs were identified using a spatial conservation prioritization framework. These conservation areas were optimized to account for the geographical distribution of P. amurense both now and in the future, to effectively promote gene flow, and to have a long period of validity. In situ and ex situ conservation, strategies for vulnerable populations were proposed. Three populations with low genetic diversity are predicted to be negatively affected by climate change, making conservation of genetic diversity challenging due to decreasing habitat suitability. Habitat suitability was important for the assessment of genetic variability in existing nature reserves, which were found to be much smaller than the proposed PCAs. Finally, a simple set of conservation measures was established through modeling. This combined molecular and computational ecology approach provides a framework for planning the protection of species endangered by climate change.     

Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change

Poleward range expansions are widespread responses to recent climate change and are crucial for the future persistence of many species. However, evolutionary change in traits such as colonization history and habitat preference may also be necessary to track environmental change across a fragmented landscape. Understanding the likelihood and speed of such adaptive change is important in determining the rate of species extinction with ongoing climate change. We conducted an amplified fragment length polymorphism (AFLP)‐based genome scan across the recently expanded UK range of the Brown Argus butterfly, Aricia agestis, and used outlier‐based (DFDIST and BayeScan) and association‐based (Isolation‐By‐Adaptation) statistical approaches to identify signatures of evolutionary change associated with range expansion and habitat use. We present evidence for (i) limited effects of range expansion on population genetic structure and (ii) strong signatures of selection at approximately 5% AFLP loci associated with both the poleward range expansion of A. agestis and differences in habitat use across long‐established and recently colonized sites. Patterns of allele frequency variation at these candidate loci suggest that adaptation to new habitats at the range margin has involved selection on genetic variation in habitat use found across the long‐established part of the range. Our results suggest that evolutionary change is likely to affect species’ responses to climate change and that genetic variation in ecological traits across species’ distributions should be maximized to facilitate range shifts across a fragmented landscape, particularly in species that show strong associations with particular habitats.     

Spatio‐temporal variation of biotic factors underpins contemporary range dynamics of congeners

Species’ ranges are complex often exhibiting multidirectional shifts over space and time. Despite the strong fingerprint of recent historical climate change on species’ distributions, biotic factors such as loss of vegetative habitat and the presence of potential competitors constitute important yet often overlooked drivers of range dynamics. Furthermore, short‐term changes in environmental conditions can influence the underlying processes of local extinction and local colonization that drive range shifts, yet are rarely considered at broad scales. We used dynamic state‐space occupancy models to test multiple hypotheses of the relative importance of major drivers of range shifts of Golden‐winged Warblers (Vermivora chrysoptera) and Blue‐winged Warblers (V. cyanoptera) between 1983 and 2012 across North America: warming temperatures; habitat changes; and occurrence of congeneric species, used here as proxy for biotic interactions. Dynamic occupancies for both species were most influenced by spatial relative to temporal variation in temperature and habitat. However, temporal variation in temperature anomalies and biotic interactions remained important. The two biotic factors considered, habitat change and biotic interactions, had the largest relative effect on estimated extinction rates followed by abiotic temperature anomalies. For the Golden‐winged Warbler, the predicted presence of the Blue‐winged Warbler, a hypothesized competitor, most influenced extinction probabilities, contributing to evidence supporting its role in site‐level species replacement. Given the overall importance of biotic factors on range‐wide dynamic occupancies, their consideration alongside abiotic factors should not be overlooked. Our results suggest that warming compounds the negative effect of habitat loss emphasizing species’ need for habitat to adapt to a changing climate. Notably, even closely related species exhibited individual responses to abiotic and biotic factors considered.     

Winter climate change and the poleward range expansion of a tropical invasive tree (Brazilian pepper—Schinus terebinthifolius)

Winter climate change is expected to lead to the tropicalization of temperate ecosystems, where tropical species expand poleward in response to a decrease in the intensity and duration of winter temperature extremes (i.e., freeze events). In the southeastern United States, freezing temperatures control the northern range limits of many invasive nonnative species. Here, we examine the influence of freezing temperatures and winter climate change on the northern range limits of an invasive nonnative tree—Schinus terebinthifolius (Brazilian pepper). Since introduction in the 1800s, Brazilian pepper has invaded ecosystems throughout south and central Florida to become the state's most widespread nonnative plant species. Although Brazilian pepper is sensitive to freezing temperatures, temperature controls on its northern distribution have not been adequately quantified. We used temperature and plant occurrence data to quantify the sensitivity of Brazilian pepper to freezing temperatures. Then, we examined the potential for range expansion under three alternative future climate scenarios (+2°C, +4°C, and +6°C). Our analyses identify a strong nonlinear sigmoidal relationship between minimum temperature and Brazilian pepper presence, with a discrete threshold temperature occurring near ?11°C. Our future scenario analyses indicate that, in response to warming winter temperatures, Brazilian pepper is expected to expand northward and transform ecosystems in north Florida and across much of the Gulf of Mexico and south Atlantic coasts of the United States. These results underscore the importance of early detection and rapid response efforts to identify and manage the northward invasion of Brazilian pepper in response to climate change. Looking more broadly, our work highlights the need to anticipate and prepare for the tropicalization of temperate ecosystems by tropical invasive species.     

Scale‐dependent complementarity of climatic velocity and environmental diversity for identifying priority areas for conservation under climate change

As most regions of the earth transition to altered climatic conditions, new methods are needed to identify refugia and other areas whose conservation would facilitate persistence of biodiversity under climate change. We compared several common approaches to conservation planning focused on climate resilience over a broad range of ecological settings across North America and evaluated how commonalities in the priority areas identified by different methods varied with regional context and spatial scale. Our results indicate that priority areas based on different environmental diversity metrics differed substantially from each other and from priorities based on spatiotemporal metrics such as climatic velocity. Refugia identified by diversity or velocity metrics were not strongly associated with the current protected area system, suggesting the need for additional conservation measures including protection of refugia. Despite the inherent uncertainties in predicting future climate, we found that variation among climatic velocities derived from different general circulation models and emissions pathways was less than the variation among the suite of environmental diversity metrics. To address uncertainty created by this variation, planners can combine priorities identified by alternative metrics at a single resolution and downweight areas of high variation between metrics. Alternately, coarse‐resolution velocity metrics can be combined with fine‐resolution diversity metrics in order to leverage the respective strengths of the two groups of metrics as tools for identification of potential macro‐ and microrefugia that in combination maximize both transient and long‐term resilience to climate change. Planners should compare and integrate approaches that span a range of model complexity and spatial scale to match the range of ecological and physical processes influencing persistence of biodiversity and identify a conservation network resilient to threats operating at multiple scales.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

Change and stasis in marine hybrid zones in response to climate warming

Aim We test the prediction that hybrid zones between warm‐ and cold‐adapted species will move towards the territory formerly occupied by the cold‐adapted species in response to a warming climate. We use multiple tests of this prediction to distinguish amongst potential mechanistic hypotheses of responses to climate change. Location We sampled 97 locations on the Atlantic coast of Spain and France and the English Channel that span three hybrid zones formed between two species of marine mussels (Mytilus galloprovincialis and M. edulis). Methods Mussels were sampled in 2005–07 and analysed at a nuclear gene (Glu‐5′) that is diagnostically differentiated between the subject species. Results were compared to those of studies made in the same region over the past two decades. Historical change in sea surface temperature (SST) was analysed using National Oceanic and Atmospheric Administration (NOAA) Optimum Interpolation Daily SST. Species distribution models (random forest and maximum entropy) of the current distribution of mussels were constructed and validated by hindcasting the historical distributions of these species. Validated models were used in combination with forecasts of SST to predict changes in mussel distribution to 2050 and 2100. Results We show that over the past two decades two of the hybrid zones in France have not changed in either position or shape. The third hybrid zone, however, has shifted in the predicted direction, c. 100 km eastward into the warming English Channel. Species distribution modelling strongly implicates changes in winter cold SST as driving this change in the position of one of the hybrid zones. Forecasts of future SST indicate that rapid changes in distribution will occur over the next century. Main conclusions Hybrid zones can be used to conduct repeated tests of ecological responses to climate change and can be valuable in sorting among prospective mechanistic hypotheses that underlie that change. Winter temperatures, but not seasonal high temperature, appear to control the distribution of both species. Species distribution modelling indicates that the collapse of these hybrid zones is imminent, with the rapid expansion of the subtropical species in response to continuing SST warming.     

Applying a framework for landscape planning under climate change for the conservation of biodiversity in the Finnish boreal forest

Conservation strategies are often established without consideration of the impact of climate change. However, this impact is expected to threaten species and ecosystem persistence and to have dramatic effects towards the end of the 21st century. Landscape suitability for species under climate change is determined by several interacting factors including dispersal and human land use. Designing effective conservation strategies at regional scales to improve landscape suitability requires measuring the vulnerabilities of specific regions to climate change and determining their conservation capacities. Although methods for defining vulnerability categories are available, methods for doing this in a systematic, cost‐effective way have not been identified. Here, we use an ecosystem model to define the potential resilience of the Finnish forest landscape by relating its current conservation capacity to its vulnerability to climate change. In applying this framework, we take into account the responses to climate change of a broad range of red‐listed species with different niche requirements. This framework allowed us to identify four categories in which representation in the landscape varies among three IPCC emission scenarios (B1, low; A1B, intermediate; A2, high emissions): (i) susceptible (B1 = 24.7%, A1B = 26.4%, A2 = 26.2%), the most intact forest landscapes vulnerable to climate change, requiring management for heterogeneity and resilience; (ii) resilient (B1 = 2.2%, A1B = 0.5%, A2 = 0.6%), intact areas with low vulnerability that represent potential climate refugia and require conservation capacity maintenance; (iii) resistant (B1 = 6.7%, A1B = 0.8%, A2 = 1.1%), landscapes with low current conservation capacity and low vulnerability that are suitable for restoration projects; (iv) sensitive (B1 = 66.4%, A1B = 72.3%, A2 = 72.0%), low conservation capacity landscapes that are vulnerable and for which alternative conservation measures are required depending on the intensity of climate change. Our results indicate that the Finnish landscape is likely to be dominated by a very high proportion of sensitive and susceptible forest patches, thereby increasing uncertainty for landscape managers in the choice of conservation strategies.     

Evidence that climate sets the lower elevation range limit in a high‐elevation endemic salamander

A frequent assumption in ecology is that biotic interactions are more important than abiotic factors in determining lower elevational range limits (i.e., the “warm edge” of a species distribution). However, for species with narrow environmental tolerances, theory suggests the presence of a strong environmental gradient can lead to persistence, even in the presence of competition. The relative importance of biotic and abiotic factors is rarely considered together, although understanding when one exerts a dominant influence on controlling range limits may be crucial to predicting extinction risk under future climate conditions. We sampled multiple transects spanning the elevational range limit of Plethodon shenandoah and site and climate covariates were recorded. A two‐species conditional occupancy model, accommodating heterogeneity in detection probability, was used to relate variation in occupancy with environmental and habitat conditions. Regional climate data were combined with datalogger observations to estimate the cloud base heights and to project future climate change impacts on cloud elevations across the survey area. By simultaneously accounting for species’ interactions and habitat variables, we find that elevation, not competition, is strongly correlated with the lower elevation range boundary, which had been presumed to be restricted mainly as a result of competitive interactions with a congener. Because the lower elevational range limit is sensitive to climate variables, projected climate change across its high‐elevation habitats will directly affect the species’ distribution. Testing assumptions of factors that set species range limits should use models which accommodate detection biases.