Coral Reef Habitat Response to Climate Change Scenarios

Coral reef ecosystems are threatened by both climate change and direct anthropogenic stress. Climate change will alter the physico-chemical environment that reefs currently occupy, leaving only limited regions that are conducive to reef habitation. Identifying these regions early may aid conservation efforts and inform decisions to transplant particular coral species or groups. Here a species distribution model (Maxent) is used to describe habitat suitable for coral reef growth. Two climate change scenarios (RCP4.5, RCP8.5) from the National Center for Atmospheric Research’s Community Earth System Model were used with Maxent to determine environmental suitability for corals (order Scleractinia). Environmental input variables best at representing the limits of suitable reef growth regions were isolated using a principal component analysis. Climate-driven changes in suitable habitat depend strongly on the unique region of reefs used to train Maxent. Increased global habitat loss was predicted in both climate projections through the 21^st century. A maximum habitat loss of 43% by 2100 was predicted in RCP4.5 and 82% in RCP8.5. When the model is trained solely with environmental data from the Caribbean/Atlantic, 83% of global habitat was lost by 2100 for RCP4.5 and 88% was lost for RCP8.5. Similarly, global runs trained only with Pacific Ocean reefs estimated that 60% of suitable habitat would be lost by 2100 in RCP4.5 and 90% in RCP8.5. When Maxent was trained solely with Indian Ocean reefs, suitable habitat worldwide increased by 38% in RCP4.5 by 2100 and 28% in RCP8.5 by 2050. Global habitat loss by 2100 was just 10% for RCP8.5. This projection suggests that shallow tropical sites in the Indian Ocean basin experience conditions today that are most similar to future projections of worldwide conditions. Indian Ocean reefs may thus be ideal candidate regions from which to select the best strands of coral for potential re-seeding efforts.     

Climate‐change refugia: shading reef corals by turbidity

Coral reefs have recently experienced an unprecedented decline as the world's oceans continue to warm. Yet global climate models reveal a heterogeneously warming ocean, which has initiated a search for refuges, where corals may survive in the near future. We hypothesized that some turbid nearshore environments may act as climate‐change refuges, shading corals from the harmful interaction between high sea‐surface temperatures and high irradiance. We took a hierarchical Bayesian approach to determine the expected distribution of 12 coral species in the Indian and Pacific Oceans, between the latitudes 37°N and 37°S, under representative concentration pathway 8.5 (W m^?2) by 2100. The turbid nearshore refuges identified in this study were located between latitudes 20–30°N and 15–25°S, where there was a strong coupling between turbidity and tidal fluctuations. Our model predicts that turbidity will mitigate high temperature bleaching for 9% of shallow reef habitat (to 30 m depth) – habitat that was previously considered inhospitable under ocean warming. Our model also predicted that turbidity will protect some coral species more than others from climate‐change‐associated thermal stress. We also identified locations where consistently high turbidity will likely reduce irradiance to <250 μmol m^?2 s^?1, and predict that 16% of reef‐coral habitat ≤30 m will preclude coral growth and reef development. Thus, protecting the turbid nearshore refuges identified in this study, particularly in the northwestern Hawaiian Islands, the northern Philippines, the Ryukyu Islands (Japan), eastern Vietnam, western and eastern Australia, New Caledonia, the northern Red Sea, and the Arabian Gulf, should become part of a judicious global strategy for reef‐coral persistence under climate change.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

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.     

Elucidating the sponge stress response; lipids and fatty acids can facilitate survival under future climate scenarios

Ocean warming (OW) and ocean acidification (OA) are threatening coral reef ecosystems, with a bleak future forecast for reef‐building corals, which are already experiencing global declines in abundance. In contrast, many coral reef sponge species are able to tolerate climate change conditions projected for 2100. To increase our understanding of the mechanisms underpinning this tolerance, we explored the lipid and fatty acid (FA) composition of four sponge species with differing sensitivities to climate change, experimentally exposed to OW and OA levels predicted for 2100, under two CO₂ Representative Concentration Pathways. Sponges with greater concentrations of storage lipid, phospholipids, sterols and elevated concentrations of n‐3 and n‐6 long‐chain polyunsaturated FA (LC PUFA), were more resistant to OW. Such biochemical constituents likely contribute to the ability of these sponges to maintain membrane function and cell homeostasis in the face of environmental change. Our results suggest that n‐3 and n‐6 LC PUFA are important components of the sponge stress response potentially via chain elongation and the eicosanoid stress‐signalling pathways. The capacity for sponges to compositionally alter their membrane lipids in response to stress was also explored using a number of specific homeoviscous adaptation (HVA) indicators. This revealed a potential mechanism via which additional CO₂ could facilitate the resistance of phototrophic sponges to thermal stress through an increased synthesis of membrane‐stabilizing sterols. Finally, OW induced an increase in FA unsaturation in phototrophic sponges but a decrease in heterotrophic species, providing support for a difference in the thermal response pathway between the sponge host and the associated photosymbionts. Here we have shown that sponge lipids and FA are likely to be an important component of the sponge stress response and may play a role in facilitating sponge survival under future climate conditions.     

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.     

Thermal history influences lesion recovery of the threatened Caribbean staghorn coral Acropora cervicornis under heat stress

Anthropogenic climate change is the biggest threat to coral reefs, but reef restoration efforts are buying time for these ecosystems. Lesion recovery, which can be a determinant of colony survival, is particularly important for restored species. Here, we evaluate lesion recovery of 18 genets of Acropora cervicornis from Florida reefs with different thermal regimes in a temperature challenge experiment. Genets demonstrated significant variability in healing, which greatly slowed under heat stress. Only 35% of fragments healed at 31.5 °C compared to 99% at 28 °C. Donor reef thermal regime significantly influenced lesion recovery under heat stress with corals from warmer reefs demonstrating greater healing than corals from cooler reefs, but did not influence recovery under ambient conditions. These findings should encourage practitioners to utilize rapidly healing genets, avoid fragmentation in high temperatures, and incorporate assisted relocation by moving corals from warmer to cooler reefs, where they might succeed under future climate conditions.

     

Escaping the heat: range shifts of reef coral taxa in coastal Western Australia

One of the most critical challenges facing ecologists today is to understand the changing geographic distribution of species in response to current and predicted global warming. Coastal Western Australia is a natural laboratory in which to assess the effect of climate change on reef coral communities over a temporal scale unavailable to studies conducted solely on modern communities. Reef corals composing Late Pleistocene reef assemblages exposed at five distinct localities along the west Australian coast were censused and the results compared with coral occurrence data published for the modern reefs offshore of each locality. The resulting comparative data set comprises modern and Late Pleistocene reef coral communities occurring over approximately 12° of latitude. For the modern reefs this gradient includes the zone of overlap between the Dampierian and Flindersian Provinces. Modern reef coral communities show a pronounced gradient in coral composition over the latitudinal range encompassed by the study, while the gradient in community composition is not as strong for Pleistocene communities. Tropical‐adapted taxa contracted their ranges north since Late Pleistocene time, emplacing two biogeographic provinces in a region in which a single province had existed previously. Beta diversity values for adjacent communities also reflect this change. Modern reefs show a distinct peak in beta diversity in the middle of the region; the peak is not matched by Pleistocene reefs. Beta diversity is correlated with distance only for comparisons between modern reefs in the north and the fossil assemblages, further supporting change in distribution of the biogeographic provinces in the study area. Coral taxa present in modern communities clearly expanded and contracted their geographic ranges in response to climate change. Those taxa that distinguish Pleistocene from modern reefs are predicted to migrate south in response to future climate change, and potentially persist in ‘temperature refugia’ as tropical reef communities farther north decline.     

Regional and global climate risks for reef corals: Incorporating species-specific vulnerability and exposure to climate hazards

Climate change is driving rapid and widespread erosion of the environmental conditions that formerly supported species persistence. Existing projections of climate change typically focus on forecasts of acute environmental anomalies and global extinction risks. The current projections also frequently consider all species within a broad taxonomic group together without differentiating species-specific patterns. Consequently, we still know little about the explicit dimensions of climate risk (i.e., species-specific vulnerability, exposure and hazard) that are vital for predicting future biodiversity responses (e.g., adaptation, migration) and developing management and conservation strategies. Here, we use reef corals as model organisms (n = 741 species) to project the extent of regional and global climate risks of marine organisms into the future. We characterise species-specific vulnerability based on the global geographic range and historical environmental conditions (1900–1994) of each coral species within their ranges, and quantify the projected exposure to climate hazard beyond the historical conditions as climate risk. We show that many coral species will experience a complete loss of pre-modern climate analogs at the regional scale and across their entire distributional ranges, and such exposure to hazardous conditions are predicted to pose substantial regional and global climate risks to reef corals. Although high-latitude regions may provide climate refugia for some tropical corals until the mid-21st century, they will not become a universal haven for all corals. Notably, high-latitude specialists and species with small geographic ranges remain particularly vulnerable as they tend to possess limited capacities to avoid climate risks (e.g., via adaptive and migratory responses). Predicted climate risks are amplified substantially under the SSP5-8.5 compared with the SSP1-2.6 scenario, highlighting the need for stringent emission controls. Our projections of both regional and global climate risks offer unique opportunities to facilitate climate action at spatial scales relevant to conservation and management.     

New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies

The mutualistic symbioses between reef‐building corals and micro‐algae form the basis of coral reef ecosystems, yet recent environmental changes threaten their survival. Diversity in host‐symbiont pairings on the sub‐species level could be an unrecognized source of functional variation in response to stress. The Caribbean elkhorn coral, Acropora palmata, associates predominantly with one symbiont species (Symbiodinium ‘fitti’), facilitating investigations of individual‐level (genotype) interactions. Individual genotypes of both host and symbiont were resolved across the entire species’ range. Most colonies of a particular animal genotype were dominated by one symbiont genotype (or strain) that may persist in the host for decades or more. While Symbiodinium are primarily clonal, the occurrence of recombinant genotypes indicates sexual recombination is the source of this genetic variation, and some evidence suggests this happens within the host. When these data are examined at spatial scales spanning the entire distribution of A. palmata, gene flow among animal populations was an order of magnitude greater than among populations of the symbiont. This suggests that independent micro‐evolutionary processes created dissimilar population genetic structures between host and symbiont. The lower effective dispersal exhibited by the dinoflagellate raises questions regarding the extent to which populations of host and symbiont can co‐evolve during times of rapid and substantial climate change. However, these findings also support a growing body of evidence, suggesting that genotype‐by‐genotype interactions may provide significant physiological variation, influencing the adaptive potential of symbiotic reef corals to severe selection.     

Paradise lost: End‐of‐century warming and acidification under business‐as‐usual emissions have severe consequences for symbiotic corals

Despite recent efforts to curtail greenhouse gas emissions, current global emission trajectories are still following the business‐as‐usual representative concentration pathway (RCP) 8.5 emission pathway. The resulting ocean warming and acidification have transformative impacts on coral reef ecosystems, detrimentally affecting coral physiology and health, and these impacts are predicted to worsen in the near future. In this study, we kept fragments of the symbiotic corals Acropora intermedia (thermally sensitive) and Porites lobata (thermally tolerant) for 7 weeks under an orthogonal design of predicted end‐of‐century RCP8.5 conditions for temperature and pCO₂ (3.5°C and 570 ppm above present‐day, respectively) to unravel how temperature and acidification, individually or interactively, influence metabolic and physiological performance. Our results pinpoint thermal stress as the dominant driver of deteriorating health in both species because of its propensity to destabilize coral–dinoflagellate symbiosis (bleaching). Acidification had no influence on metabolism but had a significant negative effect on skeleton growth, particularly when photosynthesis was absent such as in bleached corals or under dark conditions. Total loss of photosynthesis after bleaching caused an exhaustion of protein and lipid stores and collapse of calcification that ultimately led to A. intermedia mortality. Despite complete loss of symbionts from its tissue, P. lobata maintained small amounts of photosynthesis and experienced a weaker decline in lipid and protein reserves that presumably contributed to higher survival of this species. Our results indicate that ocean warming and acidification under business‐as‐usual CO₂ emission scenarios will likely extirpate thermally sensitive coral species before the end of the century, while slowing the recovery of more thermally tolerant species from increasingly severe mass coral bleaching and mortality. This could ultimately lead to the gradual disappearance of tropical coral reefs globally, and a shift on surviving reefs to only the most resilient coral species.     

Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals

Acropora is the most diverse genus of reef-building corals in the world today. It occurs in all three major oceans; it is restricted to latitudes 31 degrees N-31 degrees S, where most coral reefs occur, and reaches greatest diversity in the central Indo-Pacific. As an exemplar genus, the long-term history of Acropora has implications for the evolution and origins of present day biodiversity patterns of reef corals and for predicting their response to future climate change. Diversification of Acropora was thought to have occurred in the central Indo-Pacific within the previous two million years. We examined Eocene fossils from southern England and northern France and found evidence that precursors of up to nine of 20 currently recognized Acropora species groups existed 49-34 Myr, at palaeolatitudes far higher than current limits, to 51 degrees N. We propose that pre-existing diversity contributed to later rapid speciation in this important functional group of corals.     

How Quickly do Fragments of Coral “Self‐Attach” after Transplantation?

Transplantation of coral fragments is seen as a potential method to rapidly restore coral cover to areas of degraded reef; however, considerable research is still needed to assess the effectiveness of coral transplantation as a viable reef restoration tool. Initially, during restoration efforts, coral transplants are attached artificially. Self‐attachment (i.e., growth of coral tissue onto the substrate) provides a more secure and lasting bond, thus knowledge about self‐attachment times for corals is of importance to reef restoration. While it is known that coral fragments may generate new tissue and bond to substrata within a few weeks of transplantation, surprisingly little is known about the speed of self‐attachment for most species. Two independent experiments were carried out to examine the self‐attachment times of 12 scleractinian and one non‐scleractinian coral species to a natural calcium carbonate substrate. The first experiment examined times to self‐attachment in 11 species of differing morphologies from seven families over approximately 7 months, whereas the second experiment examined three fast‐attaching Acropora species over approximately 1 month. In the first experiment, the branching species Acropora muricata had a significantly faster self‐attachment time compared to all other species, while Echinopora lamellosa had the slowest self‐attachment time. For the second experiment, A. muricata was significantly slower to self‐attach than Acropora hyacinthus (tabular) and Acropora digitifera (corymbose‐digitate). The results suggest that a combination of factors including growth rates, growth form and life history may determine how quickly fragments of coral species self‐attach after fragmentation and transplantation.     

Associations between climate stress and coral reef diversity in the western Indian Ocean

Climatic–oceanographic stress and coral reef diversity were mapped in the western Indian Ocean (WIO) in order to determine if there were associations between high diversity coral reefs and regions with low‐to‐moderate climate stress. A multivariate stress model developed to estimate environmental exposure to stress, an empirical index of the coral community's susceptibility to stress, and field data on numbers of fish and corals taxa from 197 WIO sites were overlain to evaluate these associations. Exposure to stress was modeled from satellite data based on nine geophysical–biological oceanographic characteristics known to influence coral bleaching (i.e. temperature, light, and current variables). The environmental stress model and the coral community's susceptibility index were moderately correlated (r=?0.51) with southern and eastern parts of the WIO identified as areas with low environmental stress and coral communities with greater dominance of bleaching stress‐sensitive taxa. Numbers of coral and fish taxa were positive and moderately correlated (r=0.47) but high diversity regions for fish were in the north and west while diversity was highest for corals in central regions from Tanzania to northwestern Madagascar. Combining three and four of these variables into composite maps identified a region from southern Kenya to northern Mozambique across to northern–eastern Madagascar and the Mascarene Islands and the Mozambique–South Africa border as areas where low‐moderate environmental exposure overlaps with moderate‐high taxonomic diversity. In these areas management efforts aimed at maintaining high‐diversity and intact ecosystems are considered least likely to be undermined by climate disturbances in the near term. Reducing additional human disturbances, such as fishing and pollution, in these areas is expected to improve the chances for their persistence. These reefs are considered a high priority for increased local, national, and international management efforts aimed at establishing coral reef refugia for climate change impacts.     

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.     

Hypoxia tolerance and air-breathing ability correlate with habitat preference in coral-dwelling fishes

Hypoxia tolerance and air-breathing occur in a range of freshwater, estuarine and intertidal fishes. Here it is shown for the first time that coral reef fishes from the genera Gobiodon, Paragobiodon and Caracanthus, which all have an obligate association with living coral, also exhibit hypoxia tolerance and a well-developed air-breathing capacity. All nine species maintained adequate respiration in water at oxygen concentrations down to 15–25% air saturation. This hypoxia tolerance is probably needed when the oxygen levels in the coral habitat drops sharply at night. Air-breathing abilities of the species correlated with habitat association, being greatest (equaling oxygen uptake in water) in species that occupy corals extending into shallow water, where they may become air exposed during extreme low tides. Air-breathing was less well-developed or absent in species inhabiting corals from deeper waters. Loss of scales and a network of subcutaneous capillaries appear to be key adaptations allowing cutaneous respiration in air. While hypoxia tolerance may be an ancestral trait in these fishes, air-breathing is likely to be a more recent adaptation exemplifying convergent evolution in the unrelated genera Gobiodon and Caracanthus in response to coral-dwelling lifestyles.     

Archetypal ‘elkhorn’ coral discovered in the Pacific Ocean

The discovery of a population of elkhorn corals in the Central Pacific Ocean has important taxonomic implications, as this distinctive colony morphology was previously known only from the endemic and critically endangered Atlantic species Acropora palmata. Phylogenetic analyses confirmed that the Pacific elkhorn coral is genetically distant from A. palmata, and most likely represents a species previously synonymized with Acropora abrotanoides. The Pacific elkhorn coral is rare, and is of particular scientific interest because it represents one morphological extreme in the dominant genus of reef-building corals. The discovery of the Pacific elkhorn coral raises a number of important general issues in relation to biodiversity conservation, as this coral would not qualify for threatened species listing under current IUCN categories and criteria despite being demonstrably rare.     

Bommies away! Logistics and early effects of repositioning 400 tonnes of displaced coral colonies following cyclone impacts on the Great Barrier Reef

For over 40 years, management of the Great Barrier Reef Marine Park (GBRMP) in Australia has focused on limiting human‐use impacts to facilitate natural resilience and recovery. Compounding acute disturbances and chronic stressors have resulted in degradation of coral reef habitats in many areas of the Marine Park. Given current trends and predictions of escalating climate‐driven disturbances, it is increasingly evident that effective management of the GBRMP requires adaptive and novel approaches to protect and restore coral reef health. Here, we provide an overview of the logistical requirements and early‐stage ecological benefits of repositioning 400 tonnes of moderately sized (1–3 m diameter) Porites spp. coral colonies (bommies) that were displaced by cyclone‐generated swells that impacted reefs in the Whitsunday Islands during March 2017. An ecological survey conducted 16 months after the bommie repositioning revealed that several genera of hard coral had settled onto the bommies and that a range of reef fish species were associating with the restored habitat. Early findings suggest that the repositioning of the displaced bommies has assisted in restoring reef habitat structure and settlement habitat for juvenile corals, while improving natural aesthetics, vessel access and tourist experiences at Manta Ray Bay.