Mia O. Hoogenboom

Global warming and recurrent mass bleaching of corals

During 2015–2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene

Not enough time for recovery Coral bleaching occurs when stressful conditions result in the expulsion of the algal partner from the coral. Before anthropogenic climate warming, such events were relatively rare, allowing for recovery of the reef between events. Hughes et al. looked at 100 reefs globally and found that the average interval between bleaching events is now less than half what it was before. Such narrow recovery windows do not allow for full recovery. Furthermore, warming events such as El Niño are warmer than previously, as are general ocean conditions. Such changes are likely to make it more and more difficult for reefs to recover between stressful events. Science, this issue p. 80 Coral reefs in the present day have less time than in earlier periods to recover from bleaching events. Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño–Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.

Water Contamination Reduces the Tolerance of Coral Larvae to Thermal Stress

Coral reefs are highly susceptible to climate change, with elevated sea surface temperatures (SST) posing one of the main threats to coral survival. Successful recruitment of new colonies is important for the recovery of degraded reefs following mortality events. Coral larvae require relatively uncontaminated substratum on which to metamorphose into sessile polyps, and the increasing pollution of coastal waters therefore constitutes an additional threat to reef resilience. Here we develop and analyse a model of larval metamorphosis success for two common coral species to quantify the interactive effects of water pollution (copper contamination) and SST. We identify thresholds of temperature and pollution that prevent larval metamorphosis, and evaluate synergistic interactions between these stressors. Our analyses show that halving the concentration of Cu can protect corals from the negative effects of a 2–3°C increase in SST. These results demonstrate that effective mitigation of local impacts can reduce negative effects of global stressors.

Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa.

SUMMARY This study quantifies the relative contributions of autotrophy and heterotrophy to the energy budget of the temperate scleractinian species Cladocora caespitosa Linnaeus 1767. Colonies were incubated under different light and feeding regimes, and changes in carbon acquisition through photosynthesis and feeding were measured during a 2-month time period. This approach allowed us to quantify the rate at which adjustments to physiology occurred, as well as the magnitude of up- or downregulation of both feeding modes. In addition, we explored how shifts in carbon acquisition mode influenced tissue biomass (protein content), energy stores (lipid content) and colony growth (calcification). Increases in feeding capacity during prolonged exposure to darkness were correlated with decreases in photosynthetic capacity. However, feeding effort did not decrease when photosynthesis was high. In fact, feeding was maximal under high light conditions when food was not available. During starvation, colonies used their lipid stores to partially meet their metabolic requirements. Colonies kept in low light used nutrients from feeding to supplement calcification, whereas those kept at high light converted carbon from feeding into tissue biomass. This work provides the first estimates of rates of adjustment of heterotrophic feeding capacity in a Mediterranean scleractinian coral. For the study species, flexibility in carbon acquisition through heterotrophy was approximately equal to flexibility in photosynthesis both in magnitude and in the rate at which physiological adjustments occurred. The ability to alter feeding effort rapidly and strongly may explain the wide depth distribution of C. caespitosa, and its ability to survive in turbid coastal waters where light is often limited.

INTERACTIONS BETWEEN MORPHOLOGICAL AND PHYSIOLOGICAL PLASTICITY OPTIMIZE ENERGY ACQUISITION IN CORALS

Morphological plasticity in response to environmental heterogeneity may be performance enhancing or may simply result from an intrinsic instability in morphology during development. Although patterns of morphological change are well documented for numerous taxa, it is often unclear whether this plasticity enhances the performance of organisms in the habitat to which they have acclimatized. Reef-building corals are an ideal model system in which to investigate this question. We here develop a three-dimensional geometric model and present a comprehensive photosynthesis data set with experimentally calibrated photosynthesis models that predicts energy acquisition by foliose corals as a function of colony shape. This allows us to assess the extent to which changes in colony morphology along an environmental gradient track the predicted optimal colony morphologies. Our results provide strong evidence that phenotypic plasticity in foliose corals optimizes photosynthetic energy acquisition and is not simply a mechanism to increase light capture. We show that the optimal morphology is constrained at the boundaries of the environmental gradient, with non-optimal morphologies in these habitats having greatly reduced energy acquisition. However, at the center of the environmental gradient, flexibility in photophysiology allows energy acquisition to be very similar for multiple morphologies. Our results highlight the importance of phenotypic plasticity at multiple scales. Variation in overall morphology is important at niche boundaries at which conditions are consistently more stressful, whereas physiological flexibility is important in intermediate and less predictable habitats in which a rapid and reversible response to environmental fluctuations is required.

Effects of Light, Food Availability and Temperature Stress on the Function of Photosystem II and Photosystem I of Coral Symbionts

Background Reef corals are heterotrophic coelenterates that achieve high productivity through their photosynthetic dinoflagellate symbionts. Excessive seawater temperature destabilises this symbiosis and causes corals to “bleach,” lowering their photosynthetic capacity. Bleaching poses a serious threat to the persistence of coral reefs on a global scale. Despite expanding research on the causes of bleaching, the mechanisms remain a subject of debate. Methodology/Principal Findings This study determined how light and food availability modulate the effects of temperature stress on photosynthesis in two reef coral species. We quantified the activities of Photosystem II, Photosystem I and whole chain electron transport under combinations of normal and stressful growth temperatures, moderate and high light levels and the presence or absence of feeding of the coral hosts. Our results show that PS1 function is comparatively robust against temperature stress in both species, whereas PS2 and whole chain electron transport are susceptible to temperature stress. In the symbiotic dinoflagellates of Stylophora pistillata the contents of chlorophyll and major photosynthetic complexes were primarily affected by food availability. In Turbinaria reniformis growth temperature was the dominant influence on the contents of the photosynthetic complexes. In both species feeding the host significantly protected photosynthetic function from high temperature stress. Conclusions/Significance Our findings support the photoinhibition model of coral bleaching and demonstrate that PS1 is not a major site for thermal damage during bleaching events. Feeding mitigates bleaching in two scleractinian corals, so that reef responses to temperature stresses will likely be influenced by the coinciding availabilities of prey for the host.

Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa

This study quantified variation in net photosynthetic carbon gain in response to natural fluctuations in symbiont density for the Mediterranean coral Cladocora caespitosa, and evaluated which density maximized photosynthetic carbon acquisition. To do this, carbon acquisition was modeled as an explicit function of symbiont density. The model was parameterized using measurements of rates of photosynthesis and respiration for small colonies with a broad range of zooxanthella concentrations. Results demonstrate that rates of net photosynthesis increase asymptotically with symbiont density, whereas rates of respiration increase linearly. In combination, these functional responses meant that colony energy acquisition decreased at both low and at very high zooxanthella densities. However, there was a wide range of symbiont densities for which net daily photosynthesis was approximately equivalent. Therefore, significant changes in symbiont density do not necessarily cause a change in autotrophic energy acquisition by the colony. Model estimates of the optimal range of cell densities corresponded well with independent observations of symbiont concentrations obtained from field and laboratory studies of healthy colonies. Overall, this study demonstrates that the seasonal fluctuations, in symbiont numbers observed in healthy colonies of the Mediterranean coral investigated, do not have a strong effect on photosynthetic energy acquisition.

Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts

Understanding the sedimentation and turbidity thresholds for corals is critical in assessing the potential impacts of dredging projects in tropical marine systems. In this study, we exposed two species of coral sampled from offshore locations to six levels of total suspended solids (TSS) for 16 weeks in the laboratory, including a 4 week recovery period. Dose-response relationships were developed to quantify the lethal and sub-lethal thresholds of sedimentation and turbidity for the corals. The sediment treatments affected the horizontal foliaceous species (Montipora aequituberculata) more than the upright branching species (Acropora millepora). The lowest sediment treatments that caused full colony mortality were 30 mg l−1 TSS (25 mg cm−2 day−1) for M. aequituberculata and 100 mg l−1 TSS (83 mg cm−2 day−1) for A. millepora after 12 weeks. Coral mortality generally took longer than 4 weeks and was closely related to sediment accumulation on the surface of the corals. While measurements of damage to photosystem II in the symbionts and reductions in lipid content and growth indicated sub-lethal responses in surviving corals, the most reliable predictor of coral mortality in this experiment was long-term sediment accumulation on coral tissue.

The Coral Trait Database, a curated database of trait information for coral species from the global oceans

Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism’s function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.

Thermally tolerant corals have limited capacity to acclimatize to future warming

Thermal stress affects organism performance differently depending on the ambient temperature to which they are acclimatized, which varies along latitudinal gradients. This study investigated whether differences in physiological responses to temperature are consistent with regional differences in temperature regimes for the stony coral Oculina patagonica. To resolve this question, we experimentally assessed how colonies originating from four different locations characterized by >3 °C variation in mean maximum annual temperature responded to warming from 20 to 32 °C. We assessed plasticity in symbiont identity, density, and photosynthetic properties, together with changes in host tissue biomass. Results show that, without changes in the type of symbiont hosted by coral colonies, O. patagonica has limited capacity to acclimatize to future warming. We found little evidence of variation in overall thermal tolerance, or in thermal optima, in response to spatial variation in ambient temperature. Given that the invader O. patagonica is a relatively new member of the Mediterranean coral fauna, our results also suggest that coral populations may need to remain isolated for a long period of time for thermal adaptation to potentially take place. Our study indicates that for O. patagonica, mortality associated with thermal stress manifests primarily through tissue breakdown under moderate but prolonged warming (which does not impair symbiont photosynthesis and, therefore, does not lead to bleaching). Consequently, projected global warming is likely to cause repeat incidents of partial and whole colony mortality and might drive a gradual range contraction of Mediterranean corals.