Projecting coral responses to intensifying marine heatwaves under ocean acidification.

Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.

Integrating environmental variability to broaden the research on coral responses to future ocean conditions.

Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2 , and O2 ) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2 , and dissolved O2 , which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.

Global determinants of prey naiveté to exotic predators.

Prey naiveté-the failure of prey to recognize novel predators as threats-is thought to exacerbate the impact that exotic predators exert on prey populations. Prey naiveté varies under the influence of eco-evolutionary mediating factors, such as biogeographic isolation and prey adaptation, although an overall quantification of their influence is lacking. We conducted a global meta-analysis to test the effects of several hypothesized mediating factors on the expression of prey naiveté. Prey were overall naive towards exotic predators in marine and freshwater systems but not in terrestrial systems. Prey naiveté was most pronounced towards exotic predators that did not have native congeneric relatives in the recipient community. Time since introduction was relevant, as prey naiveté declined with the number of generations since introduction; on average, around 200 generations may be required to erode naiveté sufficiently for prey to display antipredator behaviour towards exotic predators. Given that exotic predators are a major cause of extinction, the global predictors and trends of prey naiveté presented here can inform efforts to meet conservation targets.

Tropical seagrass Halophila stipulacea shifts thermal tolerance during Mediterranean invasion.

Exotic species often face new environmental conditions that are different from those that they are adapted to. The tropical seagrass Halophila stipulacea is a Lessepsian migrant that colonized the Mediterranean Sea around 100 years ago, where at present the minimum seawater temperature is cooler than in its native range in the Red Sea. Here, we tested if the temperature range in which H. stipulacea can exist is conserved within the species or if the exotic populations have shifted their thermal breadth and optimum due to the cooler conditions in the Mediterranean. We did so by comparing the thermal niche (e.g. optimal temperatures, and upper and lower thermal limits) of native (Saudi Arabia in the Red Sea) and exotic (Greece and Cyprus in the Mediterranean Sea) populations of H. stipulacea. We exposed plants to 12 temperature treatments ranging from 8 to 40°C for 7 days. At the end of the incubation period, we measured survival, rhizome elongation, shoot recruitment, net population growth and metabolic rates. Upper and lower lethal thermal thresholds (indicated by 50% plant mortality) were conserved across populations, but minimum and optimal temperatures for growth and oxygen production were lower for Mediterranean populations than for the Red Sea one. The displacement of the thermal niche of exotic populations towards the colder Mediterranean Sea regime could have occurred within 175 clonal generations.

How many alien species will there be in 2050?

How many alien species will there be in 2050? Seebens et al. (2020) calculate that the number of alien species will continue to increase steeply everywhere across the globe. This number of emerging alien species will rise globally by about 35% from 2005 to 2050, and each continent will gain around 1,300 new species on average. Photo credit: Andrea Anton.

Differential thermal tolerance between algae and corals may trigger the proliferation of algae in coral reefs.

Marine heatwaves can lead to rapid changes in entire communities, including in the case of shallow coral reefs the potential overgrowth of algae. Here we tested experimentally the differential thermal tolerance between algae and coral species from the Red Sea through the measurement of thermal performance curves and the assessment of thermal limits. Differences across functional groups (algae vs. corals) were apparent for two key thermal performance metrics. First, two reef-associated algae species (Halimeda tuna and Turbinaria ornata) had higher lethal thermal limits than two coral species (Pocillopora verrucosa and Stylophora pistillata) conferring those species of algae with a clear advantage during heatwaves by surpassing the thermal threshold of coral survival. Second, the coral species had generally greater deactivation energies for net and gross primary production rates compared to the algae species, indicating greater thermal sensitivity in corals once the optimum temperature is exceeded. Our field surveys in the Red Sea reefs before and after the marine heatwave of 2015 show a change in benthic cover mainly in the southern reefs, where there was a decrease in coral cover and a concomitant increase in algae abundance, mainly turf algae. Our laboratory and field observations indicate that a proliferation of algae might be expected on Red Sea coral reefs with future ocean warming.

Ecological effects of non-native species in marine ecosystems relate to co-occurring anthropogenic pressures.

Predictors for the ecological effects of non-native species are lacking, even though such knowledge is fundamental to manage non-native species and mitigate their impacts. Current theories suggest that the ecological effects of non-native species may be related to other concomitant anthropogenic stressors, but this has not been tested at a global scale. We combine an exhaustive meta-analysis of the ecological effects of marine non-native species with human footprint proxies to determine whether the ecological changes due to non-native species are modulated by co-occurring anthropogenic impacts. We found that non-native species had greater negative effects on native biodiversity where human population was high and caused reductions in individual performance where cumulative human impacts were large. On this basis we identified several marine ecoregions where non-native species may have the greatest ecological effects, including areas in the Mediterranean Sea and along the northwest coast of the United States. In conclusion, our global assessment suggests coexisting anthropogenic impacts can intensify the ecological effects of non-native species.

Warming and resource availability shift food web structure and metabolism.

Climate change disrupts ecological systems in many ways. Many documented responses depend on species' life histories, contributing to the view that climate change effects are important but difficult to characterize generally. However, systematic variation in metabolic effects of temperature across trophic levels suggests that warming may lead to predictable shifts in food web structure and productivity. We experimentally tested the effects of warming on food web structure and productivity under two resource supply scenarios. Consistent with predictions based on universal metabolic responses to temperature, we found that warming strengthened consumer control of primary production when resources were augmented. Warming shifted food web structure and reduced total biomass despite increases in primary productivity in a marine food web. In contrast, at lower resource levels, food web production was constrained at all temperatures. These results demonstrate that small temperature changes could dramatically shift food web dynamics and provide a general, species-independent mechanism for ecological response to environmental temperature change.

Decoupled effects (positive to negative) of nutrient enrichment on ecosystem services.

Eutrophication is a widespread phenomenon that disrupts natural ecosystems around the globe. Despite the general recognition that ecosystems provide many services and benefits to humans, little effort has been made to address how increasing anthropogenic eutrophication affects those services. We conducted a field experiment to determine the effect of nutrient enrichment on five ecological services provided by a model coastal system, a shallow seagrass community near Mobile Bay, Alabama (USA): (1) the provision of shelter for fauna; (2) the quality of food provided to first-order consumers; (3) quantity of food provision to first-order consumers and O2/CO2 exchange; (4) producer carbon and nitrogen storage, and (5) water clarity. The results showed a severe negative impact on seagrass density and biomass, which greatly reduced the structural complexity of the community and provision of shelter to fauna. Water clarity and the standing stock of producer carbon were reduced in the fertilized area in comparison with the control area. In contrast, nutrient addition did not affect in any consistent way the total quantity of food available for first-order consumers, the net exchange of O2/CO2, or the standing stock of producer nitrogen in the community. The nutritional quality of the food available for first-order consumers increased with fertilization. These results show that the impacts of nutrient enrichment on the services provided by natural systems may be disparate, ranging from negative to positive. These findings suggest that management policies for anthropogenic eutrophication will depend on the specific ecosystem service targeted. In the case of shallow seagrass beds, the loss of biogenic habitat and drastic impacts on commercially important fauna may be sufficiently alarming to warrant rigorous control of coastal eutrophication.

Habitat-forming species trap microplastics into coastal sediment sinks.

Nearshore biogenic habitats are known to trap sediments, and may therefore also accumulate biofouled, non-buoyant microplastics. Using a current-generating field flume (TiDyFLOW), we experimentally assessed the mechanisms of microplastic trapping of two size classes, 0.5 mm and 2.5 mm particle size, by three contrasting types of biogenic habitats: 1) seagrasses, 2) macroalgae, and 3) scleractinian corals. Results showed that benthic organisms with a complex architecture and rough surface - such as hard corals - trap the highest number of microplastics in their aboveground structure. Sediment was however the major microplastic sink, accumulating 1 to 2 orders of magnitude more microplastics than the benthic structure. Microplastic accumulation in the sediment could be explained by near-bed turbulent kinetic energy (TKE), indicating that this is governed by the same hydrodynamic processes leading to sediment trapping. Thus, the most valuable biogenic habitats in terms of nursery and coastal protection services also have the highest capacity of accumulating microplastics in their sediments. A significantly larger fraction of 0.5 mm particles was trapped in the sediment compared to 2.5 mm particles, because especially the smaller microplastics are entrained into the sediment. Present observations contribute to explaining why especially microplastics smaller than 1 mm are missing in surface waters.

High summer temperatures amplify functional differences between coral- and algae-dominated reef communities.

Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bimonthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), whereas carbon losses via respiration and dissolved organic carbon release more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with coral-algal phase shifts. Algae-dominated communities may outcompete coral-dominated communities because of their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.

A framework for experimental scenarios of global change in marine systems using coral reefs as a case study.

Understanding the consequences of rising CO2 and warming on marine ecosystems is a pressing issue in ecology. Manipulative experiments that assess responses of biota to future ocean warming and acidification conditions form a necessary basis for expectations on how marine taxa may respond. Although designing experiments in the context of local variability is most appropriate, local temperature and CO2 characteristics are often unknown as such measures necessitate significant resources, and even less is known about local future scenarios. To help address these issues, we summarize current uncertainties in CO2 emission trajectories and climate sensitivity, examine region-specific changes in the ocean, and present a straightforward global framework to guide experimental designs. We advocate for the inclusion of multiple plausible future scenarios of predicted levels of ocean warming and acidification in forthcoming experimental research. Growing a robust experimental base is crucial to understanding the prospect form and function of marine ecosystems in the Anthropocene.

Are the ecological effects of the "worst" marine invasive species linked with scientific and media attention?

Non-native species are a major driver of environmental change. In this study we assessed the ecological impact of the "worst" non-native species and the associated scientific and media publications through time to understand what influences interest in these species. Ecological effect was based on a qualitative assessment reported in research publications and additional searches of the scientific and media attention were conducted to determine published articles and assess attention. We did not detect a relationship between the number of publications for a non-native species and the magnitude of the ecological effects of that species or the number of citations. Media coverage on non-native species was low, only evident for less than 50% of the non-native species assessed. Media coverage was initially related to the number of scientific publications, but was short-lived. In contrast, the attention to individual non-native species in the scientific literature was sustained through time and often continued to increase over time. Time between detection of the non-native species and the scientific/media attention were reduced with each successive introduction to a new geographic location. Tracking publications on non-native species indicated that media attention does seem to be associated with the production of scientific research while scientific attention was not related to the magnitude of the ecological effects.

Oxygen supersaturation protects coastal marine fauna from ocean warming.

Ocean warming affects the life history and fitness of marine organisms by, among others, increasing animal metabolism and reducing oxygen availability. In coastal habitats, animals live in close association with photosynthetic organisms whose oxygen supply supports metabolic demands and may compensate for acute warming. Using a unique high-frequency monitoring dataset, we show that oxygen supersaturation resulting from photosynthesis closely parallels sea temperature rise during diel cycles in Red Sea coastal habitats. We experimentally demonstrate that oxygen supersaturation extends the survival to more extreme temperatures of six species from four phyla. We clarify the mechanistic basis of the extended thermal tolerance by showing that hyperoxia fulfills the increased metabolic demand at high temperatures. By modeling 1 year of water temperatures and oxygen concentrations, we predict that oxygen supersaturation from photosynthetic activity invariably fuels peak animal metabolic demand, representing an underestimated factor of resistance and resilience to ocean warming in ectotherms.

Publisher Correction: Global ecological impacts of marine exotic species.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Global ecological impacts of marine exotic species.

Exotic species are a growing global ecological threat; however, their overall effects are insufficiently understood. While some exotic species are implicated in many species extinctions, others can provide benefits to the recipient communities. Here, we performed a meta-analysis to quantify and synthesize the ecological effects of 76 exotic marine species (about 6% of the listed exotics) on ten variables in marine communities. These species caused an overall significant, but modest in magnitude (as indicated by a mean effect size of g < 0.2), decrease in ecological variables. Marine primary producers and predators were the most disruptive trophic groups of the exotic species. Approximately 10% (that is, 2 out of 19) of the exotic species assessed in at least three independent studies had significant impacts on native species. Separating the innocuous from the disruptive exotic species provides a basis for triage efforts to control the marine exotic species that have the most impact, thereby helping to meet Aichi Biodiversity Target 9 of the Convention on Biological Diversity.

The future of Blue Carbon science.

The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Environmental and biotic correlates to lionfish invasion success in Bahamian coral reefs.

Lionfish (Pterois volitans), venomous predators from the Indo-Pacific, are recent invaders of the Caribbean Basin and southeastern coast of North America. Quantification of invasive lionfish abundances, along with potentially important physical and biological environmental characteristics, permitted inferences about the invasion process of reefs on the island of San Salvador in the Bahamas. Environmental wave-exposure had a large influence on lionfish abundance, which was more than 20 and 120 times greater for density and biomass respectively at sheltered sites as compared with wave-exposed environments. Our measurements of topographic complexity of the reefs revealed that lionfish abundance was not driven by habitat rugosity. Lionfish abundance was not negatively affected by the abundance of large native predators (or large native groupers) and was also unrelated to the abundance of medium prey fishes (total length of 5-10 cm). These relationships suggest that (1) higher-energy environments may impose intrinsic resistance against lionfish invasion, (2) habitat complexity may not facilitate the lionfish invasion process, (3) predation or competition by native fishes may not provide biotic resistance against lionfish invasion, and (4) abundant prey fish might not facilitate lionfish invasion success. The relatively low biomass of large grouper on this island could explain our failure to detect suppression of lionfish abundance and we encourage continuing the preservation and restoration of potential lionfish predators in the Caribbean. In addition, energetic environments might exert direct or indirect resistance to the lionfish proliferation, providing native fish populations with essential refuges.