Crown-of-thorns seastar (Acanthaster spp.) feeding ecology across species and regions.

The coral predators, crown-of-thorns starfish (COTS, Acanthaster spp.) remain a major cause of extensive and widespread coral loss in Indo-Pacific coral reefs. With increased phylogenetic understanding of these seastars, at least five species appear to be present across different regions. We compare the feeding ecology of these species. Where acroporid corals are prevalent, Acanthaster spp. often exhibit a preference for these corals, with Porites being least preferred, as seen in most species including Acanthaster planci in the northern Indian Ocean and Acanthaster cf. solaris in the west Pacific. In the eastern Pacific, where Acropora is largely absent, Acanthaster cf. ellisii prey on a range of coral species, including Porites. Coral predation by COTS is influenced by several factors including food availability, coral nutritional value, protective crustaceans and coral defenses, with differences in feeding ecology and behaviour emerging across the different COTS species. Feeding behaviour of COTS can act to increase coral species richness by reducing the dominance of fast-growing species. In outbreaking populations, COTS impacts reef systems by reducing live coral cover, eroding reef complexity and causing shifts in reef trophic structure. Where data are available, we synthesise and contrast the feeding preferences and foraging behaviour of Acanthaster species, and their impact on coral assemblages across the different species and regions. For areas where focal predation on Acropora occurs, also the fastest growing coral with the greatest recovery potential following mass mortality events, the combination of climate change and COTS outbreaks presents an imminent threat to coral reefs. This is exacerbated by the dietary flexibility of Acanthaster species. The impacts of heatwaves, COTS and other stressors are creating a negative feedback loop accelerating coral reef decline.

Untapped policy avenues to protect coral reef ecosystems.

Coral reefs are experiencing severe decline, and urgent action is required at local and global scales to curb ecosystem loss. Establishing new regulations to protect corals, however, can be time consuming and costly, and it is therefore necessary to leverage existing legal instruments, such as policies originally designed to address terrestrial rather than marine activities, to prevent coral reef degradation. Focusing on the United States, but drawing on successful examples worldwide, we present actionable pathways to increase coral protections under legislation that was originally designed to advance clean freshwater, safe drinking water, and emergency management. We identify specific legal policies and procedures (e.g., industrial permit limits, nonpoint source management incentives, and floodplain restoration programs) that can curb coral reef pollution and can be extended to other countries with similar regulations in place. Coral reef practitioners should consider a broad array of currently underused, actionable, and intersecting environmental policies that can be applied to mitigate coral stress.

Acclimation to low pH does not affect the thermal tolerance of Arbacia lixula progeny.

As the ocean warms, the thermal tolerance of marine invertebrates is key to determining their distributional change, where acclimation to low pH may impact the thermal range of optimal development. We compared thermal tolerance of progeny from a low pH-acclimated sea urchin (Arbacia lixula) population from the CO2 vents of Ischia (Italy) and a nearby population living at ambient pH. The percentages of normally developing gastrulae and two-armed larvae were determined across 10 temperatures representing present and future temperature conditions (16-34°C). Vent-acclimated sea urchins showed a greater percentage of normal development at 24 h, with a larger optimal developmental temperature range than control sea urchins (12.3°C versus 5.4°C range, respectively). At 48 h, upper lethal temperatures for 50% survival with respect to ambient temperatures were similar between control (+6.8°C) and vent (+6.2°C) populations. Thus, acclimation to low pH did not impact the broad thermal tolerance of A. lixula progeny. With A. lixula's barrens-forming abilities, its wide thermotolerance and its capacity to acclimate to low pH, this species will continue to be an important ecological engineer in Mediterranean macroalgal ecosystems in a changing ocean.

Mapped coral mortality and refugia in an archipelago-scale marine heat wave.

Corals are a major habitat-building life-form on tropical reefs that support a quarter of all species in the ocean and provide ecosystem services to millions of people. Marine heat waves continue to threaten and shape reef ecosystems by killing individual coral colonies and reducing their diversity. However, marine heat waves are spatially and temporally heterogeneous, and so too are the environmental and biological factors mediating coral resilience during and following thermal events. This combination results in highly variable outcomes at both the coral bleaching and mortality stages of every event. This, in turn, impedes the assessment of changing reef-scale patterns of thermal tolerance or places of resistance known as reef refugia. We developed a large-scale, high-resolution coral mortality monitoring capability based on airborne imaging spectroscopy and applied it to a major marine heat wave in the Hawaiian Islands. While water depth and thermal stress strongly mediated coral mortality, relative coral loss was also inversely correlated with preheat-wave coral cover, suggesting the existence of coral refugia. Subsequent mapping analyses indicated that potential reef refugia underwent up to 40% lower coral mortality compared with neighboring reefs, despite similar thermal stress. A combination of human and environmental factors, particularly coastal development and sedimentation levels, differentiated resilient reefs from other more vulnerable reefs. Our findings highlight the role that coral mortality mapping, rather than bleaching monitoring, can play for targeted conservation that protects more surviving corals in our changing climate.

Forecasting impacts of ocean acidification on marine communities: Utilizing volcanic CO2 vents as natural laboratories.

Oceans have absorbed approximately 30% of anthropogenic CO2 emissions, causing a phenomenon known as 'ocean acidification'. With surface ocean pH changing at a rapid pace, continued uptake of CO2 is expected to decrease ocean pH by 0.3 pH units as early as 2081, accompanied by a decrease in the saturation of calcium carbonate minerals needed to produce skeletons and shells (RCP 8.5 scenario, IPCC 2019). Natural marine CO2 vent systems provide ocean acidification proxies, offering a glimpse into what a future ocean may look like.

Impacts of pollution, fishing pressure, and reef rugosity on resource fish biomass in West Hawaii.

Human activities and land-use drivers combine in complex ways to affect coral reef health and, in turn, the diversity and abundance of reef fauna. Here we examine the impacts of different marine protected area (MPA) types, and various human and habitat drivers, on resource fish functional groups (i.e., total fish, herbivore, grazer, scraper, and browser biomass) along the 180 km west coast of Hawaii Island. Across survey years from 2008 to 2018, we observed an overall decrease in total fish biomass of 45%, with similar decreases in biomass seen across most fish functional groups. MPAs that prohibited a combination of lay nets, aquarium collection, and spear fishing were most effective in maintaining and/or increasing fish biomass across all functional groups. We also found that pollution, fishing, and habitat drivers all contributed to changes in total fish biomass, where the most negative impact was nitrogen input from land-based sewage disposal. Fish biomass relationships with our study drivers depended on fish functional grouping. For surgeonfish (grazers), changes in biomass linked most strongly to changes in reef rugosity. For parrotfish (scrapers), biomass was better explained by changes in commercial catch where current commercial fishing levels are negatively affecting scraper populations. Our observations suggest that regional management of multiple factors, including habitat, pollution, and fisheries, will benefit resource fish biomass off Hawaii Island.

Responses of sea urchin larvae to field and laboratory acidification.

Understanding the extent to which laboratory findings of low pH on marine organisms can be extrapolated to the natural environment is key toward making better projections about the impacts of global change on marine ecosystems. We simultaneously exposed larvae of the sea urchin Arbacia lixula to ocean acidification in laboratory and natural CO2 vents and assessed the arm growth response as a proxy of net calcification. Populations of embryos were simultaneously placed at both control and volcanic CO2 vent sites in Ischia (Italy), with a parallel group maintained in the laboratory in control and low pH treatments corresponding to the mean pH levels of the field sites. As expected, larvae grown at constant low pH (pHT 7.8) in the laboratory exhibited reduced arm growth, but counter to expectations, the larvae that developed at the low pH vent site (pHT 7.33-7.99) had the longest arms. The larvae at the control field site (pHT 7.87-7.99) grew at a similar rate to laboratory controls. Salinity, temperature, oxygen and flow regimes were comparable between control and vent sites; however, chlorophyll a levels and particulate organic carbon were higher at the vent site than at the control field site. This increased food availability may have modulated the effects of low pH, creating an opposite calcification response in the laboratory from that in the field. Divergent responses of the same larval populations developing in laboratory and field environments show the importance of considering larval phenotypic plasticity and the complex interactions among decreased pH, food availability and larval responses.

Limitations of cross- and multigenerational plasticity for marine invertebrates faced with global climate change.

Although cross generation (CGP) and multigenerational (MGP) plasticity have been identified as mechanisms of acclimation to global change, the weight of evidence indicates that parental conditioning over generations is not a panacea to rescue stress sensitivity in offspring. For many species, there were no benefits of parental conditioning. Even when improved performance was observed, this waned over time within a generation or across generations and fitness declined. CGP and MGP studies identified resilient species with stress tolerant genotypes in wild populations and selected family lines. Several bivalves possess favourable stress tolerance and phenotypically plastic traits potentially associated with genetic adaptation to life in habitats where they routinely experience temperature and/or acidification stress. These traits will be important to help 'climate proof' shellfish ventures. Species that are naturally stress tolerant and those that naturally experience a broad range of environmental conditions are good candidates to provide insights into the physiological and molecular mechanisms involved in CGP and MGP. It is challenging to conduct ecologically relevant global change experiments over the long times commensurate with the pace of changing climate. As a result, many studies present stressors in a shock-type exposure at rates much faster than projected scenarios. With more gradual stressor introduction over longer experimental durations and in context with conditions species are currently acclimatized and/or adapted to, the outcomes for sensitive species might differ. We highlight the importance to understand primordial germ cell development and the timing of gametogenesis with respect to stressor exposure. Although multigenerational exposure to global change stressors currently appears limited as a universal tool to rescue species in the face of changing climate, natural proxies of future conditions (upwelling zones, CO2 vents, naturally warm habitats) show that phenotypic adjustment and/or beneficial genetic selection is possible for some species, indicating complex plasticity-adaptation interactions.

Cherchez la femme - impact of ocean acidification on the egg jelly coat and attractants for sperm.

The impact of ocean acidification on marine invertebrate eggs and its consequences for sperm chemotaxis are unknown. In the sea urchins Heliocidaris tuberculata and Heliocidariserythrogramma, with small (93 µm) and large (393 µm) eggs, respectively, we documented the effect of decreased pH on the egg jelly coat, an extracellular matrix that increases target size for sperm and contains sperm-attracting molecules. In near-future conditions (pH 7.8, 7.6), the jelly coat of H. tuberculata decreased by 11% and 21%, reducing egg target size by 9% and 17%, respectively. In contrast, the egg jelly coat of H. erythrogramma was not affected. The reduction in the jelly coat has implications for sperm chemotaxis in H. tuberculata In the presence of decreased pH and egg chemicals, the sperm of this species increased their velocity, motility and linearity, behaviour that was opposite to that seen for sperm exposed to egg chemicals in ambient conditions. Egg chemistry appears to cause a reduction in sperm velocity where attractants guide the sperm in the direction of the egg. Investigation of the effects of decreased pH on sperm isolated from the influence of egg chemistry does not provide an integrative assessment of the effects of ocean acidification on sperm function. Differences in the sensitivity of the jelly coat of the two species is likely associated with egg evolution in H. erythrogramma We highlight important unappreciated impacts of ocean acidification on marine gamete functionality, and insights into potential winners and losers in a changing ocean, pointing to the advantage conveyed by the evolution of large eggs.

Marine gametes in a changing ocean: Impacts of climate change stressors on fecundity and the egg.

In marine invertebrates, the environmental history of the mother can influence fecundity and egg size. Acclimation of females in climate change stressors, increased temperature and low pH, results in a decrease in egg number and size in many taxa, with the exception of cephalopods, where eggs increase in size. With respect to spawned eggs, near future levels of ocean acidification can interfere with the egg's block to polyspermy and intracellular pH. Reduction of the extracellular egg jelly coat seen in low pH conditions has implications for impaired egg function and fertilization. Some fast generation species (e.g. copepods, polychaetes) have shown restoration of female reproductive output after several generations in treatments. It will be important to determine if the changes to egg number and size induced by exposure to climate change stressors are heritable.

Ocean acidification has little effect on developmental thermal windows of echinoderms from Antarctica to the tropics.

As the ocean warms, thermal tolerance of developmental stages may be a key driver of changes in the geographical distributions and abundance of marine invertebrates. Additional stressors such as ocean acidification may influence developmental thermal windows and are therefore important considerations for predicting distributions of species under climate change scenarios. The effects of reduced seawater pH on the thermal windows of fertilization, embryology and larval morphology were examined using five echinoderm species: two polar (Sterechinus neumayeri and Odontaster validus), two temperate (Fellaster zelandiae and Patiriella regularis) and one tropical (Arachnoides placenta). Responses were examined across 12-13 temperatures ranging from -1.1 °C to 5.7 °C (S. neumayeri), -0.5 °C to 10.7 °C (O. validus), 5.8 °C to 27 °C (F. zelandiae), 6.0 °C to 27.1 °C (P. regularis) and 13.9 °C to 34.8 °C (A. placenta) under present-day and near-future (2100+) ocean acidification conditions (-0.3 pH units) and for three important early developmental stages 1) fertilization, 2) embryo (prehatching) and 3) larval development. Thermal windows for fertilization were broad and were not influenced by a pH decrease. Embryological development was less thermotolerant. For O. validus, P. regularis and A. placenta, low pH reduced normal development, albeit with no effect on thermal windows. Larval development in all five species was affected by both temperature and pH; however, thermal tolerance was not reduced by pH. Results of this study suggest that in terms of fertilization and development, temperature will remain as the most important factor influencing species' latitudinal distributions as the ocean continues to warm and decrease in pH, and that there is little evidence of a synergistic effect of temperature and ocean acidification on the thermal control of species ranges.

Increased temperature, but not acidification, enhances fertilization and development in a tropical urchin: potential for adaptation to a tropicalized eastern Australia.

To predict the effects of global change on marine populations, it is important to measure the effects of climate stressors on performance and potential for adaptation. Adaptation depends on heritable genetic variance for stress tolerance being present in populations. We determined the effects of near-future ocean conditions on fertilization success of the sea urchin Pseudoboletia indiana. In 16 multiple dam-sire crosses, we quantified genetic variation in tolerance of warming (+3°C) and acidification (-0.3 to 0.5 pH units) at the gastrulation stage. Ocean acidification decreased fertilization across all dam-sire combinations with effects of pH significantly differing among the pairings. Decreased pH reduced the percentage of normal gastrulae with negative effects alleviated by increased temperature. Significant sire by environment interactions indicated the presence of heritable variation in tolerance of stressors at gastrulation and thus the potential for selection of resistant genotypes, which may enhance population persistence. A low genetic correlation indicated that genotypes that performed well at gastrulation in low pH did not necessarily perform well at higher temperatures. Furthermore, performance at fertilization was not necessarily a good predictor of performance at the later stage of gastrulation. Southern range edge populations of Pseudoboletia indiana may benefit from future warming with potential for extension of their distribution in south-east Australia.

Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos.

BACKGROUND: Predicting effects of rapid climate change on populations depends on measuring the effects of climate stressors on performance, and potential for adaptation. Adaptation to stressful climatic conditions requires heritable genetic variance for stress tolerance present in populations. METHODOLOGY/PRINCIPAL FINDINGS: We quantified genetic variation in tolerance of early development of the ecologically important sea urchin Centrostephanus rodgersii to near-future (2100) ocean conditions projected for the southeast Australian global change hot spot. Multiple dam-sire crosses were used to quantify the interactive effects of warming (+2-4 °C) and acidification (-0.3-0.5 pH units) across twenty-seven family lines. Acidification, but not temperature, decreased the percentage of cleavage stage embryos. In contrast, temperature, but not acidification decreased the percentage of gastrulation. Cleavage success in response to both stressors was strongly affected by sire identity. Sire and dam identity significantly affected gastrulation and both interacted with temperature to determine developmental success. Positive genetic correlations for gastrulation indicated that genotypes that did well at lower pH also did well in higher temperatures. CONCLUSIONS/SIGNIFICANCE: Significant genotype (sire) by environment interactions for both stressors at gastrulation indicated the presence of heritable variation in thermal tolerance and the ability of embryos to respond to changing environments. The significant influence of dam may be due to maternal provisioning (maternal genotype or environment) and/or offspring genotype. It appears that early development in this ecologically important sea urchin is not constrained in adapting to the multiple stressors of ocean warming and acidification. The presence of tolerant genotypes indicates the potential to adapt to concurrent warming and acidification, contributing to the resilience of C. rodgersii in a changing ocean.