Measuring multi-year changes in the Symbiodiniaceae algae in Caribbean corals on coral-depleted reefs.

Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from nine species were marked and sampled in 2017. Of these colonies, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes (2017) and the regional onset of stony coral tissue loss disease (2019). While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together, these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals.

Divergent bleaching and recovery trajectories in reef-building corals following a decade of successive marine heatwaves.

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual's lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai'i, Montipora capitata and Porites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies of P. compressa exhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptible M. capitata repeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically, M. capitata displayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely, P. compressa appeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene.

Scale dependence of coral reef oases and their environmental correlates.

Identifying relatively intact areas within ecosystems and determining the conditions favoring their existence is necessary for effective management in the context of widespread environmental degradation. In this study, we used 3766 surveys of randomly selected sites in the United States and U.S. Territories to identify the correlates of sites categorized as "oases" (defined as sites with relatively high total coral cover). We used occupancy models to evaluate the influence of 10 environmental predictors on the probability that an area (21.2-km2 cell) would harbor coral oases defined at four spatial extents: cross-basin, basin, region, and subregion. Across all four spatial extents, oases were more likely to occur in habitats with high light attenuation. The influence of the other environmental predictors on the probability of oasis occurrence were less consistent and varied with the scale of observation. Oases were most likely in areas of low human population density, but this effect was evident only at the cross-basin and subregional extents. At the regional and subregional extents oases were more likely where sea-surface temperature was more variable, whereas at the larger spatial extents the opposite was true. By identifying the correlates of oasis occurrence, the model can inform the prioritization of reef areas for management. Areas with biophysical conditions that confer corals with physiological resilience, as well as limited human impacts, likely support coral reef oases across spatial extents. Our approach is widely applicable to the development of conservation strategies to protect biodiversity and ecosystems in an era of magnified human disturbance.

Coral bleaching response is unaltered following acclimatization to reefs with distinct environmental conditions.

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change-resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine whether stress resistance is affected by transplantation beyond a coral's native reef. Here, we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between reefs with distinct pH, salinity, dissolved oxygen, sedimentation, and flow dynamics to determine whether heat stress response is altered following coral exposure to novel physicochemical conditions in situ. Critically, transplantation had no influence on coral heat stress responses, indicating that this trait was relatively fixed. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolic rates and overall fitness were higher at the reef with higher flow, salinity, sedimentation, and diel fluctuations of pH and dissolved oxygen, and did not differ between native and cross-transplanted corals, indicating acclimatization via plasticity within just 3 mo. Conversely, cross-transplants at the second reef had higher fitness than native corals, thus increasing the fitness potential of the recipient population. This experiment was conducted during a nonbleaching year, so the potential benefits to recipient population fitness are likely enhanced during bleaching years. In summary, this study demonstrates that outplanting bleaching-resistant corals is a promising tool for elevating the resistance of coral populations to ocean warming.

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails.

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO2, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO2 experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO2 oysters were consumed. The invasive snails were tolerant of elevated CO2 with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29-40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.

Larval carry-over effects from ocean acidification persist in the natural environment.

An extensive body of work suggests that altered marine carbonate chemistry can negatively influence marine invertebrates, but few studies have examined how effects are moderated and persist in the natural environment. A particularly important question is whether impacts initiated in early life might be exacerbated or attenuated over time in the presence or absence of other stressors in the field. We reared Olympia oyster (Ostrea lurida) larvae in laboratory cultures under control and elevated seawater pCO2 concentrations, quantified settlement success and size at metamorphosis, then outplanted juveniles to Tomales Bay, California, in the mid intertidal zone where emersion and temperature stress were higher, and in the low intertidal zone where conditions were more benign. We tracked survival and growth of outplanted juveniles for 4 months, halfway to reproductive age. Survival to metamorphosis in the laboratory was strongly affected by larval exposure to elevated pCO2 conditions. Survival of juvenile outplants was reduced dramatically at mid shore compared to low shore levels regardless of the pCO2 level that oysters experienced as larvae. However, juveniles that were exposed to elevated pCO2 as larvae grew less than control individuals, representing a larval carry-over effect. Although juveniles grew less at mid shore than low shore levels, there was no evidence of an interaction between the larval carry-over effect and shore level, suggesting little modulation of acidification impacts by emersion or temperature stress. Importantly, the carry-over effects of larval exposure to ocean acidification remained unabated 4 months later with no evidence of compensatory growth, even under benign conditions. This latter result points to the potential for extended consequences of brief exposures to altered seawater chemistry with potential consequences for population dynamics.

Evolutionary change during experimental ocean acidification.

Rising atmospheric carbon dioxide (CO2) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth's oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO2 levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO2 levels. Although larval development and morphology showed little response to elevated CO2, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis--gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.

Functional impacts of ocean acidification in an ecologically critical foundation species.

Anthropogenic CO(2) is reducing the pH and altering the carbonate chemistry of seawater, with repercussions for marine organisms and ecosystems. Current research suggests that calcification will decrease in many species, but compelling evidence of impaired functional performance of calcium carbonate structures is sparse, particularly in key species. Here we demonstrate that ocean acidification markedly degrades the mechanical integrity of larval shells in the mussel Mytilus californianus, a critical community member on rocky shores throughout the northeastern Pacific. Larvae cultured in seawater containing CO(2) concentrations expected by the year 2100 (540 or 970 ppm) precipitated weaker, thinner and smaller shells than individuals raised under present-day seawater conditions (380 ppm), and also exhibited lower tissue mass. Under a scenario where mussel larvae exposed to different CO(2) levels develop at similar rates, these trends suggest a suite of potential consequences, including an exacerbated vulnerability of new settlers to crushing and drilling attacks by predators; poorer larval condition, causing increased energetic stress during metamorphosis; and greater risks from desiccation at low tide due to shifts in shell area to body mass ratios. Under an alternative scenario where responses derive exclusively from slowed development, with impacted individuals reaching identical milestones in shell strength and size by settlement, a lengthened larval phase could increase exposure to high planktonic mortality rates. In either case, because early life stages operate as population bottlenecks, driving general patterns of distribution and abundance, the ecological success of this vital species may be tied to how ocean acidification proceeds in coming decades.