Sea urchin mass mortalities 40 y apart further threaten Caribbean coral reefs.

In 1983 to 1984, a mass mortality event caused a Caribbean-wide, >95% population reduction of the echinoid grazer, Diadema antillarum. This led to blooms of algae contributing to the devastation of scleractinian coral populations. Since then, D. antillarum exhibited only limited and patchy population recovery in shallow water, and in 2022 was struck by a second mass mortality reported over many reef localities in the Caribbean. Half-a-century time-series analyses of populations of this sea urchin from St. John, US Virgin Islands, reveal that the 2022 event has reduced population densities by 98.00% compared to 2021, and by 99.96% compared to 1983. In 2021, coral cover throughout the Caribbean was approaching the lowest values recorded in modern times. However, prior to 2022, locations with small aggregations of D. antillarum produced grazing halos in which weedy corals were able to successfully recruit and become the dominant coral taxa. The 2022 mortality has eliminated these algal-free halos on St. John and perhaps many other regions, thereby increasing the risk that these reefs will further transition into coral-free communities.

The scaling of metabolic traits differs among larvae and juvenile colonies of scleractinian corals.

Body size profoundly affects organism fitness and ecosystem dynamics through the scaling of physiological traits. This study tested for variation in metabolic scaling and its potential drivers among corals differing in life history strategies and taxonomic identity. Data were compiled from published sources and augmented with empirical measurements of corals in Moorea, French Polynesia. The data compilation revealed metabolic isometry in broadcasted larvae, but size-independent metabolism in brooded larvae; empirical measurements of Pocillopora acuta larvae also supported size-independent metabolism in brooded coral larvae. In contrast, for juvenile colonies (i.e. 1-4 cm diameter), metabolic scaling was isometric for Pocillopora spp., and negatively allometric for Porites spp. The scaling of biomass with surface area was isometric for Pocillopora spp., but positively allometric for Porites spp., suggesting the surface area to biomass ratio mediates metabolic scaling in these corals. The scaling of tissue biomass and metabolism were not affected by light treatment (i.e. either natural photoperiods or constant darkness) in either juvenile taxa. However, biomass was reduced by 9-15% in the juvenile corals from the light treatments and this coincided with higher metabolic scaling exponents, thus supporting the causal role of biomass in driving variation in scaling. This study shows that metabolic scaling is plastic in early life stages of corals, with intrinsic differences between life history strategy (i.e. brooded and broadcasted larvae) and taxa (i.e. Pocillopora spp. and Porites spp.), and acquired differences attributed to changes in area-normalized biomass.

Early post-settlement events, rather than settlement, drive recruitment and coral recovery at Moorea, French Polynesia.

Understanding population dynamics is a long-standing objective of ecology, but the need for progress in this area has become urgent. For coral reefs, achieving this objective is impeded by a lack of information on settlement versus post-settlement events in determining recruitment and population size. Declines in coral abundance are often inferred to be associated with reduced densities of recruits, which could arise from mechanisms occurring at larval settlement, or throughout post-settlement stages. This study uses annual measurements from 2008 to 2021 of coral cover, the density of coral settlers (S), the density of small corals (SC), and environmental conditions, to evaluate the roles of settlement versus post-settlement events in determining rates of coral recruitment and changes in coral cover at Moorea, French Polynesia. Coral cover, S, SC, and the SC:S ratio (a proxy for post-settlement success), and environmental conditions, were used in generalized additive models (GAMs) to show that: (a) coral cover was more strongly related to SC and SC:S than S, and (b) SC:S was highest when preceded by cool seawater, low concentrations of Chlorophyll a, and low flow speeds, and S showed evidence of declining with elevated temperature. Together, these results suggest that changes in coral cover in Moorea are more strongly influenced by post-settlement events than settlement. The key to understanding coral community resilience may lie in elucidating the factors attenuating the bottleneck between settlers and small corals.

Persistence of a sessile benthic organism promoted by a morphological strategy combining sheets and trees.

Sessile organisms exploit a life-history strategy in which adults are immobile and their growth position is determined at settlement. The morphological strategy exploited by these organisms has strong selective value, because it can allow beneficial matching of morphology to environmental and biological conditions. In benthic marine environments, a 'sheet-tree' morphology is a classic mechanism exploited by select sessile organisms, and milleporine hydrocorals provide one of the best examples of this strategy. Using 30-year analysis of Millepora sp. on the reefs of St. John, US Virgin Islands, I tested for the benefits of a sheet-tree morphology in mediating the ecological success of an important functional group of benthic space holders. The abundance of Millepora sp. chaotically changed from 1992 to 2021 in concert with hurricanes, bleaching and macroalgal crowding. Millepora sp. responded to these disturbances by exploiting their morphological strategy to increase the use of trees when their sheets were compromised by bleaching and spatial competition with macroalgae, and the use of sheets when their trees were broken by storms. Together, these results reveal the selective value of a plastic sheet-tree morphology, which can be exploited by sessile organisms to respond to decadal-scale variation in environmental conditions.

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.

Branching coral morphology affects physiological performance in the absence of colony integration.

For nearly 50 years, analyses of coral physiology have used small coral fragments (nubbins) to make inferences about larger colonies. However, scaling in corals shows that linear extrapolations from nubbins to whole colonies can be misleading, because polyps in nubbins are divorced of their morphologically complex and physiologically integrated corallum. We tested for the effects of integration among branches in determining size-dependent calcification of the coral Pocillopora spp. under elevated PCO2. Area-normalized net calcification was compared between branches (nubbins), aggregates of nubbins (complex morphologies without integration) and whole colonies (physiologically integrated) at 400 versus approximately 1000 µatm PCO2. Net calcification was unaffected by PCO2, but differed among colony types. Single nubbins grew faster than whole colonies, but when aggregated, nubbins changed calcification to match whole colonies even though they lacked integration among branches. Corallum morphology causes the phenotype of branching corals to differ from the summation of their branches.

Stony coral populations are more sensitive to changes in vital rates in disturbed environments.

Reef-building corals, like many long-lived organisms, experience environmental change as a combination of separate but concurrent processes, some of which are gradual yet long-lasting, while others are more acute but short-lived. For corals, some chronic environmental stressors, such as rising temperature and ocean acidification, are thought to induce gradual changes in colonies' vital rates. Meanwhile, other environmental changes, such as the intensification of tropical cyclones, change the disturbance regime that corals experience. Here, we use a physiologically structured population model to explore how chronic environmental stressors that impact the vital rates of individual coral colonies interact with the intensity and magnitude of disturbance to affect coral population dynamics and cover. We find that, when disturbances are relatively benign, intraspecific density dependence driven by space competition partially buffers coral populations against gradual changes in vital rates. However, the impact of chronic stressors is amplified in more highly disturbed environments, because disturbance weakens the buffering effect of space competition. We also show that coral cover is more sensitive to changes in colony growth and mortality than to external recruitment, at least in open populations, and that space competition and size structure mediate the extent and pace of coral population recovery following a large-scale mortality event. Understanding the complex interplay among chronic environmental stressors, mass-mortality events, and population size structure sharpens our ability to manage and to restore coral-reef ecosystems in an increasingly disturbed future.

Recruitment hotspots and bottlenecks mediate the distribution of corals on a Caribbean reef.

Recruitment hotspots are locations where organisms are added to populations at high rates. On tropical reefs where coral abundance has declined, recruitment hotspots are important because they have the potential to promote population recovery. Around St. John, US Virgin Islands, coral recruitment at five sites revealed a hotspot that has persistent for 14 years. Recruitment created a hotspot in density of juvenile corals that was 600 m southeast of the recruitment hotspot. Neither hotspot led to increased coral cover, thus revealing the stringency of the demographic bottleneck impeding progression of recruits to adult sizes and preventing population growth. Recruitment hotspots in low-density coral populations are valuable targets for conservation and sources of corals for restoration.

Emergent properties of branching morphologies modulate the sensitivity of coral calcification to high PCO2.

Experiments with coral fragments (i.e. nubbins) have shown that net calcification is depressed by elevated PCO2 Evaluating the implications of this finding requires scaling of results from nubbins to colonies, yet the experiments to codify this process have not been carried out. Building from our previous research demonstrating that net calcification of Pocillopora verrucosa (2-13 cm diameter) was unaffected by PCO2  (400 and 1000 µatm) and temperature (26.5 and 29.7°C), we sought generality to this outcome by testing how colony size modulates PCO2  and temperature sensitivity in a branching acroporid. Together, these taxa represent two of the dominant lineages of branching corals on Indo-Pacific coral reefs. Two trials conducted over 2 years tested the hypothesis that the seasonal range in seawater temperature (26.5 and 29.2°C) and a future PCO2  (1062 µatm versus an ambient level of 461 µatm) affect net calcification of an ecologically relevant size range (5-20 cm diameter) of colonies of Acropora hyacinthus As for P. verrucosa, the effects of temperature and PCO2  on net calcification (mg day-1) of A. verrucosa were not statistically detectable. These results support the generality of a null outcome on net calcification of exposing intact colonies of branching corals to environmental conditions contrasting seasonal variation in temperature and predicted future variation in PCO2 While there is a need to expand beyond an experimental culture relying on coral nubbins as tractable replicates, rigorously responding to this need poses substantial ethical and logistical challenges.

Science-based approach to using growth rate to assess coral performance and restoration outcomes.

One response to the coral reef crisis has been human intervention to enhance selection on the fittest corals through cultivation. This requires genotypes to be identified for intervention, with a primary basis for this choice being growth: corals that quickly grow on contemporary reefs might be future winners. To test for temporal stability of growth as a predictor of future performance, genotypes of the coral Porites spp. were grown in common gardens in Mo'orea, French Polynesia. Growth was measured every two to four months throughout 2018, and each period was used as a predictor of growth over the subsequent period. Area-normalized growth explained less than 29% of the variance in subsequent growth, but for biomass-normalized growth this increased to 45-60%, and was highest when summer growth was used to predict autumn growth. The capacity of initial growth to predict future performance is dependent on the units of measurement and the time of year in which it is measured. The final choice of traits to quantify performance must be informed through consideration of the species and the normalization that best capture the information inherent in the biological processes mediating variation in traits values.

Three decades of degradation lead to diminished impacts of severe hurricanes on Caribbean reefs.

Major tropical storms are destructive phenomena with large effects on the community dynamics of multiple biomes. On coral reefs, their impacts have been described for decades, leading to the expectation that future storms should have effects similar to those recorded in the past. This expectation relies on the assumption that storm intensities will remain unchanged, and the impacted coral reef communities are similar to those of the recent past; neither assumption is correct. This study quantified the effects of two category five hurricanes on the reefs of St. John, U.S. Virgin Islands, where 31 yr of time-series analyses reveal chronic coral mortality, increasing macroalgal abundance, and five major hurricanes that caused acute coral mortality. Contextualized by these trends, the effects of the most recent storms, Hurricanes Irma and Maria (September 2017), on coral cover were modest. While mean absolute coral cover declined 1-4% depending on site, these effects were not statistically discernable. Following decades of increasing abundance of macroalgae, this functional group responded to the recent hurricanes with large increases in abundance on both absolute and relative scales. Decades of chronic mortality have changed the coral assemblages of St. John to create degraded communities that are resistant to severe storms.

Density-dependence mediates coral assemblage structure.

Density dependence (DD) controls community recovery following widespread mortality, yet this principle rarely has been applied to coral assemblages. The reefs of Mo'orea, French Polynesia, provide the opportunity to study DD of coral population growth, because coral assemblages in this location responded to declines in abundance with high recruitment and an increase in cover during which recruitment of pocilloporid corals was inversely associated with density. This study tests for DD in this system, first, by describing the context within which it operates: coral cover changed from 46% in 2005, to <1% in 2010 following an outbreak of a corallivorous sea star and a cyclone, and then increased to 74% by 2017, in large part through inverse density-associated pocilloporid recruitment. Second, a test for DD of recruitment was conducted by decreasing Pocillopora spp. cover from 33% to 19%: one year later, the density of Pocillopora spp. recruits was 1.65-fold higher in the low vs. high cover treatment. Finally, the effects of DD were investigated by comparing simulated and empirical distributions of pocilloporid colonies: as predicted by DD, small colonies were randomly distributed, while large colonies were uniformly distributed. Together these results demonstrate DD of population regulation for Pocillopora spp. corals, thus revealing the potential importance of this ecological principle in determining the resilience of coral assemblages.

Intraspecific variation in growth rate is a poor predictor of fitness for reef corals.

Genetic variation underlying differences in organism performance is subject to natural selection, and organisms with high values of genetically determined phenotypic measures of fitness should perform better than those that do not. Using small scleractinian corals (i.e., ≤40-mm diameter), this principle was tested with 20 yr of census data from St. John, US Virgin Islands. Using growth rate (change in diameter) as a measure of fitness, growth in one year was tested for association with growth and survivorship in the following two years, and this process was repeated over 20 yr using a 3-yr sliding window. Virtually all variation in growth was independent of colony size, and growth among pairs of years was highly variable, with corals that grew fast in one year rarely growing fast in the next 2 yr. While growth in some pairs of years was positively correlated, ≤4% of the growth variance was explained by growth in the preceding 2 yr. Survivorship was related positively to growth in the preceding year, but the association was weak, it did not extend over 3 yr, and was inconsistent over the study. These results demonstrate the importance of the environment in translating phenotypic measures of fitness into future performance, and for small Caribbean corals, they suggest that environmental conditions may preempt genotype in determining short-term success.

Conspecific aggregations mitigate the effects of ocean acidification on calcification of the coral Pocillopora verrucosa.

In densely populated communities, such as coral reefs, organisms can modify the physical and chemical environment for neighbouring individuals. We tested the hypothesis that colony density (12 colonies each placed ∼0.5 cm apart versus ∼8 cm apart) can modulate the physiological response (measured through rates of calcification, photosynthesis and respiration in the light and dark) of the coral Pocillopora verrucosa to partial pressure of CO2 (PCO2 ) treatments (∼400 µatm and ∼1200 µatm) by altering the seawater flow regimes experienced by colonies placed in aggregations within a flume at a single flow speed. While light calcification decreased 20% under elevated versus ambient PCO2  for colonies in low-density aggregations, light calcification of high-density aggregations increased 23% at elevated versus ambient PCO2 As a result, densely aggregated corals maintained calcification rates over 24 h that were comparable to those maintained under ambient PCO2 , despite a 45% decrease in dark calcification at elevated versus ambient PCO2 Additionally, densely aggregated corals experienced reduced flow speeds and higher seawater retention times between colonies owing to the formation of eddies. These results support recent indications that neighbouring organisms, such as the conspecific coral colonies in the present example, can create small-scale refugia from the negative effects of ocean acidification.

Framework of barrier reefs threatened by ocean acidification.

To date, studies of ocean acidification (OA) on coral reefs have focused on organisms rather than communities, and the few community effects that have been addressed have focused on shallow back reef habitats. The effects of OA on outer barrier reefs, which are the most striking of coral reef habitats and are functionally and physically different from back reefs, are unknown. Using 5-m long outdoor flumes to create treatment conditions, we constructed coral reef communities comprised of calcified algae, corals, and reef pavement that were assembled to match the community structure at 17 m depth on the outer barrier reef of Moorea, French Polynesia. Communities were maintained under ambient and 1200 µatm pCO2 for 7 weeks, and net calcification rates were measured at different flow speeds. Community net calcification was significantly affected by OA, especially at night when net calcification was depressed ~78% compared to ambient pCO2 . Flow speed (2-14 cm s(-1) ) enhanced net calcification only at night under elevated pCO2 . Reef pavement also was affected by OA, with dissolution ~86% higher under elevated pCO2 compared to ambient pCO2 . These results suggest that net accretion of outer barrier reef communities will decline under OA conditions predicted within the next 100 years, largely because of increased dissolution of reef pavement. Such extensive dissolution poses a threat to the carbonate foundation of barrier reef communities.

Size-dependent physiological responses of the branching coral Pocillopora verrucosa to elevated temperature and PCO2.

Body size has large effects on organism physiology, but these effects remain poorly understood in modular animals with complex morphologies. Using two trials of a ∼24 day experiment conducted in 2014 and 2015, we tested the hypothesis that colony size of the coral Pocillopora verrucosa affects the response of calcification, aerobic respiration and gross photosynthesis to temperature (∼26.5 and ∼29.7°C) and PCO2  (∼40 and ∼1000 µatm). Large corals calcified more than small corals, but at a slower size-specific rate; area-normalized calcification declined with size. Whole-colony and area-normalized calcification were unaffected by temperature, PCO2 , or the interaction between the two. Whole-colony respiration increased with colony size, but the slopes of these relationships differed between treatments. Area-normalized gross photosynthesis declined with colony size, but whole-colony photosynthesis was unaffected by PCO2 , and showed a weak response to temperature. When scaled up to predict the response of large corals, area-normalized metrics of physiological performance measured using small corals provide inaccurate estimates of the physiological performance of large colonies. Together, these results demonstrate the importance of colony size in modulating the response of branching corals to elevated temperature and high PCO2.

The implications of reduced metabolic rate in resource-limited corals.

Many organisms exhibit depressed metabolism when resources are limited, a change that makes it possible to balance an energy budget. For symbiotic reef corals, daily cycles of light and periods of intense cloud cover can be chronic causes of food limitation through reduced photosynthesis. Furthermore, coral bleaching is common in present-day reefs, creating a context in which metabolic depression could have beneficial value to corals. In the present study, corals (massive Porites spp.) were exposed to an extreme case of resource limitation by starving them of food and light for 20 days. When resources were limited, the corals depressed area-normalized respiration to 37% of initial rates, and coral biomass declined to 64% of initial amounts, yet the corals continued to produce skeletal mass. However, the declines in biomass cannot account for the declines in area-normalized respiration, as mass-specific respiration declined to 30% of the first recorded time point. Thus, these corals appear to be capable of metabolic depression. It is possible that some coral species are better able to depress metabolic rates than others; such variation could explain differential survival during conditions that limit resources (e.g. shading). Furthermore, we found that maintenance of existing biomass, in part, supports the production of skeletal mass. This association could be explained if maintenance supplies needed energy (e.g. ATP) or inorganic carbon (i.e. CO2) that otherwise limits the production of skeletal mass. Finally, the observed metabolic depression can be explained as a change in pool sizes, and does not require a change in metabolic rules.

Stability of Caribbean coral communities quantified by long-term monitoring and autoregression models.

Tropical coral reefs exemplify ecosystems imperiled by environmental change. Anticipating the future of reef ecosystems requires understanding how scleractinian corals respond to the multiple environmental disturbances that threaten their survival. We analyzed the stability of coral reefs at three habitats at different depths along the south shore of St. John, U.S. Virgin Islands, using multivariate autoregression (MAR) models and two decades of monitoring data. We quantified several measures of ecosystem stability, including the magnitude of typical stochastic fluctuations, the rate of recovery following disturbance, and the sensitivity of coral cover to hurricanes and elevated sea temperature. Our results show that, even within a -4 km shore, coral communities in different habitats display different stability properties, and that the stability of each habitat corresponds with the habitat's known synecology. Two Orbicella-dominated habitats are less prone to annual stochastic fluctuations than coral communities in shallower water, but they recover slowly from disturbance, and one habitat has suffered recent losses in scleractinian cover that will not be quickly reversed. In contrast, a shallower, low-coral-cover habitat is subject to greater stochastic fluctuations, but rebounds more quickly from disturbance and is more robust to hurricanes and seawater warming. In some sense, the shallower community is more stable, although the stability arguably arises from having little coral cover left. Our results sharpen understanding of recent changes in coral communities at these habitats, provide a more detailed understanding of how these habitats may change in future environments, and illustrate how MAR models can be used to assess stability of communities founded upon long-lived species.

What makes a species common? No evidence of density-dependent recruitment or mortality of the sea urchin Diadema antillarum after the 1983-1984 mass mortality.

A potential consequence of individuals compensating for density-dependent processes is that rare or infrequent events can produce profound and long-term shifts in species abundance. In 1983-1984 a mass mortality event reduced the numbers of the abundant sea urchin Diadema antillarum by 95-99% throughout the Caribbean and western Atlantic. Following this event, the abundance of macroalgae increased and the few surviving D. antillarum responded by increasing in body size and fecundity. These initial observations suggested that populations of D. antillarum could recover rapidly following release from food limitation. In contrast, published studies of field manipulations indicate that this species had traits making it resistant to density-dependent effects on offspring production and adult mortality; this evidence raises the possibility that density-independent processes might keep populations at a diminished level. Decadal-scale (1983-2011) monitoring of recruitment, mortality, population density and size structure of D. antillarum from St John, US Virgin Islands, indicates that population density has remained relatively stable and more than an order of magnitude lower than that before the mortality event of 1983-1984. We detected no evidence of density-dependent mortality or recruitment since this mortality event. In this location, model estimates of equilibrium population density, assuming density-independent processes and based on parameters generated over the first decade following the mortality event, accurately predict the low population density 20 years later (2011). We find no evidence to support the notion that this historically dominant species will rebound from this temporally brief, but spatially widespread, perturbation.

Decadal-scale time series highlight the role of chronic disturbances in driving ecosystem collapse in the Anthropocene.

Biome degradation characterizes the Anthropocene Epoch, and modern ecology is deeply involved with describing the changes underway. Most research has focused on the role of acute disturbances in causing conspicuous changes in ecosystem structure, which leads to an underappreciation of the chronic effects causing large changes through the cumulative effects of small perturbations over decades. Coral reefs epitomize this trend, because the changes in community structure are profound, yet the data to quantify these effects are usually insufficient to evaluate the relative roles of different disturbance types. Here, four decades of surveys from two coral reefs (9 and 14 m depth) off St. John, US Virgin Islands, are used to quantify the associations of acute and chronic events with the changes in benthic community structure. These reefs profoundly changed over 36 years, with coral death altering species assemblages to depress abundances of the ecologically important coral Orbicella spp. and elevating the coverage of macroalgae and crustose coralline algae/turf/bare space (CTB). Linear mixed models revealed the prominent role of chronic variation in temperature in accounting for changes in coverage of corals, macroalgae, and CTB, with rising temperature associated with increases in coral cover on the deep reef, and declines on the shallow reef. Hurricanes were also associated with declines in coral cover on the shallow reef, and increases on the deep reef. Multivariate analyses revealed strong associations between community structure and temperature, but weaker associations with hurricanes, bleaching, and diseases. These results highlight the overwhelming importance of chronically increasing temperature in altering the benthic community structure of Caribbean reefs.