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.

The rising threat of peyssonnelioid algal crusts on coral reefs.

For more than a century, coral reefs have been exposed to increasing anthropogenic disturbances that have profoundly altered their community structure. These perturbations continue to challenge coral reefs in new ways as ecological paradigms are recast in the Anthropocene Epoch1. In recent decades, macroalgal blooms have blighted Caribbean reefs2, but the appearance of aggressive peyssonnelioid algal crusts (PAC) that are rapidly increasing in abundance to become dominant members of the benthos on Caribbean and Indo-Pacific reefs is a novel phenomenon in tropical seas3. By pre-empting vacant space, overgrowing corals, deterring the settlement of coral larvae, and favouring a phase transition from coral to algae4, PAC are likely to accelerate the decline in dominance of corals on global reefs (Figure 1).

Coral recruitment: patterns and processes determining the dynamics of coral populations.

Coral recruitment describes the addition of new individuals to populations, and it is one of the most fundamental demographic processes contributing to population size. As many coral reefs around the world have experienced large declines in coral cover and abundance, there has been great interest in understanding the factors causing coral recruitment to vary and the conditions under which it can support community resilience. While progress in these areas is being facilitated by technological and scientific advances, one of the best tools to quantify recruitment remains the humble settlement tile, variants of which have been in use for over a century. Here I review the biology and ecology of coral recruits and the recruitment process, largely as resolved through the use of settlement tiles, by: (i) defining how the terms 'recruit' and 'recruitment' have been used, and explaining why loose terminology has impeded scientific advancement; (ii) describing how coral recruitment is measured and why settlement tiles have value for this purpose; (iii) summarizing previous efforts to review quantitative analyses of coral recruitment; (iv) describing advances from hypothesis-driven studies in determining how refuges, seawater flow, and grazers can modulate coral recruitment; (v) reviewing the biology of small corals (i.e. recruits) to understand better how they respond to environmental conditions; and (vi) updating a quantitative compilation of coral recruitment studies extending from 1974 to present, thus revealing long-term global declines in density of recruits, juxtaposed with apparent resilience to coral bleaching. Finally, I review future directions in the study of coral recruitment, and highlight the need to expand studies to deliver taxonomic resolution, and explain why time series of settlement tile deployments are likely to remain pivotal in quantifying coral recruitment.

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.

Hidden heatwaves and severe coral bleaching linked to mesoscale eddies and thermocline dynamics.

The severity of marine heatwaves (MHWs) that are increasingly impacting ocean ecosystems, including vulnerable coral reefs, has primarily been assessed using remotely sensed sea-surface temperatures (SSTs), without information relevant to heating across ecosystem depths. Here, using a rare combination of SST, high-resolution in-situ temperatures, and sea level anomalies observed over 15 years near Moorea, French Polynesia, we document subsurface MHWs that have been paradoxical in comparison to SST metrics and associated with unexpected coral bleaching across depths. Variations in the depth range and severity of MHWs was driven by mesoscale (10s to 100s of km) eddies that altered sea levels and thermocline depths and decreased (2007, 2017 and 2019) or increased (2012, 2015, 2016) internal-wave cooling. Pronounced eddy-induced reductions in internal waves during early 2019 contributed to a prolonged subsurface MHW and unexpectedly severe coral bleaching, with subsequent mortality offsetting almost a decade of coral recovery. Variability in mesoscale eddy fields, and thus thermocline depths, is expected to increase with climate change, which, along with strengthening and deepening stratification, could increase the occurrence of subsurface MHWs over ecosystems historically insulated from surface ocean heating by the cooling effects of internal waves.

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.

A decade of invertebrate recruitment at Santa Catalina Island, California.

Marine fouling communities have long provided model systems for studying the ecology of community development, and settlement plates are the tool of choice for this purpose. Decades of plate deployments provide a baseline against which present-day trends can be interpreted, with one classic trend being the ultimate dominance of plates by colonial and encrusting taxa. Here we report the results of annual deployments of settlement plates from 2010 to 2021 in the shallow sub-tidal of southern California, where the recruitment of invertebrates and algae was recorded photographically, and resolved to functional group (solitary, encrusting, and arborescent) and the lowest taxon possible. The communities on these plates differed among years, with trends in abundances varying by functional group and taxon; solitary taxa consistently were abundant, but encrusting taxa declined in abundance. Seawater temperature and the subsurface concentration of chlorophyll a differed among years, and there was a weak inverse association between temperature and the abundances of encrusting taxa. Long-term increases in seawater temperature therefore could serve as a mechanism causing fouling communities to change. Because of the prominence of encrusting taxa in fouling communities, the shifts in abundance of this functional group reported here may portend ecologically significant changes in fouling communities exposed to warmer seawater because of an alleviation of competition for a classically limiting resource (i.e., space).

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.

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.

Scaling the effects of ocean acidification on coral growth and coral-coral competition on coral community recovery.

Ocean acidification (OA) is negatively affecting calcification in a wide variety of marine organisms. These effects are acute for many tropical scleractinian corals under short-term experimental conditions, but it is unclear how these effects interact with ecological processes, such as competition for space, to impact coral communities over multiple years. This study sought to test the use of individual-based models (IBMs) as a tool to scale up the effects of OA recorded in short-term studies to community-scale impacts, combining data from field surveys and mesocosm experiments to parameterize an IBM of coral community recovery on the fore reef of Moorea, French Polynesia. Focusing on the dominant coral genera from the fore reef, Pocillopora, Acropora, Montipora and Porites, model efficacy first was evaluated through the comparison of simulated and empirical dynamics from 2010-2016, when the reef was recovering from sequential acute disturbances (a crown-of-thorns seastar outbreak followed by a cyclone) that reduced coral cover to ~0% by 2010. The model then was used to evaluate how the effects of OA (1,100-1,200 µatm pCO2) on coral growth and competition among corals affected recovery rates (as assessed by changes in % cover y-1) of each coral population between 2010-2016. The model indicated that recovery rates for the fore reef community was halved by OA over 7 years, with cover increasing at 11% y-1 under ambient conditions and 4.8% y-1 under OA conditions. However, when OA was implemented to affect coral growth and not competition among corals, coral community recovery increased to 7.2% y-1, highlighting mechanisms other than growth suppression (i.e., competition), through which OA can impact recovery. Our study reveals the potential for IBMs to assess the impacts of OA on coral communities at temporal and spatial scales beyond the capabilities of experimental studies, but this potential will not be realized unless empirical analyses address a wider variety of response variables representing ecological, physiological and functional domains.

Response diversity in corals: hidden differences in bleaching mortality among cryptic Pocillopora species.

Variation among functionally similar species in their response to environmental stress buffers ecosystems from changing states. Functionally similar species may often be cryptic species representing evolutionarily distinct genetic lineages that are morphologically indistinguishable. However, the extent to which cryptic species differ in their response to stress, and could therefore provide a source of response diversity, remains unclear because they are often not identified or are assumed to be ecologically equivalent. Here, we uncover differences in the bleaching response between sympatric cryptic species of the common Indo-Pacific coral, Pocillopora. In April 2019, prolonged ocean heating occurred at Moorea, French Polynesia. 72% of pocilloporid colonies bleached after 22 d of severe heating (>8o C-days) at 10 m depth on the north shore fore reef. Colony mortality ranged from 11% to 42% around the island four months after heating subsided. The majority (86%) of pocilloporids that died from bleaching belonged to a single haplotype, despite twelve haplotypes, representing at least five species, being sampled. Mitochondrial (open reading frame) sequence variation was greater between the haplotypes that experienced mortality versus haplotypes that all survived than it was between nominal species that all survived. Colonies > 30 cm in diameter were identified as the haplotype experiencing the most mortality, and in 1125 colonies that were not genetically identified, bleaching and mortality increased with colony size. Mortality did not increase with colony size within the haplotype suffering the highest mortality, suggesting that size-dependent bleaching and mortality at the genus level was caused instead by differences among cryptic species. The relative abundance of haplotypes shifted between February and August, driven by declines in the same common haplotype for which mortality was estimated directly, at sites where heat accumulation was greatest, and where larger colony sizes occurred. The identification of morphologically indistinguishable species that differ in their response to thermal stress, but share a similar ecological function in terms of maintaining a coral-dominated state, has important consequences for uncovering response diversity that drives resilience, especially in systems with low or declining functional diversity.

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.

Projected shifts in coral size structure in the Anthropocene.

Changes in the size structure of coral populations have major consequences for population dynamics and community function, yet many coral reef monitoring projects do not record this critical feature. Consequently, our understanding of current and future trajectories in coral size structure, and the demographic processes underlying these changes, is still emerging. Here, we provide a conceptual summary of the benefits to be gained from more comprehensive attention to the size of coral colonies in reef monitoring projects, and we support our argument through the use of case-history examples and a simplified ecological model. We neither seek to review the available empirical data, or to rigorously explore causes and implications of changes in coral size, we seek to reveal the advantages to modifying ongoing programs to embrace the information inherent in changing coral colony size. Within this framework, we evaluate and forecast the mechanics and implications of changes in the population structure of corals that are transitioning from high to low abundance, and from large to small colonies, sometimes without striking effects on planar coral cover. Using two coral reef locations that have been sampled for coral size, we use demographic data to underscore the limitations of coral cover in understanding the causes and consequences of long-term declining coral size, and abundance. A stage-structured matrix model is used to evaluate the demographic causes of declining coral colony size and abundance, particularly with respect to the risks of extinction. The model revealed differential effects of mortality, growth and fecundity on coral size distributions. It also suggested that colony rarity and declining colony size in association with partial tissue mortality and chronic declines in fecundity, can lead to a demographic bottleneck with the potential to prolong the existence of coral populations when they are characterized by mostly very small colonies. Such bottlenecks could have ecological importance if they can delay extinction and provide time for human intervention to alleviate the environmental degradation driving reductions in coral abundance.

The rise of octocoral forests on Caribbean reefs.

Coral reefs throughout the tropics have experienced large declines in the abundance of scleractinian corals over the last few decades, and some reefs are becoming functionally dominated by animal taxa other than scleractinians. This phenomenon is striking on many shallow reefs in the tropical western Atlantic, where arborescent octocorals now are numerically and functionally dominant. Octocorals are one of several taxa that have been overlooked for decades in analyses of coral reef community dynamics, and our understanding of why octocorals are favoured (whereas scleractinians are not) on some modern reefs, and how they will affect the function of future reef communities, is not commensurate with the task of scientifically responding to the coral reef crisis. We summarize the biological and ecological features predisposing octocorals for success under contemporary conditions, and focus on those features that could have generated resistance and resilience of octocoral populations to environmental change on modern reefs. There is a rich set of opportunities for rapid advancement in understanding the factors driving the success of octocorals on modern reefs, but we underscore three lines of inquiry: (1) the functional implications of strongly mixotrophic, polytrophic, and plastic nutrition, (2) the capacity to recruit at high densities and maintain rapid initial rates of vertical growth, and (3) the emergent properties associated with dense animal forests at high colony densities.

An unusual microbiome characterises a spatially-aggressive crustose alga rapidly overgrowing shallow Caribbean reefs.

Several species of crustose coralline algae (CCA) and their associated microbial biofilms play important roles in determining the settlement location of scleractinian corals on tropical reefs. In recent decades, peyssonnelid algal crusts (PAC) have become spatial dominants across large areas of shallow Caribbean reefs, where they appear to deter the recruitment of scleractinians. Our genetic investigations of PAC in St. John, US Virgin Islands, amplifying the large-subunit ribosomal RNA and psbA protein D1 marker genes, revealed them to be identical to Ramicrusta textilis previously reported overgrowing corals in Jamaica. Specimens of PAC sampled from the Honduras were likewise identical, confirming that this crustose alga inhabits the easternmost and westernmost regions of the Caribbean. We also analysed 16S rDNA tag amplicon libraries of the biofilms associated with PAC and sympatric CCA, which is favoured for coral settlement. Our results show that the microbial communities on PAC (vs. CCA) are characterized by significantly lower numbers of the epibiotic bacterial genus Pseudoalteromonas, which facilitates the recruitment and settlement of marine invertebrates. From these data, we infer that PAC are therefore unlikely to be attractive as settlement sites for coral larvae. Given the significant ecological change anticipated on these reefs due to increasing cover of PAC, there is an urgent need to further investigate competitive interactions between PAC and scleractinian corals, and elucidate the role of PAC and their associated microbiomes in accentuating phase shifts from coral to algae on tropical reefs.

High ecological resilience of the sea fan Gorgonia ventalina during two severe hurricanes.

Since about the turn of the millennium, octocorals have been increasing in abundance on Caribbean reefs. The mechanisms underlying this trend have not been resolved, but the emergent species assemblage appears to be more resilient than the scleractinians they are replacing. The sea fan Gorgonia ventalina is an iconic species in the contemporary octocoral fauna, and here its population dynamics are described from St. John, US Virgin Islands, from 2013 to 2019. Mean densities of G. ventalina at Yawzi Point (9-m depth) varied from 1.4-1.5 colonies m-2, and their mean heights from 24-30 cm; nearby at Tektite (14-m depth), they varied from 0.6-0.8 colonies m-2 and from 25-33 cm. These reefs were impacted by two Category 5 hurricanes in 2017, but neither the density of G. ventalina, the density of their recruits (< 5-cm tall), nor the height of colonies, differed among years, although growth was depressed after the hurricanes. Nevertheless, at Tektite, colony height trended upwards over time, in part because colonies 10.1-20 cm tall were reduced in abundance after the hurricanes. These trends were sustained without density-associated effects mediating recruitment or self-thinning of adults. The dynamics of G. ventalina over seven years reveals the high resilience of this species that will contribute to the persistence of octocorals as a dominant state on Caribbean reefs.

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.

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.