Coming of age: Annual onset of coral reproduction is determined by age rather than size.

Constraints on organisms possessing a unitary body plan appear almost absent from colonial organisms. Like unitary organisms, however, coral colonies seemingly delay reproduction until reaching a critical size. Elucidating ontogenetic processes, such as puberty and aging are complicated by corals' modular design, where partial mortality and fragmentation lead to distortions in colony size-age relationships. We explored these enigmatic relations and their influence on reproduction by fragmenting sexually mature colonies of five coral species into sizes below the known size at first reproduction, nurturing them for prolonged periods, and examining their reproductive capacity and trade-offs between growth rates and reproductive investment. Most fragments were reproductive regardless of their size, and growth rates hardly affected reproduction. Our findings suggest that once the ontogenetic milestone of puberty is reached, corals retain reproductive capacity irrespective of colony size, highlighting the key role that aging may have in colonial animals, which are commonly considered non-aging.

Oceanic differences in coral-bleaching responses to marine heatwaves.

Anomalously high ocean temperatures have increased in frequency, intensity, and duration over the last several decades because of greenhouse gas emissions that cause global warming and marine heatwaves. Reef-building corals are sensitive to such temperature anomalies that commonly lead to coral bleaching, mortality, and changes in community structure. Yet, despite these overarching effects, there are geographical differences in thermal regimes, evolutionary histories, and past disturbances that may lead to different bleaching responses of corals within and among oceans. Here we examined the overall bleaching responses of corals in the Atlantic, Indian, and Pacific Oceans, using both a spatially explicit Bayesian mixed-effects model and a deep-learning neural-network model. We used a 40-year global dataset encompassing 23,288 coral-reef surveys at 11,058 sites in 88 countries, from 1980 to 2020. Focusing on ocean-wide differences we assessed the relationships between the percentage of bleached corals and different temperature-related metrics alongside a suite of environmental variables. We found that while high sea-surface temperatures were consistently, and strongly, related to coral bleaching within all oceans, there were clear geographical differences in the relationships between coral bleaching and most environmental variables. For instance, there was an increase in coral bleaching with depth in the Atlantic Ocean whereas the opposite was observed in the Indian Ocean, and no clear trend could be seen in the Pacific Ocean. The standard deviation of thermal-stress anomalies was negatively related to coral bleaching in the Atlantic and Pacific Oceans, but not in the Indian Ocean. Globally, coral bleaching has progressively occurred at higher temperatures over the last four decades within the Atlantic, Indian, and Pacific Oceans, although, again, there were differences among the three oceans. Together, such patterns highlight that historical circumstances and geographical differences in oceanographic conditions play a central role in contemporary coral-bleaching responses.

Soft coral reproductive phenology along a depth gradient: Can "going deeper" provide a viable refuge?

Many species across a wide range of taxa and habitats display phenological shifts and differences in response to both environmental gradients and climate change. Moreover, the wide-scale decline of numerous ecosystems is leading to increasing efforts to identify zones that might serve as natural refuges from various disturbances, including ocean warming. One such refuge was suggested to be that of the deep coral reefs, but whether depth can provide coral populations with a viable and reproductive refuge remains unclear. Given the global coral-reef degradation and the key role that corals play as ecosystem engineers, their reproductive ecology has been widely studied. A particular knowledge gap nonetheless exists regarding coral reproductive phenology along a depth gradient. Filling in this gap may uncover the environmental cues that regulate coral reproduction, leading to better predictions of population connectivity, and their possible responses to climate change and other environmental changes. Here, using long-term in situ observations of the soft coral Rhytisma fulvum's reproductive activity along its entire depth range (0-45 m), we examined the relationship among several environmental factors and the coral's reproductive phenology and activity over five successive annual breeding seasons. Compared with the shallow depths, a lower number of reproducing colonies was found in habitats deeper than 30 m, highlighting possible constraints on coral reproduction at the deeper end of their range. Our results further revealed that an increase in seawater temperature over 1-2-day intervals during the breeding season correlated with the onset of reproductive activity along the depth gradient, leading to different reproductive periodicities in different depths. These differences suggest that differential temperature regimes and reproductive timing across depth may create intraspecific temporal reproductive segregation, possibly reducing connectivity among populations along a depth gradient. Moreover, we found high variability among years in both the timing of breeding activities and in the level of reproductive synchrony among corals from different depths. Overall, our study questions whether depth can provide a long-term and viable refuge for corals in the face of global environmental changes.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

pH variability at volcanic CO2 seeps regulates coral calcifying fluid chemistry.

Coral reefs are iconic ecosystems with immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification (OA). Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance in predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO2 seeps in Papua New Guinea to assess their capacity to control their calcifying fluid (CF) chemistry. Several coral species living under conditions of low mean seawater pH, but with either low or high variability in seawater pH, were examined and compared with those living in 'normal' (non-seep) ambient seawater pH. We show that when mean seawater pH is low but highly variable, corals have a greater ability to maintain constant pHcf in their CF, but this characteristic was not linked with changes in abundance. Within less variable low pH seawater, corals with limited reductions in pHcf at the seep sites compared with controls tended to be more abundant at the seep site than at the control site. However, this finding was strongly influenced by a single species (Montipora foliosa), which was able to maintain complete pHcf homeostasis. Overall, although our findings indicate that there might be an association between ecological success and greater pHcf homeostasis, further research with additional species and at more sites with differing seawater pH regimes is required to solidify inferences regarding coral ecological success under future OA.

Biogeography, reproductive biology and phylogenetic divergence within the Fungiidae (mushroom corals).

While the escalating impacts of climate change and other anthropogenic pressures on coral reefs are well documented at the coral community level, studies of species-specific trends are less common, owing mostly to the difficulties and uncertainties in delineating coral species. It has also become clear that traditional coral taxonomy based largely on skeletal macromorphology has underestimated the diversity of many coral families. Here, we use targeted enrichment methods to sequence 2476 ultraconserved elements (UCEs) and exonic loci to investigate the relationship between populations of Fungia fungites from Okinawa, Japan, where this species reproduces by brooding (i.e., internal fertilization), and Papua New Guinea and Australia, where it reproduces by broadcast-spawning (i.e., external fertilization). Moreover, we analyzed the relationships between populations of additional fungiid species (Herpolitha limax and Ctenactis spp.) that reproduce only by broadcast-spawning. Our phylogenetic and species delimitation analyses reveal strong biogeographic structuring in both F. fungites and Herpolitha limax, consistent with cryptic speciation in Okinawa in both species and additionally for H. limax in the Red Sea. By combining UCE/exon data and mitochondrial sequences captured in off-target reads, we reinforce earlier findings that Ctenactis, a genus consisting of three nominal morphospecies, is not a natural group. Our results highlight the need for taxonomic and systematic re-evaluations of some species and genera within the family Fungiidae. This work demonstrates that sequence data generated by the application of targeted capture methods can provide objective criteria by which we can test phylogenetic hypotheses based on morphological and/or life history traits.

Local conditions magnify coral loss after marine heatwaves.

Climate change threatens coral reefs by causing heat stress events that lead to widespread coral bleaching and mortality. Given the global nature of these mass coral mortality events, recent studies argue that mitigating climate change is the only path to conserve coral reefs. Using a global analysis of 223 sites, we show that local stressors act synergistically with climate change to kill corals. Local factors such as high abundance of macroalgae or urchins magnified coral loss in the year after bleaching. Notably, the combined effects of increasing heat stress and macroalgae intensified coral loss. Our results offer an optimistic premise that effective local management, alongside global efforts to mitigate climate change, can help coral reefs survive the Anthropocene.

Different population trajectories of two reef-building corals with similar life-history traits.

Increases in the frequency and intensity of acute and chronic disturbances are causing declines of coral reefs world-wide. Although quantifying the responses of corals to acute disturbances is well documented, detecting subtle responses of coral populations to chronic disturbances is less common, but can also result in altered population and community structures. We investigated the population dynamics of two key reef-building Merulinid coral species, Dipsastraea favus and Platygyra lamellina, with similar life-history traits, in the Gulf of Eilat and Aqaba, Red Sea from 2015 to 2018, to assess potential differences in their population trajectories. Demographic processes, which included rates of survival, growth, reproduction and recruitment were used to parametrize integral projection models and estimate population growth rates and the likely population trajectories of both coral species. The survival and reproduction rates of both D. favus and P. lamellina were positively related to coral colony size, and elasticity analyses showed that large colonies most influenced population dynamics. Although both species have similar life-history traits and growth morphologies and are generally regarded as 'stress-tolerant', the populations showed contrasting trajectories-D. favus appears to be increasing whereas P. lamellina appears to be decreasing. As many corals have long-life expectancies, the process of local and regional decline might be subtle and slow. Ecological assessments based on total living coral coverage, morphological groups or functional traits might overlook subtle, species-specific trends. However, demographic approaches capable of detecting subtle species-specific population changes can augment ecological studies and provide valuable early warning signs of decline before major coral loss becomes evident.

Depth-dependent parental effects create invisible barriers to coral dispersal.

Historically, marine populations were considered to be interconnected across large geographic regions due to the lack of apparent physical barriers to dispersal, coupled with a potentially widely dispersive pelagic larval stage. Recent studies, however, are providing increasing evidence of small-scale genetic segregation of populations across habitats and depths, separated in some cases by only a few dozen meters. Here, we performed a series of ex-situ and in-situ experiments using coral larvae of three brooding species from contrasting shallow- and deep-water reef habitats, and show that their settlement success, habitat choices, and subsequent survival are substantially influenced by parental effects in a habitat-dependent manner. Generally, larvae originating from deep-water corals, which experience less variable conditions, expressed more specific responses than shallow-water larvae, with a higher settlement success in simulated parental-habitat conditions. Survival of juvenile corals experimentally translocated to the sea was significantly lower when not at parental depths. We conclude that local adaptations and parental effects alongside larval selectivity and phenotype-environment mismatches combine to create invisible semipermeable barriers to coral dispersal and connectivity, leading to habitat-dependent population segregation.

Population dynamics and growth rates of free-living mushroom corals (Scleractinia: Fungiidae) in the sediment-stressed reefs of Singapore.

The reefs of Singapore provide an excellent opportunity to study the population dynamics and growth rates of free-living mushroom corals (Fungiidae) under sediment-stressed conditions. Transect surveys at four study sites revealed a total of 11 free-living mushroom coral species-the same 11 species as those found by local studies since the 1980s. The abundance of the four most common species ranged from 1.0 to 68.3 Ind. per 100m2, while their population size-structure showed a common pattern of a higher proportion of small-sized corals than large-sized ones (i.e. positively skewed size-structure), although very few individuals of the smallest-size classes were recorded for any of the four species. A more positively skewed size-structure for each of the four most common species was observed at the reef slope (5-6m depth) than at the reef crest (2-3m depth), possibly due to a slower growth rate caused by light reduction with depth. All the mushroom corals studied exhibited a decline in growth rate with increasing size and weight, indicating determinate growth. Growth rate of each of the four most common species was similar among the study sites, despite variation in environmental conditions. Our results demonstrate species richness stability over the past three decades, suggesting that these free-living mushroom coral assemblages comprise species that are well-adapted to the chronic high sedimentation characteristic of Singapore's reefs. However, if the paucity of individuals of the smallest-size classes reflects poor recruitment and/or early mortality, there may be some cause for concern. Our robust baseline data can contribute to a long-term monitoring strategy for determination of changes in mushroom coral population dynamics.

Breakdown in spawning synchrony: A silent threat to coral persistence.

The impacts of human and natural disturbances on coral reefs are typically quantified through visible damage (e.g., reduced coral coverage as a result of bleaching events), but changes in environmental conditions may also cause damage in less visible ways. Despite the current paradigm, which suggests consistent, highly synchronized spawning events, corals that reproduce by broadcast spawning are particularly vulnerable because their reproductive phenology is governed by environmental cues. Here, we quantify coral spawning intensity during four annual reproductive seasons, alongside laboratory analyses at the polyp, colony, and population levels, and we demonstrate that, compared with historical data, several species from the Red Sea have lost their reproductive synchrony. Ultimately, such a synchrony breakdown reduces the probability of successful fertilization, leading to a dearth of new recruits, which may drive aging populations to extinction.

Repetitive sex change in the stony coral Herpolitha limax across a wide geographic range.

Sex change has been widely studied in animals and plants. However, the conditions favoring sex change, its mode and timing remain poorly known. Here, for the first time in stony corals, we report on a protandrous (youngest individuals are males) repetitive sex change exhibited by the fungiid coral Herpolitha limax across large spatial scales (the coral reefs of Japan, Jordan and Israel) and temporal scales (2004-2017). In contrast to most corals, this species is a daytime spawner (08:00-10:00 AM) that spawned at the same time/same date across all the study sites. The sporadically scattered populations of H. limax among the coral reefs of Eilat (Israel) and Aqaba (Jordan) exhibited significantly slower growth, earlier sex change, and lower percentages of reproduction and sex change in comparison to the densely aggregated populations in Okinawa (Japan). At all sites, sex ratio varied among years, but was almost always biased towards maleness. Growth rate decreased with size. We conclude that comparable to dioecious plants that display labile sexuality in response to energetic and/or environmental constraints, the repetitive sex change displayed by H. limax increases its overall fitness reinforcing the important role of reproductive plasticity in the Phylum Cnidaria in determining their evolutionary success.

Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt.

Mesophotic coral ecosystems (i.e., deep coral reefs at 30-120 m depth) appear to be thriving while many shallow reefs in the world are declining. Amid efforts to understand and manage their decline, it was suggested that mesophotic reefs might serve as natural refuges and a possible source of propagules for the shallow reefs. However, our knowledge of how reproductive performance of corals alters with depth is sparse. Here, we present a comprehensive study of the reproductive phenology, fecundity, and abundance of seven reef-building conspecific corals in shallow and mesophotic habitats. Significant differences were found in the synchrony and timing of gametogenesis and spawning between shallow and mesophotic coral populations. Thus, mesophotic populations exhibited delayed or protracted spawning events, which led to spawning of the mesophotic colonies in large proportions at times where the shallow ones had long been depleted of reproductive material. All species investigated demonstrated a substantial reduction in fecundity and/or oocyte sizes at mesophotic depths (40-60 m). Two species (Seriatopora hystrix and Galaxea fascicularis) displayed a reduction in both fecundity and oocyte size at mesophotic depths. Turbinaria reniformis had only reduced fecundity and Acropora squarrosa and Acropora valida only reduced oocyte size. In Montipora verrucosa, reduced fecundity was found during one annual reproductive season while, in the following year, only reduced oocyte size was found. In contrast, reduced oocyte size in mesophotic populations of Acropora squarrosa was consistent along three studied years. One species, Acropora pharaonis, was found to be infertile at mesophotic depths along two studied years. This indicates that reproductive performance decreases with depth; and that although some species are capable of reproducing at mesophotic depths, their contribution to the replenishment of shallow reefs may be inconsequential. Reduced reproductive performance with depth, combined with the possible narrower tolerance to environmental factors, further suggests that mesophotic corals may in fact be more vulnerable than previously conceived. Furthermore, we posit that the observed temporal segregation in reproduction could lead to assortative mating, and this, in turn, may facilitate adaptive divergence across depth.

Reproductive strategies of the coral Turbinaria reniformis in the northern Gulf of Aqaba (Red Sea).

Here we describe for the first time the reproductive biology of the scleractinian coral Turbinaria reniformis studied during three years at the coral reefs of Eilat and Aqaba. We also investigated the possibility of sex change in individually tagged colonies followed over a period of 12 years. T. reniformis was found to be a stable gonochorist (no detected sex change) that reproduces by broadcast spawning 5-6 nights after the full moon of June and July. Spawning was highly synchronized between individuals in the field and in the lab. Reproduction of T. reniformis is temporally isolated from the times at which most other corals reproduce in Eilat. Its relatively long reproductive cycle compared to other hermaphroditic corals may be due to the high reproductive effort associated with the production of eggs by gonochoristic females. Sex ratio in both the Aqaba and Eilat coral populations deviated significantly from a 1:1 ratio. The larger number of males than of females may provide a compensation for sperm limitation due to its dilution in the water column. We posit that such sex allocation would facilitate adaptation within gonochoristic species by increasing fertilization success in low density populations, constituting a phenomenon possibly regulated by chemical communication.