Global warming impairs stock-recruitment dynamics of corals.

Changes in disturbance regimes due to climate change are increasingly challenging the capacity of ecosystems to absorb recurrent shocks and reassemble afterwards, escalating the risk of widespread ecological collapse of current ecosystems and the emergence of novel assemblages1-3. In marine systems, the production of larvae and recruitment of functionally important species are fundamental processes for rebuilding depleted adult populations, maintaining resilience and avoiding regime shifts in the face of rising environmental pressures4,5. Here we document a regional-scale shift in stock-recruitment relationships of corals along the Great Barrier Reef-the world's largest coral reef system-following unprecedented back-to-back mass bleaching events caused by global warming. As a consequence of mass mortality of adult brood stock in 2016 and 2017 owing to heat stress6, the amount of larval recruitment declined in 2018 by 89% compared to historical levels. For the first time, brooding pocilloporids replaced spawning acroporids as the dominant taxon in the depleted recruitment pool. The collapse in stock-recruitment relationships indicates that the low resistance of adult brood stocks to repeated episodes of coral bleaching is inexorably tied to an impaired capacity for recovery, which highlights the multifaceted processes that underlie the global decline of coral reefs. The extent to which the Great Barrier Reef will be able to recover from the collapse in stock-recruitment relationships remains uncertain, given the projected increased frequency of extreme climate events over the next two decades7.

Global warming transforms coral reef assemblages.

Global warming is rapidly emerging as a universal threat to ecological integrity and function, highlighting the urgent need for a better understanding of the impact of heat exposure on the resilience of ecosystems and the people who depend on them 1 . Here we show that in the aftermath of the record-breaking marine heatwave on the Great Barrier Reef in 2016 2 , corals began to die immediately on reefs where the accumulated heat exposure exceeded a critical threshold of degree heating weeks, which was 3-4 °C-weeks. After eight months, an exposure of 6 °C-weeks or more drove an unprecedented, regional-scale shift in the composition of coral assemblages, reflecting markedly divergent responses to heat stress by different taxa. Fast-growing staghorn and tabular corals suffered a catastrophic die-off, transforming the three-dimensionality and ecological functioning of 29% of the 3,863 reefs comprising the world's largest coral reef system. Our study bridges the gap between the theory and practice of assessing the risk of ecosystem collapse, under the emerging framework for the International Union for Conservation of Nature (IUCN) Red List of Ecosystems 3 , by rigorously defining both the initial and collapsed states, identifying the major driver of change, and establishing quantitative collapse thresholds. The increasing prevalence of post-bleaching mass mortality of corals represents a radical shift in the disturbance regimes of tropical reefs, both adding to and far exceeding the influence of recurrent cyclones and other local pulse events, presenting a fundamental challenge to the long-term future of these iconic ecosystems.

Disturbance-Induced Changes in Population Size Structure Promote Coral Biodiversity.

AbstractReef-building coral assemblages are typically species rich, yet the processes maintaining high biodiversity remain poorly understood. Disturbance has long been thought to promote coral species coexistence by reducing the strength of competition (i.e., the intermediate disturbance hypothesis [IDH]). However, such disturbance-induced effects are insufficient to inhibit competitive exclusion. Nevertheless, there are other mechanisms by which disturbance and, more generally, environmental variation can favor coexistence. Here, we develop a size-structured, stochastic coral competition model calibrated with field data from two common colony morphologies to investigate the effects of hydrodynamic disturbance on community dynamics. We show that fluctuations in wave action can promote coral species coexistence but that this occurs via interspecific differences in size-dependent mortality rather than solely via stochastic fluctuations in competition (i.e., free space availability). While this mechanism differs from that originally envisioned in the IDH, it is nonetheless a mechanism by which intermediate levels of disturbance do promote coexistence. Given the sensitivity of coexistence to disturbance frequency and intensity, anthropogenic changes in disturbance regimes are likely to affect coral assemblages in ways that are not predictable from single-population models.

A hybrid-capture approach to reconstruct the phylogeny of Scleractinia (Cnidaria: Hexacorallia).

A well-supported evolutionary tree representing most major lineages of scleractinian corals is in sight with the development and application of phylogenomic approaches. Specifically, hybrid-capture techniques are shedding light on the evolution and systematics of corals. Here, we reconstructed a broad phylogeny of Scleractinia to test previous phylogenetic hypotheses inferred from a few molecular markers, in particular, the relationships among major scleractinian families and genera, and to identify clades that require further research. We analysed 449 nuclear loci from 422 corals, comprising 266 species spanning 26 families, combining data across whole genomes, transcriptomes, hybrid capture and low-coverage sequencing to reconstruct the largest phylogenomic tree of scleractinians to date. Due to the large number of loci and data completeness (less than 38% missing data), node supports were high across shallow and deep nodes with incongruences observed in only a few shallow nodes. The "Robust" and "Complex" clades were recovered unequivocally, and our analyses confirmed that Micrabaciidae Vaughan, 1905 is sister to the "Robust" clade, transforming our understanding of the "Basal" clade. Several families remain polyphyletic in our phylogeny, including Deltocyathiidae Kitahara, Cairns, Stolarski & Miller, 2012, Caryophylliidae Dana, 1846, and Coscinaraeidae Benzoni, Arrigoni, Stefani & Stolarski, 2012, and we hereby formally proposed the family name Pachyseridae Benzoni & Hoeksema to accommodate Pachyseris Milne Edwards & Haime, 1849, which is phylogenetically distinct from Agariciidae Gray, 1847. Results also revealed species misidentifications and inconsistencies within morphologically complex clades, such as Acropora Oken, 1815 and Platygyra Ehrenberg, 1834, underscoring the need for reference skeletal material and topotypes, as well as the importance of detailed taxonomic work. The approach and findings here provide much promise for further stabilising the topology of the scleractinian tree of life and advancing our understanding of coral evolution.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Solving the Coral Species Delimitation Conundrum.

Distinguishing coral species is not only crucial for physiological, ecological, and evolutionary studies but also to enable effective management of threatened reef ecosystems. However, traditional hypotheses that delineate coral species based on morphological traits from the coral skeleton are frequently at odds with tree-based molecular approaches. Additionally, a dearth of species-level molecular markers has made species delimitation particularly challenging in species-rich coral genera, leading to the widespread assumption that interspecific hybridization might be responsible for this apparent conundrum. Here, we used three lines of evidence-morphology, breeding trials, and molecular approaches-to identify species boundaries in a group of ecologically important tabular Acropora corals. In contrast to previous studies, our morphological analysis yielded groups that were congruent with experimental crosses as well as with coalescent-based and allele sharing-based multilocus approaches to species delimitation. Our results suggest that species of the genus Acropora are reproductively isolated and independently evolving units that can be distinguished morphologically. These findings not only pave the way for a taxonomic revision of coral species but also outline an approach that can provide a solid basis to address species delimitation and provide conservation support to a wide variety of keystone organisms. [Acropora; coral reefs; hybridization; reproductive isolation; taxonomy.].

Global warming and recurrent mass bleaching of corals.

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Reef fishes weaken dietary preferences after coral mortality, altering resource overlap.

The direct and indirect effects of climate change can affect, and are mediated by, changes in animal behaviour. However, we often lack sufficient empirical data to assess how large-scale disturbances affect the behaviour of individuals, which scales up to influence communities. Here, we investigate these patterns by focusing on the foraging behaviour of butterflyfishes, prominent coral-feeding fishes on coral reefs, before and after a mass coral bleaching event in Iriomote, Japan. In response to 65% coral mortality, coral-feeding fishes broadened their diets, showing a significant weakening of dietary preferences across species. Multiple species reduced their consumption of bleaching-sensitive Acropora corals, while expanding their diets to consume a variety of other coral genera. This resulted in decreased dietary overlap among butterflyfishes. Behavioural changes in response to bleaching may increase resilience of coral reef fishes in the short term. However, coral mortality has reduced populations of coral-feeders world-wide, indicating the changes in feeding behaviour we document here may not be sufficient to ensure long-term resilience of butterflyfishes on coral reefs.

Green fluorescence from cnidarian hosts attracts symbiotic algae.

Reef-building corals thrive in nutrient-poor marine environments because of an obligate symbiosis with photosynthetic dinoflagellates of the genus Symbiodinium Symbiosis is established in most corals through the uptake of Symbiodinium from the environment. Corals are sessile for most of their life history, whereas free-living Symbiodinium are motile; hence, a mechanism to attract Symbiodinium would greatly increase the probability of encounter between host and symbiont. Here, we examined whether corals can attract free-living motile Symbiodinium by their green fluorescence, emitted by the excitation of endogenous GFP by purple-blue light. We found that Symbiodinium have positive and negative phototaxis toward weak green and strong purple-blue light, respectively. Under light conditions that cause corals to emit green fluorescence, (e.g., strong blue light), Symbiodinium were attracted toward live coral fragments. Symbiodinium were also attracted toward an artificial green fluorescence dye with similar excitation and emission spectra to coral-GFP. In the field, more Symbiodinium were found in traps painted with a green fluorescence dye than in controls. Our results revealed a biological signaling mechanism between the coral host and its potential symbionts.

Phylogenomics of Porites from the Arabian Peninsula.

The advent of high throughput sequencing technologies provides an opportunity to resolve phylogenetic relationships among closely related species. By incorporating hundreds to thousands of unlinked loci and single nucleotide polymorphisms (SNPs), phylogenomic analyses have a far greater potential to resolve species boundaries than approaches that rely on only a few markers. Scleractinian taxa have proved challenging to identify using traditional morphological approaches and many groups lack an adequate set of molecular markers to investigate their phylogenies. Here, we examine the potential of Restriction-site Associated DNA sequencing (RADseq) to investigate phylogenetic relationships and species limits within the scleractinian coral genus Porites. A total of 126 colonies were collected from 16 localities in the seas surrounding the Arabian Peninsula and ascribed to 12 nominal and two unknown species based on their morphology. Reference mapping was used to retrieve and compare nearly complete mitochondrial genomes, ribosomal DNA, and histone loci. De novo assembly and reference mapping to the P. lobata coral transcriptome were compared and used to obtain thousands of genome-wide loci and SNPs. A suite of species discovery methods (phylogenetic, ordination, and clustering analyses) and species delimitation approaches (coalescent-based, species tree, and Bayesian Factor delimitation) suggested the presence of eight molecular lineages, one of which included six morphospecies. Our phylogenomic approach provided a fully supported phylogeny of Porites from the Arabian Peninsula, suggesting the power of RADseq data to solve the species delineation problem in this speciose coral genus.

Biogeographical disparity in the functional diversity and redundancy of corals.

Corals are major contributors to a range of key ecosystem functions on tropical reefs, including calcification, photosynthesis, nutrient cycling, and the provision of habitat structure. The abundance of corals is declining at multiple scales, and the species composition of assemblages is responding to escalating human pressures, including anthropogenic global warming. An urgent challenge is to understand the functional consequences of these shifts in abundance and composition in different biogeographical contexts. While global patterns of coral species richness are well known, the biogeography of coral functions in provinces and domains with high and low redundancy is poorly understood. Here, we quantify the functional traits of all currently recognized zooxanthellate coral species (n = 821) in both the Indo-Pacific and Atlantic domains to examine the relationships between species richness and the diversity and redundancy of functional trait space. We find that trait diversity is remarkably conserved (>75% of the global total) along latitudinal and longitudinal gradients in species richness, falling away only in species-poor provinces (n < 200), such as the Persian Gulf (52% of the global total), Hawaii (37%), the Caribbean (26%), and the East-Pacific (20%), where redundancy is also diminished. In the more species-poor provinces, large and ecologically important areas of trait space are empty, or occupied by just a few, highly distinctive species. These striking biogeographical differences in redundancy could affect the resilience of critical reef functions and highlight the vulnerability of relatively depauperate, peripheral locations, which are often a low priority for targeted conservation efforts.

An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives.

Targeted enrichment of genomic DNA can profoundly increase the phylogenetic resolution of clades and inform taxonomy. Here, we redesign a custom bait set previously developed for the cnidarian class Anthozoa to more efficiently target and capture ultraconserved elements (UCEs) and exonic loci within the subclass Hexacorallia. We test this enhanced bait set (targeting 2476 loci) on 99 specimens of scleractinian corals spanning both the "complex" (Acroporidae, Agariciidae) and "robust" (Fungiidae) clades. Focused sampling in the staghorn corals (genus Acropora) highlights the ability of sequence capture to inform the taxonomy of a clade previously deficient in molecular resolution. A mean of 1850 (±298) loci were captured per taxon (955 UCEs, 894 exons), and a 75% complete concatenated alignment of 96 samples included 1792 loci (991 UCE, 801 exons) and ~1.87 million base pairs. Maximum likelihood and Bayesian analyses recovered robust molecular relationships and revealed that species-level relationships within the Acropora are incongruent with traditional morphological groupings. Both UCE and exon datasets delineated six well-supported clades within Acropora. The enhanced bait set will facilitate investigations of the evolutionary history of many important groups of reef corals, particularly where previous molecular marker development has been unsuccessful.

Climate-driven shift in coral morphological structure predicts decline of juvenile reef fishes.

Rapid intensification of environmental disturbances has sparked widespread decline and compositional shifts in foundation species in ecosystems worldwide. Now, an emergent challenge is to understand the consequences of shifts and losses in such habitat-forming species for associated communities and ecosystem processes. Recently, consecutive coral bleaching events shifted the morphological makeup of habitat-forming coral assemblages on the Great Barrier Reef (GBR). Considering the disparity of coral morphological growth forms in shelter provision for reef fishes, we investigated how shifts in the morphological structure of coral assemblages affect the abundance of juvenile and adult reef fishes. We used a temporal dataset from shallow reefs in the northern GBR to estimate coral convexity (a fine-scale quantitative morphological trait) and two widely used coral habitat descriptors (coral cover and reef rugosity) for disentangling the effects of coral morphology on reef fish assemblages. Changes in coral convexity, rather than live coral cover or reef rugosity, disproportionately affected juvenile reef fishes when compared to adults, and explained more than 20% of juvenile decline. The magnitude of this effect varied by fish body size with juveniles of small-bodied species showing higher vulnerability to changes in coral morphology. Our findings suggest that continued large-scale shifts in the relative abundance of morphological groups within coral assemblages are likely to affect population replenishment and dynamics of future reef fish communities. The different responses of juvenile and adult fishes according to habitat descriptors indicate that focusing on coarse-scale metrics alone may mask fine-scale ecological responses that are key to understand ecosystem functioning and resilience. Nonetheless, quantifying coral morphological traits may contribute to forecasting the structure of reef fish communities on novel reef ecosystems shaped by climate change.

Partitioning colony size variation into growth and partial mortality.

Body size is a trait that broadly influences the demography and ecology of organisms. In unitary organisms, body size tends to increase with age. In modular organisms, body size can either increase or decrease with age, with size changes being the net difference between modules added through growth and modules lost through partial mortality. Rates of colony extension are independent of body size, but net growth is allometric, suggesting a significant role of size-dependent mortality. In this study, we develop a generalizable model of partitioned growth and partial mortality and apply it to data from 11 species of reef-building coral. We show that corals generally grow at constant radial increments that are size independent, and that partial mortality acts more strongly on small colonies. We also show a clear life-history trade-off between growth and partial mortality that is governed by growth form. This decomposition of net growth can provide mechanistic insights into the relative demographic effects of the intrinsic factors (e.g. acquisition of food and life-history strategy), which tend to affect growth, and extrinsic factors (e.g. physical damage, and predation), which tend to affect mortality.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Testing biodiversity theory using species richness of reef-building corals across a depth gradient.

Natural environmental gradients encompass systematic variation in abiotic factors that can be exploited to test competing explanations of biodiversity patterns. The species-energy (SE) hypothesis attempts to explain species richness gradients as a function of energy availability. However, limited empirical support for SE is often attributed to idiosyncratic, local-scale processes distorting the underlying SE relationship. Meanwhile, studies are also often confounded by factors such as sampling biases, dispersal boundaries and unclear definitions of energy availability. Here, we used spatially structured observations of 8460 colonies of photo-symbiotic reef-building corals and a null-model to test whether energy can explain observed coral species richness over depth. Species richness was left-skewed, hump-shaped and unrelated to energy availability. While local-scale processes were evident, their influence on species richness was insufficient to reconcile observations with model predictions. Therefore, energy availability, either in isolation or in combination with local deterministic processes, was unable to explain coral species richness across depth. Our results demonstrate that local-scale processes do not necessarily explain deviations in species richness from theoretical models, and that the use of idiosyncratic small-scale factors to explain large-scale ecological patterns requires the utmost caution.

Negligible effect of competition on coral colony growth.

Competition is an important determinant of assemblage structure and population regulation, often resulting in decreased growth, fecundity or survival. In corals, most studies testing for an effect of competition on demographic traits, such as growth, have been experimental and often impose very high levels of competition upon colonies. To more realistically assess the role of competition on coral traits, multispecies studies in the wild are required. Here, we use 5 yr of data that includes 11 coral species on the reef crest at Lizard Island on the Great Barrier Reef to quantify the effect of competition on growth. Additionally, we test whether species differ in their susceptibility to direct-contact (overgrowth and digestion) and overtopping competition, and whether species from some morphological groups are more likely to compete with one another than with species from other morphological groups. We also investigate the relationships between competitive ability and three key traits: growth rate, mechanical stability and fecundity. In contrast to most previous work using field manipulations of competition, we found a negligible effect of competition on growth. Acropora species consistently won overtopping encounters but lost in direct-contact encounters, and these results were consistent among the four Acropora morphological groups. In contrast, the massive Goniastrea spp. were poor at overtopping but generally won direct-contact encounters. Only tabular colonies were disproportionally more likely to compete against one another than with other morphologies. This propensity increases intraspecific relative to interspecific competition, a phenomenon that can promote coexistence when it is present among dominant competitors. Good competitors grew more quickly and had higher fecundity but were less mechanically stable, implying a tradeoff between performance during disturbance vs. performance in the absence of disturbance. We conclude that competition among adults is less likely to influence community dynamics than previously thought. If competition does have an effect, it is more likely to occur at life-stages other than adults.

BioTIME: A database of biodiversity time series for the Anthropocene.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

Coral tumor-like growth anomalies induce an immune response and reduce fecundity.

Coral growth anomalies (GAs) are chronic diseases that adversely affect organism health and fitness. We investigated immunity and fecundity within and among GA-affected and visually healthy control colonies of the reef-building coral Acropora hyacinthus. Compared to controls, GAs had higher activity of the key immunity enzyme phenoloxidase (PO), suggesting a localised immune response within the GA. Both GAs and healthy tissue of GA-affected colonies had significantly greater total potential PO (tpPO)-PO activity inclusive of the activated latent PO, prophenoloxidase-than control colonies. Higher tpPO activity in GA-affected corals suggests elevated constitutive immunity compared to visually healthy controls. Additionally, fewer GA-affected colonies produced gametes, fewer polyps had oocytes (p < 0.001) and the number of oocytes per polyp was lower. Therefore, GAs in A. hyacinthus might induce, or represent a shift in resource investment towards immunity and away from reproduction. While the effect on population growth is likely to be small, reduced fecundity in GA-affected colonies does suggest a selective pressure against GAs.

Allometric growth in reef-building corals.

Predicting demographic rates is a critical part of forecasting the future of ecosystems under global change. Here, we test if growth rates can be predicted from morphological traits for a highly diverse group of colonial symbiotic organisms: scleractinian corals. We ask whether growth is isometric or allometric among corals, and whether most variation in coral growth rates occurs at the level of the species or morphological group. We estimate growth as change in planar area for 11 species, across five morphological groups and over 5 years. We show that coral growth rates are best predicted from colony size and morphology rather than species. Coral size follows a power scaling law with a constant exponent of 0.91. Despite being colonial organisms, corals have consistent allometric scaling in growth. This consistency simplifies the task of projecting community responses to disturbance and climate change.