Bathymetric evolution of black corals through deep time.

Deep-sea lineages are generally thought to arise from shallow-water ancestors, but this hypothesis is based on a relatively small number of taxonomic groups. Anthozoans, which include corals and sea anemones, are significant contributors to the faunal diversity of the deep sea, but the timing and mechanisms of their invasion into this biome remain elusive. Here, we reconstruct a fully resolved, time-calibrated phylogeny of 83 species in the order Antipatharia (black coral) to investigate their bathymetric evolutionary history. Our reconstruction indicates that extant black coral lineages first diversified in continental slope depths (∼250-3000 m) during the early Silurian (∼437 millions of years ago (Ma)) and subsequently radiated into, and diversified within, both continental shelf (less than 250 m) and abyssal (greater than 3000 m) habitats. Ancestral state reconstruction analysis suggests that the appearance of morphological features that enhanced the ability of black corals to acquire nutrients coincided with their invasion of novel depths. Our findings have important conservation implications for anthozoan lineages, as the loss of 'source' slope lineages could threaten millions of years of evolutionary history and confound future invasion events, thereby warranting protection.

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.

Intraspecific variation reshapes coral assemblages under elevated temperature and acidity.

Insights into assemblages that can persist in extreme environments are still emerging. Ocean warming and acidification select against species with low physiological tolerance (trait-based 'filtering'). However, intraspecific trait variation can promote species adaptation and persistence, with potentially large effects on assemblage structure. By sampling nine coral traits (four morphological, four tissue and one skeletal) along an offshore-inshore gradient in temperature and pH, we show that distantly related coral species undergo consistent intraspecific changes as they cross into warm, acidic environments. Intraspecific variation and species turnover each favoured colonies with greater tissue biomass, higher symbiont densities and reduced skeletal investments, indicating strong filtering on colony physiology within and across species. Physiological tissue traits were highly variable within species and were independent of morphology, enabling morphologically diverse species to cross into sites of elevated temperature and acidity. Widespread intraspecific change can therefore counter the loss of biodiversity and morphological structure across a steep environmental gradient.

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.

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.

Ecological and morphological traits predict depth-generalist fishes on coral reefs.

Ecological communities that occupy similar habitats may exhibit functional convergence despite significant geographical distances and taxonomic dissimilarity. On coral reefs, steep gradients in key environmental variables (e.g. light and wave energy) restrict some species to shallow depths. We show that depth-generalist reef fishes are correlated with two species-level traits: caudal fin aspect ratio and diet. Fishes with high aspect ratio (lunate) caudal fins produce weaker vortices in the water column while swimming, and we propose that 'silent swimming' reduces the likelihood of detection and provides an advantage on deeper reefs with lower light irradiance and water motion. Significant differences in depth preference among trophic guilds reflect variations in the availability of different food sources along a depth gradient. The significance of these two traits across three geographically and taxonomically distinct assemblages suggests that deep-water habitats exert a strong environmental filter on coral reef-fish assemblages.

Dynamic habitat suitability modelling reveals rapid poleward distribution shift in a mobile apex predator.

Many taxa are undergoing distribution shifts in response to anthropogenic climate change. However, detecting a climate signal in mobile species is difficult due to their wide-ranging, patchy distributions, often driven by natural climate variability. For example, difficulties associated with assessing pelagic fish distributions have rendered fisheries management ill-equipped to adapt to the challenges posed by climate change, leaving pelagic species and ecosystems vulnerable. Here, we demonstrate the value of citizen science data for modelling the dynamic habitat suitability of a mobile pelagic predator (black marlin, Istiompax indica) within the south-west Pacific Ocean. The extensive spatial and temporal coverage of our occurrence data set (n = 18 717), collected at high resolution (~1.85 km(2) ), enabled identification of suitable habitat at monthly time steps over a 16-year period (1998-2013). We identified considerable monthly, seasonal and interannual variability in the extent and distribution of suitable habitat, predominately driven by chlorophyll a and sea surface height. Interannual variability correlated with El Nino Southern Oscillation (ENSO) events, with suitable habitat extending up to ~300 km further south during La Nina events. Despite the strong influence of ENSO, our model revealed a rapid poleward shift in the geometric mean of black marlin habitat, occurring at 88.2 km decade(-1) . By incorporating multiple environmental factors at monthly time steps, we were able to demonstrate a rapid distribution shift in a mobile pelagic species. Our findings suggest that the rapid velocity of climate change in the south-west Pacific Ocean is likely affecting mobile pelagic species, indicating that they may be more vulnerable to climate change than previously thought.

Factors influencing incidental representation of previously unknown conservation features in marine protected areas.

Spatially explicit information on species distributions for conservation planning is invariably incomplete; therefore, the use of surrogates is required to represent broad-scale patterns of biodiversity. Despite significant interest in the effectiveness of surrogates for predicting spatial distributions of biodiversity, few researchers have explored questions involving the ability of surrogates to incidentally represent unknown features of conservation interest. We used the Great Barrier Reef marine reserve network to examine factors affecting incidental representation of conservation features that were unknown at the time the reserve network was established. We used spatially explicit information on the distribution of 39 seabed habitats and biological assemblages and the conservation planning software Marxan to examine how incidental representation was affected by the spatial characteristics of the features; the conservation objectives (the minimum proportion of each feature included in no-take areas); the spatial configuration of no-take areas; and the opportunity cost of conservation. Cost was closely and inversely correlated to incidental representation. However, incidental representation was achieved, even in a region with only coarse-scale environmental data, by adopting a precautionary approach that explicitly considered the potential for unknown features. Our results indicate that incidental representation is enhanced by partitioning selection units along biophysical gradients to account for unknown within-feature variability and ensuring that no-take areas are well distributed throughout the region; by setting high conservation objectives that (in this case >33%) maximize the chances of capturing unknown features incidentally; and by carefully considering the designation of cost to planning units when using decision-support tools for reserve design. The lessons learned from incidental representation in the Great Barrier Reef have implications for conservation planning in other regions, particularly those that lack detailed environmental and ecological data.

Functional consequences of Palaeozoic reef collapse.

Biogenic reefs have been hotspots of biodiversity and evolutionary novelty throughout the Phanerozoic. The largest reef systems in Earth's history occurred in the Devonian period, but collapsed during the Late Devonian Mass Extinction. However, the consequences for the functional diversity of Palaeozoic reefs have received little attention. Here, we examine changes in the functional diversity of tabulate coral assemblages over a 35 million year period from the middle Devonian to the Carboniferous, straddling the multiphase extinction event to identify the causes and ecological consequences of the extinction for tabulate corals. By examining five key morphological traits, we show a divergent response of taxonomic and functional diversity to the mass extinction: taxonomic richness peaked during the Givetian (~ 388-383 Ma) and coincided with peak reef building, but functional diversity was only moderate because many species had very similar trait combinations. The collapse of taxonomic diversity and reef building in the late Devonian had minimal impact on functional richness of coral assemblages. However, non-random shifts towards species with larger corallites and lower colony integration suggest a shift from photosymbiotic to asymbiotic taxa associated over the study period. Our results suggest that the collapse of the huge Devonian reef systems was correlated with a breakdown of photosymbiosis and extinction of photosymbiotic tabulate coral taxa. Despite the appearance of new tabulate coral species over the next 35 million years, the extinction of taxa with photosymbiotic traits had long-lasting consequences for reef building and, by extension, shallow marine ecosystems in the Palaeozoic.

Five new species of black coral (Anthozoa; Antipatharia) from the Great Barrier Reef and Coral Sea, Australia.

We describe five new species of black corals from the Great Barrier Reef and Coral Sea, collected at depths ranging from 14 to 789 m: two in the family Antipathidae (Antipathes falkorae sp. nov. and Antipathes morrisi sp. nov.), two in the family Aphanipathidae (Aphanipathes flailum sp. nov. and Rhipidipathes helae sp. nov.), and one in the family Cladopathidae (Hexapathes bikofskii sp. nov.). We also present a phylogeny of 80 black corals reconstructed from a target capture dataset of ultraconserved elements and exons, to show the systematic relationships among new and nominal species. This phylogeny also represents a backbone for future species descriptions and research into the evolutionary history of the Antipatharia.

Morphological and molecular description of a new genus and species of black coral (Cnidaria: Anthozoa: Hexacorallia: Antipatharia: Antipathidae: Blastopathes) from Papua New Guinea.

Blastopathes medusa gen. nov., sp. nov., is described from Kimbe Bay, Papua New Guinea, based on morphological and molecular data. Blastopathes, assigned to the Antipathidae, is a large, mythology-inspiring black coral characterized by clusters of elongate stem-like branches that extend out at their base and then curve upward. Colonies are not pinnulate and contain single branches, which could represent new branch cluster formations. Morphological and molecular (mitochondrial DNA and targeted capture of nuclear loci) evidence supporting the establishment of a new genus is discussed. This is the first study to utilize the target capture of ultraconserved elements (UCEs) and exonic loci to elucidate phylogenetic relationships among black corals and to identify and place a new genus and species.

Variability in the functional composition of coral reef fish communities on submerged and emergent reefs in the central Great Barrier Reef, Australia.

On coral reefs, depth and gradients related to depth (e.g. light and wave exposure) influence the composition of fish communities. However, most studies focus only on emergent reefs that break the sea surface in shallow waters (<10 m). On the Great Barrier Reef (GBR), submerged reefs (reefs that do not break the sea surface) occupy an area equivalent to all emergent reefs. However, submerged reefs have received comparatively little research attention, and fish communities associated with submerged reefs remain poorly quantified. Here, we quantify fish assemblages at each of three depths (10, 20 and 30 m) on eight submerged reefs (four mid-shelf and four outer-shelf) and two nearby emergent reefs in the central GBR where reef habitat extends from 0-~25 m depth. We examine how total fish abundance, the abundance of 13 functional groups, and the functional composition of fish communities varies among depths, reef types (submerged versus emergent reefs), and shelf position (mid-shelf versus outer-shelf). Overall fish abundance decreased sevenfold with depth, but declined less steeply (twofold) on outer-shelf submerged reefs than on both mid-shelf submerged reefs and emergent reefs. The functional composition of the fish assemblage also varied significantly among depths and reef types. Turnover in the functional composition of the fish community was also steeper on the mid-shelf, suggesting that shallow-affiliated groups extend further in deeper water on the outer-shelf. Ten of the 13 functional groups were more strongly associated with the shallowest depths (the upper reef slope of emergent reefs or the 'crests' of submerged reefs), two groups (soft coral/sponge feeders and mesopredators) were more abundant at the deepest sites. Our results confirm that submerged reefs in the central GBR support a wide range of coral reef fishes, and are an important component of the GBR ecosystem.

Resolving the depth zonation paradox in reef-building corals.

Changes in abundance across a natural environmental gradient provide important insights into a species' realized ecological niche. In reef-building corals, a species' niche is often defined using its depth range. However, most reef-building coral species occur over a broad depth range, a fact that is incompatible with the strong zonation found in coral assemblages across depth. We resolve this paradox by modeling the abundance distributions of 110 coral species across a 45 m depth gradient to show that most are in fact depth specialists and reveal that depth range alone is incapable of capturing a species' depth use. We then highlight the significance of our results by demonstrating how depth range greatly overestimates the potential number of species with a refuge at depth from global warming. Our findings illustrate both the limitations of the simple metric of depth range and the ecological insights that can be gained by moving beyond it.

Spatial variability in benthic assemblage composition in shallow and upper mesophotic coral ecosystems in the Philippines.

Mesophotic coral ecosystems (MCEs) have received increasing attention in recent years in recognition of their unique biodiversity and also their potential importance as refuges from disturbance events. However, knowledge of the composition of MCEs and how they vary in space is lacking in many regions, particularly the Coral Triangle biodiversity hotspot. Here, we compared the benthic components and coral genera composition between shallow-water reefs (SWRs, 8-13 m depth) and upper MCEs (30-40 m) in four locations in the Philippines that are exposed to differing environmental conditions. Coral cover, abundance, and generic diversity were lower in MCEs than SWRs at three of the four locations. Benthic composition and coral generic composition also varied significantly among locations for both shallow and deep sites. Differences in benthic composition among sites was due primarily to variation in hard corals, macroalgae, sand and silt, while variation in coral assemblage was due to differences in abundance of encrusting Porites, branching Acropora, branching Seriatopora. Our results showed that the composition of MCE communities varied significantly from adjacent shallow reefs, but also among MCEs in differing geographic locations. Furthermore, our results suggest disturbances affecting shallow-water reefs, particularly sedimentation, also negatively impact MCEs, and that depth therefore provides no potential refuge from these disturbances. We recommend that conservation of MCEs consider spatial variability in community composition among sites, and urge further research to better understand the spatial variation in the composition of MCE communities in the Philippines.

Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.

Without drastic efforts to reduce carbon emissions and mitigate globalized stressors, tropical coral reefs are in jeopardy. Strategic conservation and management requires identification of the environmental and socioeconomic factors driving the persistence of scleractinian coral assemblages-the foundation species of coral reef ecosystems. Here, we compiled coral abundance data from 2,584 Indo-Pacific reefs to evaluate the influence of 21 climate, social and environmental drivers on the ecology of reef coral assemblages. Higher abundances of framework-building corals were typically associated with: weaker thermal disturbances and longer intervals for potential recovery; slower human population growth; reduced access by human settlements and markets; and less nearby agriculture. We therefore propose a framework of three management strategies (protect, recover or transform) by considering: (1) if reefs were above or below a proposed threshold of >10% cover of the coral taxa important for structural complexity and carbonate production; and (2) reef exposure to severe thermal stress during the 2014-2017 global coral bleaching event. Our findings can guide urgent management efforts for coral reefs, by identifying key threats across multiple scales and strategic policy priorities that might sustain a network of functioning reefs in the Indo-Pacific to avoid ecosystem collapse.

Black corals (Anthozoa: Antipatharia) from the deep (916 m-2542 m) Coral Sea, north-eastern Australia.

Black corals (Anthozoa: Antipatharia) occur in all the world's oceans in a wide range of habitats from shallow-water coral reefs to the deep-sea. However, the taxonomy of black corals is poorly known compared to many other anthozoan groups. This knowledge gap is particularly acute for the deep-sea, where collecting specimens is logistically difficult and costly. Here, we identify 21 black coral specimens collected from the western Coral Sea adjacent to north-east Australia. The specimens represent five nominal species from five genera and two families. All species represent new records for the region, including the first record for the family Cladopathidae Brook, 1889. We describe the morphology of these specimens, note geographic and bathymetric range expansions, and provide evidence to support the hypothesis that Bathypathes seculata Opresko, 2005 is the juvenile stage of Bathypathes patula Brook, 1889, thus warranting synonymization. Our findings demonstrate that deep-sea antipatharians in this region are much more diverse than previously reported. Furthermore, this study highlights the importance of museum collections in terms of increasing our understanding of taxonomy and patterns of biodiversity, particularly for poorly-studied habitats such as the deep-sea.

Universal target-enrichment baits for anthozoan (Cnidaria) phylogenomics: New approaches to long-standing problems.

Anthozoans (e.g., corals, anemones) are an ecologically important and diverse group of marine metazoans that occur from shallow to deep waters worldwide. However, our understanding of the evolutionary relationships among the ~7,500 species within this class is hindered by the lack of phylogenetically informative markers that can be reliably sequenced across a diversity of taxa. We designed and tested 16,306 RNA baits to capture 720 ultraconserved element loci and 1,071 exon loci. Library preparation and target enrichment were performed on 33 taxa from all orders within the class Anthozoa. Following Illumina sequencing and Trinity assembly, we recovered 1,774 of 1,791 targeted loci. The mean number of loci recovered from each species was 638 ± 222, with more loci recovered from octocorals (783 ± 138 loci) than hexacorals (475 ± 187 loci). Parsimony informative sites ranged from 26 to 49% for alignments at differing hierarchical taxonomic levels (e.g., Anthozoa, Octocorallia, Hexacorallia). The per cent of variable sites within each of three genera (Acropora, Alcyonium, and Sinularia) for which multiple species were sequenced ranged from 4.7% to 30%. Maximum-likelihood analyses recovered highly resolved trees with topologies matching those supported by other studies, including the monophyly of the order Scleractinia. Our results demonstrate the utility of this target-enrichment approach to resolve phylogenetic relationships from relatively old to recent divergences. Redesigning the baits with improved affinities to capture loci within each subclass will provide a valuable toolset to address systematic questions, further our understanding of the timing of diversifications and help resolve long-standing controversial relationships in the class Anthozoa.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño-Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.