Deep sea treasures - Insights from museum archives shed light on coral microbial diversity within deepest ocean ecosystems.

Deep sea benthic habitats are low productivity ecosystems that host an abundance of organisms within the Cnidaria phylum. The technical limitations and the high cost of deep sea surveys have made exploring deep sea environments and the biology of the organisms that inhabit them challenging. In spite of the widespread recognition of Cnidaria's environmental importance in these ecosystems, the microbial assemblage and its role in coral functioning have only been studied for a few deep water corals. Here, we explored the microbial diversity of deep sea corals by recovering nucleic acids from museum archive specimens. Firstly, we amplified and sequenced the V1-V3 regions of the 16S rRNA gene of these specimens, then we utilized the generated sequences to shed light on the microbial diversity associated with seven families of corals collected from depth in the Coral Sea (depth range 1309 to 2959 m) and Southern Ocean (depth range 1401 to 2071 m) benthic habitats. Surprisingly, Cyanobacteria sequences were consistently associated with six out of seven coral families from both sampling locations, suggesting that these bacteria are potentially ubiquitous members of the microbiome within these cold and deep sea water corals. Additionally, we show that Cnidaria might benefit from symbiotic associations with a range of chemosynthetic bacteria including nitrite, carbon monoxide and sulfur oxidizers. Consistent with previous studies, we show that sequences associated with the bacterial phyla Proteobacteria, Verrucomicrobia, Planctomycetes and Acidobacteriota dominated the microbial community of corals in the deep sea. We also explored genomes of the bacterial genus Mycoplasma, which we identified as associated with specimens of three deep sea coral families, finding evidence that these bacteria may aid the host immune system. Importantly our results show that museum specimens retain components of host microbiome that can provide new insights into the diversity of deep sea coral microbiomes (and potentially other organisms), as well as the diversity of microbes writ large in deep sea ecosystems.

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.

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.

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.

Biophysical and anthropogenic influences on the status of Tonga's coral reefs and reef fish fishery.

Despite increasing threats to Tonga's coral reefs from stressors that are both local (e.g. overfishing and pollution) and global (e.g. climate change), there is yet to be a systematic assessment of the status of the country's coral reef ecosystem and reef fish fishery stocks. Here, we provide a national ecological assessment of Tonga's coral reefs and reef fish fishery using ecological survey data from 375 sites throughout Tonga's three main island groups (Ha'apai, Tongatapu and Vava'u), represented by seven key metrics of reef health and fish resource status. Boosted regression tree analysis was used to assess and describe the relative importance of 11 socio-environmental variables associated with these key metrics of reef condition. Mean live coral cover across Tonga was 18%, and showed a strong increase from north to south correlated with declining sea surface temperature, as well as with increasing distance from each provincial capital. Tongatapu, the southernmost island group, had 2.5 times greater coral cover than the northernmost group, Vava'u (24.9% and 10.4% respectively). Reef fish species richness and density were comparable throughout Tongatapu and the middle island group, Ha'apai (~35 species/transect and ~2500 fish/km2), but were significantly lower in Vava'u (~24 species/transect and ~1700 fish/km2). Spatial patterns in the reef fish assemblage were primarily influenced by habitat-associated variables (slope, structural complexity, and hard coral cover). The biomass of target reef fish was greatest in Ha'apai (~820 kg/ha) and lowest in Vava'u (~340 kg/ha), and was negatively associated with higher human influence and fishing activity. Overall mean reef fish biomass values suggest that Tonga's reef fish fishery can be classified as moderately to heavily exploited, with 64% of sites having less than 500 kg/ha. This study provides critical baseline ecological information for Tonga's coral reefs that will: (1) facilitate ongoing management and research; and (2) enable accurate reporting on conservation targets locally and internationally.

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.

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.

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.

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.

Marginal sinks or potential refuges? Costs and benefits for coral-obligate reef fishes at deep range margins.

Escalating climate-related disturbances and asymmetric habitat losses will increasingly result in species living in more marginal habitats. Marginal habitats may represent important refuges if individuals can acquire adequate resources to survive and reproduce. However, resources at range margins are often distributed more sparsely; therefore, increased effort to acquire resources can result in suboptimal performance and lead to marginal populations becoming non-self-sustaining sink-populations. Shifting resource availability is likely to be particularly problematic for dietary specialists. Here, we use extensive in situ behavioural observations and physiological condition measurements to examine the costs and benefits of resource-acquisition along a depth gradient in two obligate corallivore reef fishes with contrasting levels of dietary specialization. As expected, the space used to secure coral resources increased towards the lower depth margin. However, increased territory sizes resulted in equal or greater availability of resources within deeper territories. In addition, we observed decreased competition and no differences in foraging distance, pairing behaviour, body condition or fecundity at greater depths. Contrary to expectation, our results demonstrate that coral-obligate fishes can select high-quality coral patches on the deeper-reef to access equal or greater resources than their shallow-water counterparts, with no extra costs. This suggests depth offers a viable potential refuge for some at-risk coral-specialist fishes.

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.

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.

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.

Corrigendum: The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

This corrects the article DOI: 10.1038/sdata.2016.17.