Decline of a distinct coral reef holobiont community under ocean acidification.

BACKGROUND: Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH - an important global coral reef stressor - can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. RESULTS: We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. CONCLUSIONS: We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. Video Abstract.

Life goes on: Spatial heterogeneity promotes biodiversity in an urbanized coastal marine ecosystem.

Both human populations and marine biodiversity are concentrated along coastlines, with growing conservation interest in how these ecosystems can survive intense anthropogenic impacts. Tropical urban centres provide valuable research opportunities because these megacities are often adjacent to mega-diverse coral reef systems. The Pearl River Delta is a prime exemplar, as it encompasses one of the most densely populated and impacted regions in the world and is located just northwest of the Coral Triangle. However, the spatial and taxonomic complexity of this biodiversity, most of which is small, cryptic in habitat and poorly known, make comparative analyses challenging. We deployed standardized settlement structures at seven sites differing in the intensity of human impacts and used COI metabarcoding to characterize benthic biodiversity, with a focus on metazoans. We found a total of 7184 OTUs, with an average of 665 OTUs per sampling unit; these numbers exceed those observed in many previous studies using comparable methods, despite the location of our study in an urbanized environment. Beta diversity was also high, with 52% of the OTUs found at just one site. As expected, we found that the sites close to point sources of pollution had substantially lower diversity (44% less) relative to sites bathed in less polluted oceanic waters. However, the polluted sites contributed substantially to the total animal diversity of the region, with 25% of all OTUs occurring only within polluted sites. Further analysis of Arthropoda, Annelida and Mollusca showed that phylogenetic clustering within a site was common, suggesting that environmental filtering reduced biodiversity to a subset of lineages present within the region, a pattern that was most pronounced in polluted sites and for the Arthropoda. The water quality gradients surrounding the PRD highlight the unique role of in situ studies for understanding the impacts of complex urbanization pressures on biodiversity.

The search for ocean solutions.

The search for ways to protect and restore ocean health is rapidly accelerating and expanding. A new collection of articles draws on biological and social sciences to suggest changes in how ocean science and conservation are conducted to achieve a sustainable, healthy and inclusive future.

Linking photoacclimation responses and microbiome shifts between depth-segregated sibling species of reef corals.

Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the corals Orbicella annularis and O. franksi, two young species with contrasting vertical distribution in the Caribbean. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation and low mortality, and maintained a consistent bacterial community. By contrast, O. annularis experienced high mortality and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts.

Effects of low pH on the coral reef cryptic invertebrate communities near CO2 vents in Papua New Guinea.

Small cryptic invertebrates (the cryptofauna) are extremely abundant, ecologically important, and species rich on coral reefs. Ongoing ocean acidification is likely to have both direct effects on the biology of these organisms, as well as indirect effects through cascading impacts on their habitats and trophic relationships. Naturally acidified habitats have been important model systems for studying these complex interactions because entire communities that are adapted to these environmental conditions can be analyzed. However, few studies have examined the cryptofauna because they are difficult to census quantitatively in topographically complex habitats and are challenging to identify. We addressed these challenges by using Autonomous Reef Monitoring Structures (ARMS) for sampling reef-dwelling invertebrates >2 mm in size and by using DNA barcoding for taxonomic identifications. The study took place in Papua New Guinea at two reef localities, each with three sites at varying distances from carbon dioxide seeps, thereby sampling across a natural gradient in acidification. We observed sharp overall declines in both the abundance (34-56%) and diversity (42-45%) of organisms in ARMS under the lowest pH conditions sampled (7.64-7.75). However, the overall abundance of gastropods increased slightly in lower pH conditions, and crustacean and gastropod families exhibited varying patterns. There was also variability in response between the two localities, despite their close proximity, as one control pH site displayed unusually low diversity and abundances for all invertebrate groups. The data illustrate the complexity of responses of the reef fauna to pH conditions, and the role of additional factors that influence the diversity and abundance of cryptic reef invertebrates.

Base-substitution mutation rate across the nuclear genome of Alpheus snapping shrimp and the timing of isolation by the Isthmus of Panama.

BACKGROUND: The formation of the Isthmus of Panama and final closure of the Central American Seaway (CAS) provides an independent calibration point for examining the rate of DNA substitutions. This vicariant event has been widely used to estimate the substitution rate across mitochondrial genomes and to date evolutionary events in other taxonomic groups. Nuclear sequence data is increasingly being used to complement mitochondrial datasets for phylogenetic and evolutionary investigations; these studies would benefit from information regarding the rate and pattern of DNA substitutions derived from the nuclear genome. RESULTS: To estimate the genome-wide neutral mutation rate (µ), genotype-by-sequencing (GBS) datasets were generated for three transisthmian species pairs in Alpheus snapping shrimp. A range of bioinformatic filtering parameters were evaluated in order to minimize potential bias in mutation rate estimates that may result from SNP filtering. Using a Bayesian coalescent approach (G-PhoCS) applied to 44,960 GBS loci, we estimated µ to be 2.64E-9 substitutions/site/year, when calibrated with the closure of the CAS at 3 Ma. Post-divergence gene flow was detected in one species pair. Failure to account for this post-split migration inflates our substitution rate estimates, emphasizing the importance of demographic methods that can accommodate gene flow. CONCLUSIONS: Results from our study, both parameter estimates and bioinformatic explorations, have broad-ranging implications for phylogeographic studies in other non-model taxa using reduced representation datasets. Our best estimate of µ that accounts for coalescent and demographic processes is remarkably similar to experimentally derived mutation rates in model arthropod systems. These results contradicted recent suggestions that the closure of the Isthmus was completed much earlier (around 10 Ma), as mutation rates based on an early calibration resulted in uncharacteristically low genomic mutation rates. Also, stricter filtering parameters resulted in biased datasets that generated lower mutation rate estimates and influenced demographic parameters, serving as a cautionary tale for the adherence to conservative bioinformatic strategies when generating reduced-representation datasets at the species level. To our knowledge this is the first use of transisthmian species pairs to calibrate the rate of molecular evolution from GBS data.

Ocean Optimism: Moving Beyond the Obituaries in Marine Conservation.

While the ocean has suffered many losses, there is increasing evidence that important progress is being made in marine conservation. Examples include striking recoveries of once-threatened species, increasing rates of protection of marine habitats, more sustainably managed fisheries and aquaculture, reductions in some forms of pollution, accelerating restoration of degraded habitats, and use of the ocean and its habitats to sequester carbon and provide clean energy. Many of these achievements have multiple benefits, including improved human well-being. Moreover, better understanding of how to implement conservation strategies effectively, new technologies and databases, increased integration of the natural and social sciences, and use of indigenous knowledge promise continued progress. Enormous challenges remain, and there is no single solution; successful efforts typically are neither quick nor cheap and require trust and collaboration. Nevertheless, a greater focus on solutions and successes will help them to become the norm rather than the exception.

Environmental DNA survey captures patterns of fish and invertebrate diversity across a tropical seascape.

Accurate, rapid, and comprehensive biodiversity assessments are critical for investigating ecological processes and supporting conservation efforts. Environmental DNA (eDNA) surveys show promise as a way to effectively characterize fine-scale patterns of community composition. We tested whether a single PCR survey of eDNA in seawater using a broad metazoan primer could identify differences in community composition between five adjacent habitats at 19 sites across a tropical Caribbean bay in Panama. We paired this effort with visual fish surveys to compare methods for a conspicuous taxonomic group. eDNA revealed a tremendous diversity of animals (8,586 operational taxonomic units), including many small taxa that would be undetected in traditional in situ surveys. Fish comprised only 0.07% of the taxa detected by a broad COI primer, yet included 43 species not observed in the visual survey. eDNA revealed significant differences in fish and invertebrate community composition across adjacent habitats and areas of the bay driven in part by taxa known to be habitat-specialists or tolerant to wave action. Our results demonstrate the ability of broad eDNA surveys to identify biodiversity patterns in the ocean.

Rebuilding marine life.

Sustainable Development Goal 14 of the United Nations aims to "conserve and sustainably use the oceans, seas and marine resources for sustainable development". Achieving this goal will require rebuilding the marine life-support systems that deliver the many benefits that society receives from a healthy ocean. Here we document the recovery of marine populations, habitats and ecosystems following past conservation interventions. Recovery rates across studies suggest that substantial recovery of the abundance, structure and function of marine life could be achieved by 2050, if major pressures-including climate change-are mitigated. Rebuilding marine life represents a doable Grand Challenge for humanity, an ethical obligation and a smart economic objective to achieve a sustainable future.

Climate change and ecosystems: threats, opportunities and solutions.

The rapid anthropogenic climate change that is being experienced in the early twenty-first century is intimately entwined with the health and functioning of the biosphere. Climate change is impacting ecosystems through changes in mean conditions and in climate variability, coupled with other associated changes such as increased ocean acidification and atmospheric carbon dioxide concentrations. It also interacts with other pressures on ecosystems, including degradation, defaunation and fragmentation. There is a need to understand the ecological dynamics of these climate impacts, to identify hotspots of vulnerability and resilience and to identify management interventions that may assist biosphere resilience to climate change. At the same time, ecosystems can also assist in the mitigation of, and adaptation to, climate change. The mechanisms, potential and limits of such nature-based solutions to climate change need to be explored and quantified. This paper introduces a thematic issue dedicated to the interaction between climate change and the biosphere. It explores novel perspectives on how ecosystems respond to climate change, how ecosystem resilience can be enhanced and how ecosystems can assist in addressing the challenge of a changing climate. It draws on a Royal Society-National Academy of Sciences Forum held in Washington DC in November 2018, where these themes and issues were discussed. We conclude by identifying some priorities for academic research and practical implementation, in order to maximize the potential for maintaining a diverse, resilient and well-functioning biosphere under the challenging conditions of the twenty-first century. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

GenBank is a reliable resource for 21st century biodiversity research.

Traditional methods of characterizing biodiversity are increasingly being supplemented and replaced by approaches based on DNA sequencing alone. These approaches commonly involve extraction and high-throughput sequencing of bulk samples from biologically complex communities or samples of environmental DNA (eDNA). In such cases, vouchers for individual organisms are rarely obtained, often unidentifiable, or unavailable. Thus, identifying these sequences typically relies on comparisons with sequences from genetic databases, particularly GenBank. While concerns have been raised about biases and inaccuracies in laboratory and analytical methods, comparatively little attention has been paid to the taxonomic reliability of GenBank itself. Here we analyze the metazoan mitochondrial sequences of GenBank using a combination of distance-based clustering and phylogenetic analysis. Because of their comparatively rapid evolutionary rates and consequent high taxonomic resolution, mitochondrial sequences represent an invaluable resource for the detection of the many small and often undescribed organisms that represent the bulk of animal diversity. We show that metazoan identifications in GenBank are surprisingly accurate, even at low taxonomic levels (likely <1% error rate at the genus level). This stands in contrast to previously voiced concerns based on limited analyses of particular groups and the fact that individual researchers currently submit annotated sequences to GenBank without significant external taxonomic validation. Our encouraging results suggest that the rapid uptake of DNA-based approaches is supported by a bioinformatic infrastructure capable of assessing both the losses to biodiversity caused by global change and the effectiveness of conservation efforts aimed at slowing or reversing these losses.

Dietary partitioning promotes the coexistence of planktivorous species on coral reefs.

Theories involving niche diversification to explain high levels of tropical diversity propose that species are more likely to co-occur if they partition at least one dimension of their ecological niche space. Yet, numerous species appear to have widely overlapping niches based upon broad categorizations of resource use or functional traits. In particular, the extent to which food partitioning contributes to species coexistence in hyperdiverse tropical ecosystems remains unresolved. Here, we use a molecular approach to investigate inter- and intraspecific dietary partitioning between two species of damselfish (Dascyllus flavicaudus, Chromis viridis) that commonly co-occur in branching corals. Species-level identification of their diverse zooplankton prey revealed significant differences in diet composition between species despite their seemingly similar feeding strategies. Dascyllus exhibited a more diverse diet than Chromis, whereas Chromis tended to select larger prey items. A large calanoid copepod, Labidocera sp., found in low density and higher in the water column during the day, explained more than 19% of the variation in dietary composition between Dascyllus and Chromis. Dascyllus did not significantly shift its diet in the presence of Chromis, which suggests intrinsic differences in feeding behaviour. Finally, prey composition significantly shifted during the ontogeny of both fish species. Our findings show that levels of dietary specialization among coral reef associated species have likely been underestimated, and they underscore the importance of characterizing trophic webs in tropical ecosystems at higher levels of taxonomic resolution. They also suggest that niche redundancy may not be as common as previously thought.

Climate change promotes parasitism in a coral symbiosis.

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26 °C) and sub-bleaching (31 °C) temperatures under elevated nitrate. Warming to 31 °C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change.

The Paradox of Environmental Symbiont Acquisition in Obligate Mutualisms.

Mutually beneficial interactions between species (mutualisms) shaped the evolution of eukaryotes and remain critical to the survival of species globally [1, 2]. Theory predicts that hosts should pass mutualist symbionts to their offspring (vertical transmission) [3-8]. However, offspring acquire symbionts from the environment in a surprising number of species (horizontal acquisition) [9-12]. A classic example of this paradox is the reef-building corals, in which 71% of species horizontally acquire algal endosymbionts [9]. An untested hypothesis explaining this paradox suggests that horizontal acquisition allows offspring to avoid symbiont-induced harm early in life. We reconstructed the evolution of symbiont transmission across 252 coral species and detected evolutionary transitions consistent with costs of vertical transmission among broadcast spawners, whose eggs tend to be positively buoyant and aggregate at the sea surface. Broadcasters with vertical transmission produce eggs with traits that favor reduced buoyancy (less wax ester lipid) and rapid development to the swimming stage (small egg size), both of which decrease the amount of time offspring spend at the sea surface. Wax ester provisioning decreased after vertically transmitting species evolved brooding from broadcasting, indicating that reduced buoyancy evolves only when offspring bear symbionts. We conclude that horizontal acquisition protects offspring from damage caused by high light and temperatures near the sea surface while providing benefits from enhanced fertilization and outcrossing. These findings help explain why modes of symbiont transmission and reproduction are strongly associated in corals and highlight benefits of delaying mutualist partnerships, offering an additional hypothesis for the pervasiveness of this theoretically paradoxical strategy.

Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions.

Anthropogenic habitats are increasingly prevalent in coastal marine environments. Previous research on sessile epifauna suggests that artificial habitats act as a refuge for nonindigenous species, which results in highly homogenous communities across locations. However, vertebrate assemblages that live in association with artificial habitats are poorly understood. Here, we quantify the biodiversity of small, cryptic (henceforth "cryptobenthic") fishes from marine dock pilings across six locations over 35° of latitude from Maine to Panama. We also compare assemblages from dock pilings to natural habitats in the two southernmost locations (Panama and Belize). Our results suggest that the biodiversity patterns of cryptobenthic fishes from dock pilings follow a Latitudinal Diversity Gradient (LDG), with average local and regional diversity declining sharply with increasing latitude. Furthermore, a strong correlation between community composition and spatial distance suggests distinct regional assemblages of cryptobenthic fishes. Cryptobenthic fish assemblages from dock pilings in Belize and Panama were less diverse and had lower densities than nearby reef habitats. However, dock pilings harbored almost exclusively native species, including two species of conservation concern absent from nearby natural habitats. Our results suggest that, in contrast to sessile epifaunal assemblages on artificial substrates, artificial marine habitats can harbor diverse, regionally characteristic assemblages of vertebrates that follow macroecological patterns that are well documented for natural habitats. We therefore posit that, although dock pilings cannot function as a replacement for natural habitats, dock pilings may provide cost-effective means to preserve native vertebrate biodiversity, and provide a habitat that can be relatively easily monitored to track the status and trends of fish biodiversity in highly urbanized coastal marine environments.