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.

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.

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.

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.

Tropical dead zones and mass mortalities on coral reefs.

Degradation of coastal water quality in the form of low dissolved oxygen levels (hypoxia) can harm biodiversity, ecosystem function, and human wellbeing. Extreme hypoxic conditions along the coast, leading to what are often referred to as "dead zones," are known primarily from temperate regions. However, little is known about the potential threat of hypoxia in the tropics, even though the known risk factors, including eutrophication and elevated temperatures, are common. Here we document an unprecedented hypoxic event on the Caribbean coast of Panama and assess the risk of dead zones to coral reefs worldwide. The event caused coral bleaching and massive mortality of corals and other reef-associated organisms, but observed shifts in community structure combined with laboratory experiments revealed that not all coral species are equally sensitive to hypoxia. Analyses of global databases showed that coral reefs are associated with more than half of the known tropical dead zones worldwide, with >10% of all coral reefs at elevated risk for hypoxia based on local and global risk factors. Hypoxic events in the tropics and associated mortality events have likely been underreported, perhaps by an order of magnitude, because of the lack of local scientific capacity for their detection. Monitoring and management plans for coral reef resilience should incorporate the growing threat of coastal hypoxia and include support for increased detection and research capacity.

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.

DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity.

Documenting the diversity of marine life is challenging because many species are cryptic, small, and rare, and belong to poorly known groups. New sequencing technologies, especially when combined with standardized sampling, promise to make comprehensive biodiversity assessments and monitoring feasible on a large scale. We used this approach to characterize patterns of diversity on oyster reefs across a range of geographic scales comprising a temperate location [Virginia (VA)] and a subtropical location [Florida (FL)]. Eukaryotic organisms that colonized multilayered settlement surfaces (autonomous reef monitoring structures) over a 6-mo period were identified by cytochrome c oxidase subunit I barcoding (>2-mm mobile organisms) and metabarcoding (sessile and smaller mobile organisms). In a total area of ∼ 15.64 m(2) and volume of ∼ 0.09 m(3), 2,179 operational taxonomic units (OTUs) were recorded from 983,056 sequences. However, only 10.9% could be matched to reference barcodes in public databases, with only 8.2% matching barcodes with both genus and species names. Taxonomic coverage was broad, particularly for animals (22 phyla recorded), but 35.6% of OTUs detected via metabarcoding could not be confidently assigned to a taxonomic group. The smallest size fraction (500 to 106 µm) was the most diverse (more than two-thirds of OTUs). There was little taxonomic overlap between VA and FL, and samples separated by ∼ 2 m were significantly more similar than samples separated by ∼ 100 m. Ground-truthing with independent assessments of taxonomic composition indicated that both presence-absence information and relative abundance information are captured by metabarcoding data, suggesting considerable potential for ecological studies and environmental monitoring.

Commonness and rarity in the marine biosphere.

Explaining patterns of commonness and rarity is fundamental for understanding and managing biodiversity. Consequently, a key test of biodiversity theory has been how well ecological models reproduce empirical distributions of species abundances. However, ecological models with very different assumptions can predict similar species abundance distributions, whereas models with similar assumptions may generate very different predictions. This complicates inferring processes driving community structure from model fits to data. Here, we use an approximation that captures common features of "neutral" biodiversity models--which assume ecological equivalence of species--to test whether neutrality is consistent with patterns of commonness and rarity in the marine biosphere. We do this by analyzing 1,185 species abundance distributions from 14 marine ecosystems ranging from intertidal habitats to abyssal depths, and from the tropics to polar regions. Neutrality performs substantially worse than a classical nonneutral alternative: empirical data consistently show greater heterogeneity of species abundances than expected under neutrality. Poor performance of neutral theory is driven by its consistent inability to capture the dominance of the communities' most-abundant species. Previous tests showing poor performance of a neutral model for a particular system often have been followed by controversy about whether an alternative formulation of neutral theory could explain the data after all. However, our approach focuses on common features of neutral models, revealing discrepancies with a broad range of empirical abundance distributions. These findings highlight the need for biodiversity theory in which ecological differences among species, such as niche differences and demographic trade-offs, play a central role.

Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea.

High-throughput sequencing (HTS) of DNA barcodes (metabarcoding), particularly when combined with standardized sampling protocols, is one of the most promising approaches for censusing overlooked cryptic invertebrate communities. We present biodiversity estimates based on sequencing of the cytochrome c oxidase subunit 1 (COI) gene for coral reefs of the Gulf of Aqaba, a semi-enclosed system in the northern Red Sea. Samples were obtained from standardized sampling devices (Autonomous Reef Monitoring Structures (ARMS)) deployed for 18 months. DNA barcoding of non-sessile specimens >2 mm revealed 83 OTUs in six phyla, of which only 25% matched a reference sequence in public databases. Metabarcoding of the 2 mm - 500 µm and sessile bulk fractions revealed 1197 OTUs in 15 animal phyla, of which only 4.9% matched reference barcodes. These results highlight the scarcity of COI data for cryptobenthic organisms of the Red Sea. Compared with data obtained using similar methods, our results suggest that Gulf of Aqaba reefs are less diverse than two Pacific coral reefs but much more diverse than an Atlantic oyster reef at a similar latitude. The standardized approaches used here show promise for establishing baseline data on biodiversity, monitoring the impacts of environmental change, and quantifying patterns of diversity at regional and global scales.

The Global Invertebrate Genomics Alliance (GIGA): developing community resources to study diverse invertebrate genomes.

Over 95% of all metazoan (animal) species comprise the "invertebrates," but very few genomes from these organisms have been sequenced. We have, therefore, formed a "Global Invertebrate Genomics Alliance" (GIGA). Our intent is to build a collaborative network of diverse scientists to tackle major challenges (e.g., species selection, sample collection and storage, sequence assembly, annotation, analytical tools) associated with genome/transcriptome sequencing across a large taxonomic spectrum. We aim to promote standards that will facilitate comparative approaches to invertebrate genomics and collaborations across the international scientific community. Candidate study taxa include species from Porifera, Ctenophora, Cnidaria, Placozoa, Mollusca, Arthropoda, Echinodermata, Annelida, Bryozoa, and Platyhelminthes, among others. GIGA will target 7000 noninsect/nonnematode species, with an emphasis on marine taxa because of the unrivaled phyletic diversity in the oceans. Priorities for selecting invertebrates for sequencing will include, but are not restricted to, their phylogenetic placement; relevance to organismal, ecological, and conservation research; and their importance to fisheries and human health. We highlight benefits of sequencing both whole genomes (DNA) and transcriptomes and also suggest policies for genomic-level data access and sharing based on transparency and inclusiveness. The GIGA Web site (http://giga.nova.edu) has been launched to facilitate this collaborative venture.

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.

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.

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.

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.

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.