Correction: Remote reefs and seamounts are the last refuges for marine predators across the Indo-Pacific.

[This corrects the article DOI: 10.1371/journal.pbio.3000366.].

Remote reefs and seamounts are the last refuges for marine predators across the Indo-Pacific.

Since the 1950s, industrial fisheries have expanded globally, as fishing vessels are required to travel further afield for fishing opportunities. Technological advancements and fishery subsidies have granted ever-increasing access to populations of sharks, tunas, billfishes, and other predators. Wilderness refuges, defined here as areas beyond the detectable range of human influence, are therefore increasingly rare. In order to achieve marine resources sustainability, large no-take marine protected areas (MPAs) with pelagic components are being implemented. However, such conservation efforts require knowledge of the critical habitats for predators, both across shallow reefs and the deeper ocean. Here, we fill this gap in knowledge across the Indo-Pacific by using 1,041 midwater baited videos to survey sharks and other pelagic predators such as rainbow runner (Elagatis bipinnulata), mahi-mahi (Coryphaena hippurus), and black marlin (Istiompax indica). We modeled three key predator community attributes: vertebrate species richness, mean maximum body size, and shark abundance as a function of geomorphology, environmental conditions, and human pressures. All attributes were primarily driven by geomorphology (35%-62% variance explained) and environmental conditions (14%-49%). While human pressures had no influence on species richness, both body size and shark abundance responded strongly to distance to human markets (12%-20%). Refuges were identified at more than 1,250 km from human markets for body size and for shark abundance. These refuges were identified as remote and shallow seabed features, such as seamounts, submerged banks, and reefs. Worryingly, hotpots of large individuals and of shark abundance are presently under-represented within no-take MPAs that aim to effectively protect marine predators, such as the British Indian Ocean Territory. Population recovery of predators is unlikely to occur without strategic placement and effective enforcement of large no-take MPAs in both coastal and remote locations.

Forecasting intensifying disturbance effects on coral reefs.

Anticipating future changes of an ecosystem's dynamics requires knowledge of how its key communities respond to current environmental regimes. The Great Barrier Reef (GBR) is under threat, with rapid changes of its reef-building hard coral (HC) community structure already evident across broad spatial scales. While several underlying relationships between HC and multiple disturbances have been documented, responses of other benthic communities to disturbances are not well understood. Here we used statistical modelling to explore the effects of broad-scale climate-related disturbances on benthic communities to predict their structure under scenarios of increasing disturbance frequency. We parameterized a multivariate model using the composition of benthic communities estimated by 145,000 observations from the northern GBR between 2012 and 2017. During this time, surveyed reefs were variously impacted by two tropical cyclones and two heat stress events that resulted in extensive HC mortality. This unprecedented sequence of disturbances was used to estimate the effects of discrete versus interacting disturbances on the compositional structure of HC, soft corals (SC) and algae. Discrete disturbances increased the prevalence of algae relative to HC while the interaction between cyclones and heat stress was the main driver of the increase in SC relative to algae and HC. Predictions from disturbance scenarios included relative increases in algae versus SC that varied by the frequency and types of disturbance interactions. However, high uncertainty of compositional changes in the presence of several disturbances shows that responses of algae and SC to the decline in HC needs further research. Better understanding of the effects of multiple disturbances on benthic communities as a whole is essential for predicting the future status of coral reefs and managing them in the light of new environmental regimes. The approach we develop here opens new opportunities for reaching this goal.

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts.

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high-resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown-of-thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km2 , predicting a mean annual coral loss of -0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner-shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no-take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.

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.

The effect of small-scale morphology on thermal dynamics in coral microenvironments.

The thermal microenvironments of corals is a topic of current interest given their relationship to coral bleaching. We present computational fluid dynamics (CFD) model of corals with both smooth and rugged polyp surface topographies for two species of massive corals (Leptastrea purpurea and Platygyra sinensis) in order to predict their microscale surface warming. This study explores whether variation in polyp depth (PD) may directly effect a coral overall surface area-to-volume (A/V) ratio and consequently its surface warming. Validation of our models was made against detailed laboratory measurements of coral surface warming and thermal boundary layer thickness. Our results suggested that while differences in surface warming exist between smooth surfaces and surfaces covered in micro-polyps (5 mm depth), the variation in terms of surface warming is small (~0.18-0.19∘C) and it can be largely attributed to increasing A/V ratios. Our results demonstrated good agreement with measurements of surface temperatures on living corals and that ignoring the presence of polyps by modelling heat transfer associated with a smooth surface makes no material difference to the values obtained or the interpretation of the processes leading to surface warming.

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.

Bayesian adaptive design: improving the effectiveness of monitoring of the Great Barrier Reef.

Monitoring programs are essential for understanding patterns, trends, and threats in ecological and environmental systems. However, such programs are costly in terms of dollars, human resources, and technology, and complex in terms of balancing short- and long-term requirements. In this work, We develop new statistical methods for implementing cost-effective adaptive sampling and monitoring schemes for coral reef that can better utilize existing information and resources, and which can incorporate available prior information. Our research was motivated by developing efficient monitoring practices for Australia's Great Barrier Reef. We develop and implement two types of adaptive sampling schemes, static and sequential, and show that they can be more informative and cost-effective than an existing (nonadaptive) monitoring program. Our methods are developed in a Bayesian framework with a range of utility functions relevant to environmental monitoring. Our results demonstrate the considerable potential for adaptive design to support improved management outcomes in comparison to set-and-forget styles of surveillance monitoring.

Phenotypic covariance at species' borders.

BACKGROUND: Understanding the evolution of species limits is important in ecology, evolution, and conservation biology. Despite its likely importance in the evolution of these limits, little is known about phenotypic covariance in geographically marginal populations, and the degree to which it constrains, or facilitates, responses to selection. We investigated phenotypic covariance in morphological traits at species' borders by comparing phenotypic covariance matrices (P), including the degree of shared structure, the distribution of strengths of pair-wise correlations between traits, the degree of morphological integration of traits, and the ranks of matricies, between central and marginal populations of three species-pairs of coral reef fishes. RESULTS: Greater structural differences in P were observed between populations close to range margins and conspecific populations toward range centres, than between pairs of conspecific populations that were both more centrally located within their ranges. Approximately 80% of all pair-wise trait correlations within populations were greater in the north, but these differences were unrelated to the position of the sampled population with respect to the geographic range of the species. CONCLUSIONS: Neither the degree of morphological integration, nor ranks of P, indicated greater evolutionary constraint at range edges. Characteristics of P observed here provide no support for constraint contributing to the formation of these species' borders, but may instead reflect structural change in P caused by selection or drift, and their potential to evolve in the future.

Multi-scale marine biodiversity patterns inferred efficiently from habitat image processing.

Cost-effective proxies of biodiversity and species abundance, applicable across a range of spatial scales, are needed for setting conservation priorities and planning action. We outline a rapid, efficient, and low-cost measure of spectral signal from digital habitat images that, being an effective proxy for habitat complexity, correlates with species diversity and requires little image processing or interpretation. We validated this method for coral reefs of the Great Barrier Reef (GBR), Australia, across a range of spatial scales (1 m to 10 km), using digital photographs of benthic communities at the transect scale and high-resolution Landsat satellite images at the reef scale. We calculated an index of image-derived spatial heterogeneity, the mean information gain (MIG), for each scale and related it to univariate (species richness and total abundance summed across species) and multivariate (species abundance matrix) measures of fish community structure, using two techniques that account for the hierarchical structure of the data: hierarchical (mixed-effect) linear models and distance-based partial redundancy analysis. Over the length and breadth of the GBR, MIG alone explained up to 29% of deviance in fish species richness, 33% in total fish abundance, and 25% in fish community structure at multiple scales, thus demonstrating the possibility of easily and rapidly exploiting spatial information contained in digital images to complement existing methods for inferring diversity and abundance patterns among fish communities. Thus, the spectral signal of unprocessed remotely sensed images provides an efficient and low-cost way to optimize the design of surveys used in conservation planning. In data-sparse situations, this simple approach also offers a viable method for rapid assessment of potential local biodiversity, particularly where there is little local capacity in terms of skills or resources for mounting in-depth biodiversity surveys.

Reef size and isolation determine the temporal stability of coral reef fish populations.

Temporal variance in species abundance, a potential driver of extinction, is linked to mean abundance through Taylor's power law, the empirical observation of a linear log-log relationship with a slope between 1 and 2 for most species. Here we test the idea that the slope of Taylor's power law can vary both among species and spatially as a function of habitat area and isolation. We used the world's most extensive database of coral reef fish communities comprising a 15-year series of fish abundances on 43 reefs of Australia's Great Barrier Reef. Greater temporal variances were observed at small and isolated reefs, and lower variances at large and connected ones. The combination of reef area and isolation was associated with an even greater effect on temporal variances, indicating strong empirical support for the idea that populations on small and isolated reefs will succumb more frequently to local extinction via higher temporal variability, resulting in lower resilience at the community level. Based on these relationships, we constructed a regional predictive map of the dynamic fragility of coral reef fish assemblages on the Great Barrier Reef.

Latitude and protection affect decadal trends in reef trophic structure over a continental scale.

The relative roles of top-down (consumer-driven) and bottom-up (resource-driven) forcing in exploited marine ecosystems have been much debated. Examples from a variety of marine systems of exploitation-induced, top-down trophic forcing have led to a general view that human-induced predator perturbations can disrupt entire marine food webs, yet other studies that have found no such evidence provide a counterpoint. Though evidence continues to emerge, an unresolved debate exists regarding both the relative roles of top-down versus bottom-up forcing and the capacity of human exploitation to instigate top-down, community-level effects. Using time-series data for 104 reef communities spanning tropical to temperate Australia from 1992 to 2013, we aimed to quantify relationships among long-term trophic group population density trends, latitude, and exploitation status over a continental-scale biogeographic range. Specifically, we amalgamated two long-term monitoring databases of marine community dynamics to test for significant positive or negative trends in density of each of three key trophic levels (predators, herbivores, and algae) across the entire time series at each of the 104 locations. We found that trophic control tended toward bottom-up driven in tropical systems and top-down driven in temperate systems. Further, alternating long-term population trends across multiple trophic levels (a method of identifying trophic cascades), presumably due to top-down trophic forcing, occurred in roughly fifteen percent of locations where the prerequisite significant predator trends occurred. Such alternating trophic trends were significantly more likely to occur at locations with increasing predator densities over time. Within these locations, we found a marked latitudinal gradient in the prevalence of long-term, alternating trophic group trends, from rare in the tropics (<5% of cases) to relatively common in temperate areas (~45%). Lastly, the strongest trends in predator and algal density occurred in older no-take marine reserves; however, exploitation status did not affect the likelihood of alternating long-term trophic group trends occurring. Our data suggest that the type and degree of trophic forcing in this system are likely related to one or more covariates of latitude, and that ecosystem resiliency to top-down control does not universally vary in this system based on exploitation level.

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.

Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation.

BACKGROUND: Management strategies for coral reefs are dependant on information about the spatial population structure and connectivity of reef organisms. Genetic tools can reveal important information about population structure, however, this information is lacking for many reef species. We used a mitochondrial molecular marker to examine the population genetic structure and the potential for meta-population dynamics in a direct developing coral reef fish using 283 individuals from 15 reefs on the Great Barrier Reef, Australia. We employed a hierarchical sampling design to test genetic models of population structure at multiple geographical scales including among regions, among shelf position and reefs within regions. Predictions from island, isolation-by-distance and meta-population models, including the potential for asymmetric migration, local extinction and patterns of re-colonisation were examined. RESULTS: Acanthochromis polyacanthus displayed strong genetic structure among regions (PhiST = 0.81, P < 0.0001) that supported an equilibrium isolation-by-distance model (r = 0.77, P = 0.001). Significant structuring across the continental shelf was only evident in the northern region (PhiST = 0.31, P < 0.001) and no evidence of isolation-by-distance was found within any region. Pairwise PhiST values indicated overall strong but variable genetic structure (mean PhiST among reefs within regions = 0.28, 0.38, 0.41), and asymmetric migration rates among reefs with low genetic structure. Genetic differentiation among younger reefs was greater than among older reefs supporting a meta-population propagule-pool colonisation model. Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one. CONCLUSION: Our findings provide genetic evidence for meta-population dynamics in a direct developing coral reef fish and we reject the equilibrium island and isolation-by distance models at local spatial scales. Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations. These meta-population dynamics varied across the geographical range examined with edge populations exhibiting lower genetic diversities and higher rates of population expansion than more central populations. Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.

Factors affecting the evolution of bleaching resistance in corals.

We present a mathematical model of coevolutionary interactions between partners in a coral-algae mutualistic symbiosis. Our goal is to better understand factors affecting the potential evolution of bleaching resistance in corals in response to increased average sea temperatures. We explore the evolutionary consequences of four factors: (i) trade-offs among fitness components, (ii) different proximate mechanisms of coral bleaching, (iii) the genetic determination of bleaching resistance, and (iv) the mode of sexual reproduction. We show that traits in mutualistic symbioses, such as thermal tolerance in corals, are potentially subject to novel kinds of evolutionary constraints and that these constraints are mediated by ecological dynamics. We also show that some proximate mechanisms of bleaching yield faster evolutionary responses to temperature stress and that the nature of interspecific control of bleaching resistance and the mode of sexual reproduction interact to strongly influence the rate of spread of resistance alleles. These qualitative theoretical results highlight important future directions for empirical research in order to quantify the potential for coral reefs to evolve resistance to thermal stress.

Prediction of solar irradiance using ray-tracing techniques for coral macro- and micro-habitats.

Light distribution on coral reefs is very heterogeneous at the microhabitat level and is an important determinant of coral thermal microenvironments. This study implemented a solar load model that uses a backward ray-tracing method to estimate macroscale and microscale variations of solar irradiance penetrating the ocean surface and impacting the surfaces of coral colonies. We then explored whether morphological characteristics such as tissue darkness (or pigmentation) and thickness may influence the amount of light captured and its spectral distribution by two contrasting coral colony morphologies, branching and massive. Results of global horizontal irradiance above and below the sea-surface and at the surface of coral colonies were validated using spectrometer scans, field measurements, and empirical correlations. The macroscale results of horizontal, irradiated, and shaded irradiance levels and solar altitude angles for PAR, UVA and UVB compared very well with the spectrometer-based observations (typically within < 5%). In general, a comparison between the model results and field and empirical measurements indicated that the contributions of clouds, turbidity, and tides to variations in irradiance at various depth (up to 5 m) were typically within 5-10% of each other. Moreover, the effect of colony darkness or pigmentation on light microenvironment was notably more pronounced for the massive species than branching colony. This study provided insights that species with thinner tissue have the ability to intercept more light with the difference in terms of irradiance levels between 0.1 mm and 0.8 mm tissue thickness for both massive and branching colonies were approximately 2 W m-2, which was quite unlikely to influence the overall coral heat budgets.

Using virtual reality to estimate aesthetic values of coral reefs.

Aesthetic value, or beauty, is important to the relationship between humans and natural environments and is, therefore, a fundamental socio-economic attribute of conservation alongside other ecosystem services. However, beauty is difficult to quantify and is not estimated well using traditional approaches to monitoring coral-reef aesthetics. To improve the estimation of ecosystem aesthetic values, we developed and implemented a novel framework used to quantify features of coral-reef aesthetics based on people's perceptions of beauty. Three observer groups with different experience to reef environments (Marine Scientist, Experienced Diver and Citizen) were virtually immersed in Australian's Great Barrier Reef (GBR) using 360° images. Perceptions of beauty and observations were used to assess the importance of eight potential attributes of reef-aesthetic value. Among these, heterogeneity, defined by structural complexity and colour diversity, was positively associated with coral-reef-aesthetic values. There were no group-level differences in the way the observer groups perceived reef aesthetics suggesting that past experiences with coral reefs do not necessarily influence the perception of beauty by the observer. The framework developed here provides a generic tool to help identify indicators of aesthetic value applicable to a wide variety of natural systems. The ability to estimate aesthetic values robustly adds an important dimension to the holistic conservation of the GBR, coral reefs worldwide and other natural ecosystems.

Challenges of transferring models of fish abundance between coral reefs.

Reliable abundance estimates for species are fundamental in ecology, fisheries, and conservation. Consequently, predictive models able to provide reliable estimates for un- or poorly-surveyed locations would prove a valuable tool for management. Based on commonly used environmental and physical predictors, we developed predictive models of total fish abundance and of abundance by fish family for ten representative taxonomic families for the Great Barrier Reef (GBR) using multiple temporal scenarios. We then tested if models developed for the GBR (reference system) could predict fish abundances at Ningaloo Reef (NR; target system), i.e., if these GBR models could be successfully transferred to NR. Models of abundance by fish family resulted in improved performance (e.g., 44.1%  0.05). High spatio-temporal variability of patterns in fish abundance at the family and population levels in both reef systems likely affected the transferability of these models. Inclusion of additional predictors with potential direct effects on abundance, such as local fishing effort or topographic complexity, may improve transferability of fish abundance models. However, observations of these local-scale predictors are often not available, and might thereby hinder studies on model transferability and its usefulness for conservation planning and management.

Outstanding Challenges in the Transferability of Ecological Models.

Predictive models are central to many scientific disciplines and vital for informing management in a rapidly changing world. However, limited understanding of the accuracy and precision of models transferred to novel conditions (their 'transferability') undermines confidence in their predictions. Here, 50 experts identified priority knowledge gaps which, if filled, will most improve model transfers. These are summarized into six technical and six fundamental challenges, which underlie the combined need to intensify research on the determinants of ecological predictability, including species traits and data quality, and develop best practices for transferring models. Of high importance is the identification of a widely applicable set of transferability metrics, with appropriate tools to quantify the sources and impacts of prediction uncertainty under novel conditions.

From transcriptome to biological function: environmental stress in an ectothermic vertebrate, the coral reef fish Pomacentrus moluccensis.

BACKGROUND: Our understanding of the importance of transcriptional regulation for biological function is continuously improving. We still know, however, comparatively little about how environmentally induced stress affects gene expression in vertebrates, and the consistency of transcriptional stress responses to different types of environmental stress. In this study, we used a multi-stressor approach to identify components of a common stress response as well as components unique to different types of environmental stress. We exposed individuals of the coral reef fish Pomacentrus moluccensis to hypoxic, hyposmotic, cold and heat shock and measured the responses of approximately 16,000 genes in liver. We also compared winter and summer responses to heat shock to examine the capacity for such responses to vary with acclimation to different ambient temperatures. RESULTS: We identified a series of gene functions that were involved in all stress responses examined here, suggesting some common effects of stress on biological function. These common responses were achieved by the regulation of largely independent sets of genes; the responses of individual genes varied greatly across different stress types. In response to heat exposure over five days, a total of 324 gene loci were differentially expressed. Many heat-responsive genes had functions associated with protein turnover, metabolism, and the response to oxidative stress. We were also able to identify groups of co-regulated genes, the genes within which shared similar functions. CONCLUSION: This is the first environmental genomic study to measure gene regulation in response to different environmental stressors in a natural population of a warm-adapted ectothermic vertebrate. We have shown that different types of environmental stress induce expression changes in genes with similar gene functions, but that the responses of individual genes vary between stress types. The functions of heat-responsive genes suggest that prolonged heat exposure leads to oxidative stress and protein damage, a challenge of the immune system, and the re-allocation of energy sources. This study hence offers insight into the effects of environmental stress on biological function and sheds light on the expected sensitivity of coral reef fishes to elevated temperatures in the future.