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.

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.

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.

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.

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.

Resolving the depth zonation paradox in reef-building corals.

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

Spatial 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.

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.

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.

Timing anthropogenic stressors to mitigate their impact on marine ecosystem resilience.

Better mitigation of anthropogenic stressors on marine ecosystems is urgently needed to address increasing biodiversity losses worldwide. We explore opportunities for stressor mitigation using whole-of-systems modelling of ecological resilience, accounting for complex interactions between stressors, their timing and duration, background environmental conditions and biological processes. We then search for ecological windows, times when stressors minimally impact ecological resilience, defined here as risk, recovery and resistance. We show for 28 globally distributed seagrass meadows that stressor scheduling that exploits ecological windows for dredging campaigns can achieve up to a fourfold reduction in recovery time and 35% reduction in extinction risk. Although the timing and length of windows vary among sites to some degree, global trends indicate favourable windows in autumn and winter. Our results demonstrate that resilience is dynamic with respect to space, time and stressors, varying most strongly with: (i) the life history of the seagrass genus and (ii) the duration and timing of the impacting stress.

The effect of allometric scaling in coral thermal microenvironments.

A long-standing interest in marine science is in the degree to which environmental conditions of flow and irradiance, combined with optical, thermal and morphological characteristics of individual coral colonies, affects their sensitivity of thermal microenvironments and susceptibility to stress-induced bleaching within and/or among colonies. The physiological processes in Scleractinian corals tend to scale allometrically as a result of physical and geometric constraints on body size and shape. There is a direct relationship between scaling to thermal stress, thus, the relationship between allometric scaling and rates of heating and cooling in coral microenvironments is a subject of great interest. The primary aim of this study was to develop an approximation that predicts coral thermal microenvironments as a function of colony morphology (shape and size), light or irradiance, and flow velocity or regime. To do so, we provided intuitive interpretation of their energy budgets for both massive and branching colonies, and then quantified the heat-size exponent (b*) and allometric constant (m) using logarithmic linear regression. The data demonstrated a positive relationship between thermal rates and changes in irradiance, A/V ratio, and flow, with an interaction where turbulent regime had less influence on overall stress which may serve to ameliorate the effects of temperature rise compared to the laminar regime. These findings indicated that smaller corals have disproportionately higher stress, however they can reach thermal equilibrium quicker. Moreover, excellent agreements between the predicted and simulated microscale temperature values with no significant bias were observed for both the massive and branching colonies, indicating that the numerical approximation should be within the accuracy with which they could be measured. This study may assist in estimating the coral microscale temperature under known conditions of water flow and irradiance, in particular when examining the intra- and inter-colony variability found during periods of bleaching conditions.

Modelling environmental drivers of black band disease outbreaks in populations of foliose corals in the genus Montipora.

Seawater temperature anomalies associated with warming climate have been linked to increases in coral disease outbreaks that have contributed to coral reef declines globally. However, little is known about how seasonal scale variations in environmental factors influence disease dynamics at the level of individual coral colonies. In this study, we applied a multi-state Markov model (MSM) to investigate the dynamics of black band disease (BBD) developing from apparently healthy corals and/or a precursor-stage, termed 'cyanobacterial patches' (CP), in relation to seasonal variation in light and seawater temperature at two reef sites around Pelorus Island in the central sector of the Great Barrier Reef. The model predicted that the proportion of colonies transitioning from BBD to Healthy states within three months was approximately 57%, but 5.6% of BBD cases resulted in whole colony mortality. According to our modelling, healthy coral colonies were more susceptible to BBD during summer months when light levels were at their maxima and seawater temperatures were either rising or at their maxima. In contrast, CP mostly occurred during spring, when both light and seawater temperatures were rising. This suggests that environmental drivers for healthy coral colonies transitioning into a CP state are different from those driving transitions into BBD. Our model predicts that (1) the transition from healthy to CP state is best explained by increasing light, (2) the transition between Healthy to BBD occurs more frequently from early to late summer, (3) 20% of CP infected corals developed BBD, although light and temperature appeared to have limited impact on this state transition, and (4) the number of transitions from Healthy to BBD differed significantly between the two study sites, potentially reflecting differences in localised wave action regimes.

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.

Models of Marine Fish Biodiversity: Assessing Predictors from Three Habitat Classification Schemes.

Prioritising biodiversity conservation requires knowledge of where biodiversity occurs. Such knowledge, however, is often lacking. New technologies for collecting biological and physical data coupled with advances in modelling techniques could help address these gaps and facilitate improved management outcomes. Here we examined the utility of environmental data, obtained using different methods, for developing models of both uni- and multivariate biodiversity metrics. We tested which biodiversity metrics could be predicted best and evaluated the performance of predictor variables generated from three types of habitat data: acoustic multibeam sonar imagery, predicted habitat classification, and direct observer habitat classification. We used boosted regression trees (BRT) to model metrics of fish species richness, abundance and biomass, and multivariate regression trees (MRT) to model biomass and abundance of fish functional groups. We compared model performance using different sets of predictors and estimated the relative influence of individual predictors. Models of total species richness and total abundance performed best; those developed for endemic species performed worst. Abundance models performed substantially better than corresponding biomass models. In general, BRT and MRTs developed using predicted habitat classifications performed less well than those using multibeam data. The most influential individual predictor was the abiotic categorical variable from direct observer habitat classification and models that incorporated predictors from direct observer habitat classification consistently outperformed those that did not. Our results show that while remotely sensed data can offer considerable utility for predictive modelling, the addition of direct observer habitat classification data can substantially improve model performance. Thus it appears that there are aspects of marine habitats that are important for modelling metrics of fish biodiversity that are not fully captured by remotely sensed data. As such, the use of remotely sensed data to model biodiversity represents a compromise between model performance and data availability.

The Point Count Transect Method for Estimates of Biodiversity on Coral Reefs: Improving the Sampling of Rare Species.

Understanding patterns in species richness and diversity over environmental gradients (such as altitude and depth) is an enduring component of ecology. As most biological communities feature few common and many rare species, quantifying the presence and abundance of rare species is a crucial requirement for analysis of these patterns. Coral reefs present specific challenges for data collection, with limitations on time and site accessibility making efficiency crucial. Many commonly used methods, such as line intercept transects (LIT), are poorly suited to questions requiring the detection of rare events or species. Here, an alternative method for surveying reef-building corals is presented; the point count transect (PCT). The PCT consists of a count of coral colonies at a series of sample stations, located at regular intervals along a transect. In contrast the LIT records the proportion of each species occurring under a transect tape of a given length. The same site was surveyed using PCT and LIT to compare species richness estimates between the methods. The total number of species increased faster per individual sampled and unit of time invested using PCT. Furthermore, 41 of the 44 additional species recorded by the PCT occurred ≤ 3 times, demonstrating the increased capacity of PCT to detect rare species. PCT provides a more accurate estimate of local-scale species richness than the LIT, and is an efficient alternative method for surveying reef corals to address questions associated with alpha-diversity, and rare or incidental events.

Key Questions in Marine Megafauna Movement Ecology.

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.