Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

The threat to coral reefs from more intense cyclones under climate change.

Ocean warming under climate change threatens coral reefs directly, through fatal heat stress to corals and indirectly, by boosting the energy of cyclones that cause coral destruction and loss of associated organisms. Although cyclone frequency is unlikely to rise, cyclone intensity is predicted to increase globally, causing more frequent occurrences of the most destructive cyclones with potentially severe consequences for coral reef ecosystems. While increasing heat stress is considered a pervasive risk to coral reefs, quantitative estimates of threats from cyclone intensification are lacking due to limited data on cyclone impacts to inform projections. Here, using extensive data from Australia's Great Barrier Reef (GBR), we show that increases in cyclone intensity predicted for this century are sufficient to greatly accelerate coral reef degradation. Coral losses on the outer GBR were small, localized and offset by gains on undisturbed reefs for more than a decade, despite numerous cyclones and periods of record heat stress, until three unusually intense cyclones over 5 years drove coral cover to record lows over >1500 km. Ecological damage was particularly severe in the central-southern region where 68% of coral cover was destroyed over >1000 km, forcing record declines in the species richness and abundance of associated fish communities, with many local extirpations. Four years later, recovery of average coral cover was relatively slow and there were further declines in fish species richness and abundance. Slow recovery of community diversity appears likely from such a degraded starting point. Highly unusual characteristics of two of the cyclones, aside from high intensity, inflated the extent of severe ecological damage that would more typically have occurred over 100s of km. Modelling published predictions of future cyclone activity, the likelihood of more intense cyclones within time frames of coral recovery by mid-century poses a global threat to coral reefs and dependent societies.

Delayed coral recovery in a warming ocean.

Climate change threatens coral reefs across the world. Intense bleaching has caused dramatic coral mortality in many tropical regions in recent decades, but less obvious chronic effects of temperature and other stressors can be equally threatening to the long-term persistence of diverse coral-dominated reef systems. Coral reefs persist if coral recovery rates equal or exceed average rates of mortality. While mortality from acute destructive events is often obvious and easy to measure, estimating recovery rates and investigating the factors that influence them requires long-term commitment. Coastal development is increasing in many regions, and sea surface temperatures are also rising. The resulting chronic stresses have predictable, adverse effects on coral recovery, but the lack of consistent long-term data sets has prevented measurement of how much coral recovery rates are actually changing. Using long-term monitoring data from 47 reefs spread over 10 degrees of latitude on Australia's Great Barrier Reef (GBR), we used a modified Gompertz equation to estimate coral recovery rates following disturbance. We compared coral recovery rates in two periods: 7 years before and 7 years after an acute and widespread heat stress event on the GBR in 2002. From 2003 to 2009, there were few acute disturbances in the region, allowing us to attribute the observed shortfall in coral recovery rates to residual effects of acute heat stress plus other chronic stressors. Compared with the period before 2002, the recovery of fast-growing Acroporidae and of "Other" slower growing hard corals slowed after 2002, doubling the time taken for modest levels of recovery. If this persists, recovery times will be increasing at a time when acute disturbances are predicted to become more frequent and intense. Our study supports the need for management actions to protect reefs from locally generated stresses, as well as urgent global action to mitigate climate change.

Corrigendum: Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

[This corrects the article DOI: 10.1093/biosci/biw180.].

Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continental- and decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.

The 27-year decline of coral cover on the Great Barrier Reef and its causes.

The world's coral reefs are being degraded, and the need to reduce local pressures to offset the effects of increasing global pressures is now widely recognized. This study investigates the spatial and temporal dynamics of coral cover, identifies the main drivers of coral mortality, and quantifies the rates of potential recovery of the Great Barrier Reef. Based on the world's most extensive time series data on reef condition (2,258 surveys of 214 reefs over 1985-2012), we show a major decline in coral cover from 28.0% to 13.8% (0.53% y(-1)), a loss of 50.7% of initial coral cover. Tropical cyclones, coral predation by crown-of-thorns starfish (COTS), and coral bleaching accounted for 48%, 42%, and 10% of the respective estimated losses, amounting to 3.38% y(-1) mortality rate. Importantly, the relatively pristine northern region showed no overall decline. The estimated rate of increase in coral cover in the absence of cyclones, COTS, and bleaching was 2.85% y(-1), demonstrating substantial capacity for recovery of reefs. In the absence of COTS, coral cover would increase at 0.89% y(-1), despite ongoing losses due to cyclones and bleaching. Thus, reducing COTS populations, by improving water quality and developing alternative control measures, could prevent further coral decline and improve the outlook for the Great Barrier Reef. Such strategies can, however, only be successful if climatic conditions are stabilized, as losses due to bleaching and cyclones will otherwise increase.

Spatial variation in the functional characteristics of herbivorous fish communities and the resilience of coral reefs.

Many ecosystems face degradation unless factors that underpin their resilience can be effectively managed. In tropical reef ecosystems, grazing by herbivorous fishes can prevent coral-macroalgal phase shifts that commonly signal loss of resilience. However, knowledge of grazing characteristics that most promote resilience is typically experimental, localized, and sparse, which limits broad management applications. Applying sound ecological theory to broad-scale data may provide an alternative basis for ecosystem management. We explore the idea that resilience is positively related to the diversity within and among functional groups of organisms. Specifically, we infer the relative vulnerability of different subregions of the Great Barrier Reef (GBR) to phase shifts based on functional characteristics of the local herbivorous fish communities. Reef slopes on 92 reefs set in three zones of the continental shelf in eight latitudinal sectors of the GBR were surveyed on multiple occasions between 1995 and 2009. Spatial variation in fish community structure was high and driven primarily by shelf position. Measures of functional diversity, functional redundancy, and abundance were generally higher offshore and lower inshore. Two turbid inshore subregions were considered most vulnerable based on very low measures of herbivore function, and this was supported by the occurrence of phase shifts within one of three subregions. Eleven reefs that resisted phase shifts after major coral mortality included some with very low measures of herbivore function. The fact that phase shifts did not necessarily occur when large herbivores were scarce indicates that other environmental factors compensated to preserve resilience. Estimates of vulnerability based solely on herbivore function may thus prove conservative, but caution is appropriate, since compensatory factors are largely unknown and could be eroded unwittingly by anthropogenic stresses. Our data suggest that managing the threat of phase shifts in coral reef ecosystems successfully will require spatially explicit strategies that consider both the functional characteristics of local herbivore communities and environmental factors that may raise or lower resilience thresholds. A strong positive correlation between water clarity and the species richness and abundance of herbivorous fishes suggests that management of water quality is of generic importance to ensure the ecosystem services of this important group of herbivores.

Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves.

The Great Barrier Reef (GBR) provides a globally significant demonstration of the effectiveness of large-scale networks of marine reserves in contributing to integrated, adaptive management. Comprehensive review of available evidence shows major, rapid benefits of no-take areas for targeted fish and sharks, in both reef and nonreef habitats, with potential benefits for fisheries as well as biodiversity conservation. Large, mobile species like sharks benefit less than smaller, site-attached fish. Critically, reserves also appear to benefit overall ecosystem health and resilience: outbreaks of coral-eating, crown-of-thorns starfish appear less frequent on no-take reefs, which consequently have higher abundance of coral, the very foundation of reef ecosystems. Effective marine reserves require regular review of compliance: fish abundances in no-entry zones suggest that even no-take zones may be significantly depleted due to poaching. Spatial analyses comparing zoning with seabed biodiversity or dugong distributions illustrate significant benefits from application of best-practice conservation principles in data-poor situations. Increases in the marine reserve network in 2004 affected fishers, but preliminary economic analysis suggests considerable net benefits, in terms of protecting environmental and tourism values. Relative to the revenue generated by reef tourism, current expenditure on protection is minor. Recent implementation of an Outlook Report provides regular, formal review of environmental condition and management and links to policy responses, key aspects of adaptive management. Given the major threat posed by climate change, the expanded network of marine reserves provides a critical and cost-effective contribution to enhancing the resilience of the Great Barrier Reef.

Diversity and stability of herbivorous fishes on coral reefs.

Biodiversity may provide insurance against ecosystem collapse by stabilizing assemblages that perform particular ecological functions (the "portfolio effect"). However, the extent to which this occurs in nature and the importance of different mechanisms that generate portfolio effects remain controversial. On coral reefs, herbivory helps maintain coral dominated states, so volatility in levels of herbivory has important implications for reef ecosystems. Here, we used an extensive time series of abundances on 35 reefs of the Great Barrier Reef of Australia to quantify the strength of the portfolio effect for herbivorous fishes. Then, we disentangled the contributions of two mechanisms that underlie it (compensatory interactions and differential responses to environmental fluctuations ["response diversity"]) by fitting a community-dynamic model that explicitly includes terms for both mechanisms. We found that portfolio effects operate strongly in herbivorous fishes, as shown by nearly independent fluctuations in abundances over time. Moreover, we found strong evidence for high response diversity, with nearly independent responses to environmental fluctuations. In contrast, we found little evidence that the portfolio effect in this system was enhanced by compensatory ecological interactions. Our results show that portfolio effects are driven principally by response diversity for herbivorous fishes on coral reefs. We conclude that portfolio effects can be very strong in nature and that, for coral reefs in particular, response diversity may help maintain herbivory above the threshold levels that trigger regime shifts.

Volatility in coral cover erodes niche structure, but not diversity, in reef fish assemblages.

The world's coral reefs are experiencing increasing volatility in coral cover, largely because of anthropogenic environmental change, highlighting the need to understand how such volatility will influence the structure and dynamics of reef assemblages. These changes may influence not only richness or evenness but also the temporal stability of species' relative abundances (temporal beta-diversity). Here, we analyzed reef fish assemblage time series from the Great Barrier Reef to show that, overall, 75% of the variance in abundance among species was attributable to persistent differences in species' long-term mean abundances. However, the relative importance of stochastic fluctuations in abundance was higher on reefs that experienced greater volatility in coral cover, whereas it did not vary with drivers of alpha-diversity. These findings imply that increased coral cover volatility decreases temporal stability in relative abundances of fishes, a transformation that is not detectable from static measures of biodiversity.

Rapid increase in fish numbers follows creation of world's largest marine reserve network.

No-take marine reserves (NTMRs) are much advocated as a solution to managing marine ecosystems, protecting exploited species and restoring natural states of biodiversity [1,2]. Increasingly, it is becoming clear that effective marine conservation and management at ecosystem and regional scales requires extensive networks of NTMRs [1,2]. The world's largest network of such reserves was established on Australia's Great Barrier Reef (GBR) in 2004. Closing such a large area to all fishing has been socially and politically controversial, making it imperative that the effectiveness of this new reserve network be assessed. Here we report evidence, first, that the densities of the major target species of the GBR reef line fisheries were significantly higher in the new NTMRs, compared with fished sites, in just two years; and second, that the positive differences were consistent for multiple marine reserves over an unprecedented spatial scale (>1,000 km).

Thermal stress and coral cover as drivers of coral disease outbreaks.

Very little is known about how environmental changes such as increasing temperature affect disease dynamics in the ocean, especially at large spatial scales. We asked whether the frequency of warm temperature anomalies is positively related to the frequency of coral disease across 1,500 km of Australia's Great Barrier Reef. We used a new high-resolution satellite dataset of ocean temperature and 6 y of coral disease and coral cover data from annual surveys of 48 reefs to answer this question. We found a highly significant relationship between the frequencies of warm temperature anomalies and of white syndrome, an emergent disease, or potentially, a group of diseases, of Pacific reef-building corals. The effect of temperature was highly dependent on coral cover because white syndrome outbreaks followed warm years, but only on high (>50%) cover reefs, suggesting an important role of host density as a threshold for outbreaks. Our results indicate that the frequency of temperature anomalies, which is predicted to increase in most tropical oceans, can increase the susceptibility of corals to disease, leading to outbreaks where corals are abundant.

Can juvenile corals be surveyed effectively using digital photography?: implications for rapid assessment techniques.

The widespread decline of coral reefs requires integrated management measures across whole regions. Knowledge of demographic processes of reef organisms is important for informed management, yet current techniques for assessing such processes are time consuming, making it impractical to gather relevant information over large scales. We tested the usefulness of digital still photography as a rapid assessment technique to estimate coral recruitment--an important process in coral reef recovery. Estimates of the density and diversity of juvenile hard corals from digital images were compared with direct visual estimates from the same plots made in the field. Multiple plots were sampled on four reefs from a range of locations on Australia's Great Barrier Reef. On average, estimates of juvenile densities from photographic images were lower, in both absolute and relative terms, than that estimated from images. This was the case whether colonies <20 mm or <50 mm in diameter were considered. Overall differences between methods were generally greater at reefs where recruitment was higher, though proportional differences (density from images/density from direct visual census) still varied among reefs. Although the ranking of taxa, in terms of their densities, from the two methods were similar, the density of common genera was generally underestimated in images, and the occurrence of 'unknown' taxa was higher. We conclude that photographic images do not constitute a reliable rapid assessment method for estimating the spatial patterns in the density or diversity of juvenile hard corals.

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.

A ubiquitous subcuticular bacterial symbiont of a coral predator, the crown-of-thorns starfish, in the Indo-Pacific.

BACKGROUND: Population outbreaks of the crown-of-thorns starfish (Acanthaster planci sensu lato; COTS), a primary predator of reef-building corals in the Indo-Pacific Ocean, are a major threat to coral reefs. While biological and ecological knowledge of COTS has been accumulating since the 1960s, little is known about its associated bacteria. The aim of this study was to provide fundamental information on the dominant COTS-associated bacteria through a multifaceted molecular approach. METHODS: A total of 205 COTS individuals from 17 locations throughout the Indo-Pacific Ocean were examined for the presence of COTS-associated bacteria. We conducted 16S rRNA metabarcoding of COTS to determine the bacterial profiles of different parts of the body and generated a full-length 16S rRNA gene sequence from a single dominant bacterium, which we designated COTS27. We performed phylogenetic analysis to determine the taxonomy, screening of COTS27 across the Indo-Pacific, FISH to visualize it within the COTS tissues, and reconstruction of the bacterial genome from the hologenome sequence data. RESULTS: We discovered that a single bacterium exists at high densities in the subcuticular space in COTS forming a biofilm-like structure between the cuticle and the epidermis. COTS27 belongs to a clade that presumably represents a distinct order (so-called marine spirochetes) in the phylum Spirochaetes and is universally present in COTS throughout the Indo-Pacific Ocean. The reconstructed genome of COTS27 includes some genetic traits that are probably linked to adaptation to marine environments and evolution as an extracellular endosymbiont in subcuticular spaces. CONCLUSIONS: COTS27 can be found in three allopatric COTS species, ranging from the northern Red Sea to the Pacific, implying that the symbiotic relationship arose before the speciation events (approximately 2 million years ago). The universal association of COTS27 with COTS and nearly mono-specific association at least with the Indo-Pacific COTS provides a useful model system for studying symbiont-host interactions in marine invertebrates and may have applications for coral reef conservation. Video Abstract.

Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs.

Many marine scientists have concluded that coral reefs are moving toward or are locked into a seaweed-dominated state. However, because there have been no regional- or global-scale analyses of such coral reef "phase shifts," the magnitude of this phenomenon was unknown. We analyzed 3581 quantitative surveys of 1851 reefs performed between 1996 and 2006 to determine the frequency, geographical extent, and degree of macroalgal dominance of coral reefs and of coral to macroalgal phase shifts around the world. Our results indicate that the replacement of corals by macroalgae as the dominant benthic functional group is less common and less geographically extensive than assumed. Although we found evidence of moderate local increases in macroalgal cover, particularly in the Caribbean, only 4% of reefs were dominated by macroalgae (i.e., > 50% cover). Across the Indo-Pacific, where regional averages of macroalgal cover were 9-12%, macroalgae only dominated 1% of the surveyed reefs. Between 1996 and 2006, phase shift severity decreased in the Caribbean, did not change in the Florida Keys and Indo-Pacific, and increased slightly on the Great Barrier Reef due to moderate coral loss. Coral reef ecosystems appear to be more resistant to macroalgal blooms than assumed, which has important implications for reef management.

Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment.

1. The impact of environmental disturbance and habitat loss on associated species is expected to be dependent on a species' level of specialization. We examined habitat use and specialization of coral reef fish from the diverse and ecologically important family Pomacentridae, and determined which species are susceptible to declines in coral cover due to disturbance induced by crown-of-thorns seastar (COTS, Acanthaster planci L.). 2. A high proportion of pomacentrid species live in association with live coral as adults (40%) or juveniles (53%). Adults of many species had strong affiliations with branching corals, while juveniles favoured plating growth forms, reflecting the sizes of refuge provided by coral types. 3. Juveniles of species that associated with coral had narrower niche breadths than adult conspecifics, due to associations with specific coral types. The especially high coral association and narrower niche breadth of juveniles suggest that the presence of live coral is crucial for many species during early life history, and that disturbance-induced coral loss may have serious flow-on effects on adult abundance. 4. Microhabitat availability was a poor predictor of fish species abundance. Significant correlations between coverage of coral types and abundance of five adults and two juvenile species were detected; however, these relationships explained <35% and <10% of the variation in abundance of adult and juvenile species, respectively. 5. Niche breadth explained 74% of the variation in species' mean response to coral decline and it is clear that disturbance has a greater impact on resource specialists, suggesting that increasing frequency and intensity of coral loss will cause reef fish communities to become dominated by habitat generalists at the expense of coral-dwelling specialists.

Reef fish communities are spooked by scuba surveys and may take hours to recover.

Ecological monitoring programs typically aim to detect changes in the abundance of species of conservation concern or which reflect system status. Coral reef fish assemblages are functionally important for reef health and these are most commonly monitored using underwater visual surveys (UVS) by divers. In addition to estimating numbers, most programs also collect estimates of fish lengths to allow calculation of biomass, an important determinant of a fish's functional impact. However, diver surveys may be biased because fishes may either avoid or are attracted to divers and the process of estimating fish length could result in fish counts that differ from those made without length estimations. Here we investigated whether (1) general diver disturbance and (2) the additional task of estimating fish lengths affected estimates of reef fish abundance and species richness during UVS, and for how long. Initial estimates of abundance and species richness were significantly higher than those made on the same section of reef after diver disturbance. However, there was no evidence that estimating fish lengths at the same time as abundance resulted in counts different from those made when estimating abundance alone. Similarly, there was little consistent bias among observers. Estimates of the time for fish taxa that avoided divers after initial contact to return to initial levels of abundance varied from three to 17 h, with one group of exploited fishes showing initial attraction to divers that declined over the study period. Our finding that many reef fishes may disperse for such long periods after initial contact with divers suggests that monitoring programs should take great care to minimise diver disturbance prior to surveys.

Assessing Different Causes of Crown-of-Thorns Starfish Outbreaks and Appropriate Responses for Management on the Great Barrier Reef.

The crown-of-thorns starfish Acanthaster planci (COTS) has contributed greatly to declines in coral cover on Australia's Great Barrier Reef, and remains one of the major acute disturbances on Indo-Pacific coral reefs. Despite uncertainty about the underlying causes of outbreaks and the management responses that might address them, few studies have critically and directly compared competing hypotheses. This study uses qualitative modelling to compare hypotheses relating to outbreak initiation, explicitly considering the potential role of positive feedbacks, elevated nutrients, and removal of starfish predators by fishing. When nutrients and fishing are considered in isolation, the models indicate that a range of alternative hypotheses are capable of explaining outbreak initiation with similar levels of certainty. The models also suggest that outbreaks may be caused by multiple factors operating simultaneously, rather than by single proximal causes. As the complexity and realism of the models increased, the certainty of outcomes decreased, but key areas that require further research to improve the structure of the models were identified. Nutrient additions were likely to result in outbreaks only when COTS larvae alone benefitted from nutrients. Similarly, the effects of fishing on the decline of corals depended on the complexity of interactions among several categories of fishes. Our work suggests that management approaches which seek to be robust to model structure uncertainty should allow for multiple potential causes of outbreaks. Monitoring programs can provide tests of alternative potential causes of outbreaks if they specifically monitor all key taxa at reefs that are exposed to appropriate combinations of potential causal factors.