High response diversity and conspecific density-dependence, not species interactions, drive dynamics of coral reef fish communities.

Species-to-species and species-to-environment interactions are key drivers of community dynamics. Disentangling these drivers in species-rich assemblages is challenging due to the high number of potentially interacting species (the 'curse of dimensionality'). We develop a process-based model that quantifies how intraspecific and interspecific interactions, and species' covarying responses to environmental fluctuations, jointly drive community dynamics. We fit the model to reef fish abundance time series from 41 reefs of Australia's Great Barrier Reef. We found that fluctuating relative abundances are driven by species' heterogenous responses to environmental fluctuations, whereas interspecific interactions are negligible. Species differences in long-term average abundances are driven by interspecific variation in the magnitudes of both conspecific density-dependence and density-independent growth rates. This study introduces a novel approach to overcoming the curse of dimensionality, which reveals highly individualistic dynamics in coral reef fish communities that imply a high level of niche structure.

Protecting Great Barrier Reef resilience through effective management of crown-of-thorns starfish outbreaks.

Resilience-based management is essential to protect ecosystems in the Anthropocene. Unlike large-scale climate threats to Great Barrier Reef (GBR) corals, outbreaks of coral-eating crown-of-thorns starfish (COTS; Acanthaster cf. solaris) can be directly managed through targeted culling. Here, we evaluate the outcomes of a decade of strategic COTS management in suppressing outbreaks and protecting corals during the 4th COTS outbreak wave at reef and regional scales (sectors). We compare COTS density and coral cover dynamics during the 3rd and 4th outbreak waves. During the 4th outbreak wave, sectors that received limited to no culling had sustained COTS outbreaks causing significant coral losses. In contrast, in sectors that received timely and sufficient cull effort, coral cover increased substantially, and outbreaks were suppressed with COTS densities up to six-fold lower than in the 3rd outbreak wave. In the Townsville sector for example, despite exposure to comparable disturbance regimes during the 4th outbreak wave, effective outbreak suppression coincided with relative increases in sector-wide coral cover (44%), versus significant coral cover declines (37%) during the 3rd outbreak wave. Importantly, these estimated increases span entire sectors, not just reefs with active COTS control. Outbreaking reefs with higher levels of culling had net increases in coral cover, while the rate of coral loss was more than halved on reefs with lower levels of cull effort. Our results also indicate that outbreak wave progression to adjoining sectors has been delayed, probably via suppression of COTS larval supply. Our findings provide compelling evidence that proactive, targeted, and sustained COTS management can effectively suppress COTS outbreaks and deliver coral growth and recovery benefits at reef and sector-wide scales. The clear coral protection outcomes demonstrate the value of targeted manual culling as both a scalable intervention to mitigate COTS outbreaks, and a potent resilience-based management tool to "buy time" for coral reefs, protecting reef ecosystem functions and biodiversity as the climate changes.

Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

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.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Fish predators control outbreaks of Crown-of-Thorns Starfish.

Outbreaks of corallivorous Crown-of-Thorns Starfish (CoTS, Acanthaster spp.) have caused persistent and widespread loss of coral cover across Indo-Pacific coral reefs. The potential drivers of these outbreaks have been debated for more than 50 years, hindering effective management to limit their destructive impacts. Here, we show that fish biomass removal through commercial and recreational fisheries may be a major driver of CoTS population outbreaks. CoTS densities increase systematically with increasing fish biomass removal, including for known CoTS predators. Moreover, the biomass of fish species and families that influence CoTS densities are 1.4 to 2.1-fold higher on reefs within no-take marine reserves, while CoTS densities are 2.8-fold higher on reefs that are open to fishing, indicating the applicability of fisheries-based management to prevent CoTS outbreaks. Designing targeted fisheries management with consideration of CoTS population dynamics may offer a tangible and promising contribution to effectively reduce the detrimental impacts of CoTS outbreaks across the Indo-Pacific.

Comparability and complementarity of reef fish measures from underwater visual census (UVC) and baited remote underwater video stations (BRUVS).

The much-publicized threats to coral reef systems necessitate a considered management response based on comprehensive ecological data. However, data from large reef systems commonly originate from multiple monitoring programs that use different methods, each with distinct biases that limit united assessments of ecological status. The effective integration of data from different monitoring methods would allow better assessment of system status and hence, more informed management. Here we examine the scope for comparability and complementarity of fish data from two different methods used on Australia's Great Barrier Reef (GBR): underwater visual census (UVC) and baited remote underwater video stations (BRUVS). We compared commonly reported reef fish measures from UVC and BRUVS on similar reef slope habitats of three central GBR reefs. Both methods recorded similar estimates of total species richness, although ~30% of recorded species were not common to both methods. There were marked differences between methods in sub-group species richness, frequency of species occurrences, relative abundances of taxa and assemblage structure. The magnitude and orientation of inter-method differences were often inconsistent among taxa. However, each method better categorized certain components of fish communities: BRUVS sampled more predatory species in higher numbers while UVC was similarly better at sampling damselfishes (Pomacentridae). Our results suggest limited scope for direct or adjusted comparisons of data from UVC and BRUVS. Conversely, complementary aspects of the two methods confirm that their integration in monitoring programs will provide a more complete and extensive assessment of reef fish status for managers than from either method alone.

Substrate stabilisation and small structures in coral restoration: State of knowledge, and considerations for management and implementation.

Coral reef ecosystems are under increasing pressure from local and regional stressors and a changing climate. Current management focuses on reducing stressors to allow for natural recovery, but in many areas where coral reefs are damaged, natural recovery can be restricted, delayed or interrupted because of unstable, unconsolidated coral fragments, or rubble. Rubble fields are a natural component of coral reefs, but repeated or high-magnitude disturbances can prevent natural cementation and consolidation processes, so that coral recruits fail to survive. A suite of interventions have been used to target this issue globally, such as using mesh to stabilise rubble, removing the rubble to reveal hard substrate and deploying rocks or other hard substrates over the rubble to facilitate recruit survival. Small, modular structures can be used at multiple scales, with or without attached coral fragments, to create structural complexity and settlement surfaces. However, these can introduce foreign materials to the reef, and a limited understanding of natural recovery processes exists for the potential of this type of active intervention to successfully restore local coral reef structure. This review synthesises available knowledge about the ecological role of coral rubble, natural coral recolonisation and recovery rates and the potential benefits and risks associated with active interventions in this rapidly evolving field. Fundamental knowledge gaps include baseline levels of rubble, the structural complexity of reef habitats in space and time, natural rubble consolidation processes and the risks associated with each intervention method. Any restoration intervention needs to be underpinned by risk assessment, and the decision to repair rubble fields must arise from an understanding of when and where unconsolidated substrate and lack of structure impair natural reef recovery and ecological function. Monitoring is necessary to ascertain the success or failure of the intervention and impacts of potential risks, but there is a strong need to specify desired outcomes, the spatial and temporal context and indicators to be measured. With a focus on the Great Barrier Reef, we synthesise the techniques, successes and failures associated with rubble stabilisation and the use of small structures, review monitoring methods and indicators, and provide recommendations to ensure that we learn from past projects.

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.

Counts of coral reef fishes by an experienced observer are not biased by the number of target species.

Fishes are commercially, recreationally and functionally important inhabitants of coral reefs. Accordingly, accurate assessments of fish abundance and diversity are necessary for effective reef management. While some reef fish monitoring programmes target all fishes, many survey a subset of common and visually obvious species. Changing to counts of all species, while desirable, risks new and unwelcome biases from altered observer swimming speeds and search patterns. Here we test whether substantially increasing the number of target species in an established fish monitoring programme biases counts of the original subset, so precluding ongoing comparisons with historical data. A subset of 141 fish species have been visually surveyed along 50 × 5 m transects over 27 years throughout Australia's Great Barrier Reef. We experimentally compared counts of the subset from standard subset-only surveys and from surveys of all species (excluding small site-attached fishes that are surveyed separately) at three diverse reefs. Subset species richness and abundance, in total and of major families, and assemblage structure did not differ due to survey method. The high-level experience of the one observer appeared to overcome new biases from counting more species and the extra 2 min/transect was not logistically excessive. Surveys of all fishes recorded almost 80% more species than subset-only surveys and >130% higher total abundance on average from >150% more genera that included abundant and functionally important taxa. Overall, fish counts by an experienced observer were not biased by the number of species surveyed and counts of all species markedly improved assessments of reef fish diversity and function.

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.

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.

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.

Post-Disturbance Stability of Fish Assemblages Measured at Coarse Taxonomic Resolution Masks Change at Finer Scales.

Quantifying changes to coral reef fish assemblages in the wake of cyclonic disturbances is challenging due to spatial variability of damage inherent in such events. Often, fish abundance appears stable at one spatial scale (e.g. reef-wide), but exhibits substantial change at finer scales (e.g. site-specific decline or increase). Taxonomic resolution also plays a role; overall stability at coarse taxonomic levels (e.g. family) may mask species-level turnover. Here we document changes to reef fish communities after severe Tropical Cyclone Ita crossed Lizard Island, Great Barrier Reef. Coral and reef fish surveys were conducted concurrently before and after the cyclone at four levels of exposure to the prevailing weather. Coral cover declined across all exposures except sheltered sites, with the largest decline at exposed sites. There was no significant overall reduction in the total density, biomass and species richness of reef fishes between 2011 and 2015, but individual fish taxa (families and species) changed in complex and unpredictable ways. For example, more families increased in density and biomass than decreased following Cyclone Ita, particularly at exposed sites whilst more fish families declined at lagoon sites even though coral cover did not decline. All sites lost biomass of several damselfish species, and at most sites there was an increase in macroinvertivores and grazers. Overall, these results suggest that the degree of change measured at coarse taxonomic levels masked high species-level turnover, although other potential explanations include that there was no impact of the storm, fish assemblages were impacted but underwent rapid recovery or that there is a time lag before the full impacts become apparent. This study confirms that in high-complexity, high diversity ecosystems such as coral reefs, species level analyses are essential to adequately capture the consequences of disturbance events.

Marine protected areas increase resilience among coral reef communities.

With marine biodiversity declining globally at accelerating rates, maximising the effectiveness of conservation has become a key goal for local, national and international regulators. Marine protected areas (MPAs) have been widely advocated for conserving and managing marine biodiversity yet, despite extensive research, their benefits for conserving non-target species and wider ecosystem functions remain unclear. Here, we demonstrate that MPAs can increase the resilience of coral reef communities to natural disturbances, including coral bleaching, coral diseases, Acanthaster planci outbreaks and storms. Using a 20-year time series from Australia's Great Barrier Reef, we show that within MPAs, (1) reef community composition was 21-38% more stable; (2) the magnitude of disturbance impacts was 30% lower and (3) subsequent recovery was 20% faster that in adjacent unprotected habitats. Our results demonstrate that MPAs can increase the resilience of marine communities to natural disturbance possibly through herbivory, trophic cascades and portfolio effects.

Expectations and Outcomes of Reserve Network Performance following Re-zoning of the Great Barrier Reef Marine Park.

Networks of no-take marine reserves (NTMRs) are widely advocated for preserving exploited fish stocks and for conserving biodiversity. We used underwater visual surveys of coral reef fish and benthic communities to quantify the short- to medium-term (5 to 30 years) ecological effects of the establishment of NTMRs within the Great Barrier Reef Marine Park (GBRMP). The density, mean length, and biomass of principal fishery species, coral trout (Plectropomus spp., Variola spp.), were consistently greater in NTMRs than on fished reefs over both the short and medium term. However, there were no clear or consistent differences in the structure of fish or benthic assemblages, non-target fish density, fish species richness, or coral cover between NTMR and fished reefs. There was no indication that the displacement and concentration of fishing effort reduced coral trout populations on fished reefs. A severe tropical cyclone impacted many survey reefs during the study, causing similar declines in coral cover and fish density on both NTMR and fished reefs. However, coral trout biomass declined only on fished reefs after the cyclone. The GBRMP is performing as expected in terms of the protection of fished stocks and biodiversity for a developed country in which fishing is not excessive and targets a narrow range of species. NTMRs cannot protect coral reefs directly from acute regional-scale disturbance but, after a strong tropical cyclone, impacted NTMR reefs supported higher biomass of key fishery-targeted species and so should provide valuable sources of larvae to enhance population recovery and long-term persistence.

Retention of habitat complexity minimizes disassembly of reef fish communities following disturbance: a large-scale natural experiment.

High biodiversity ecosystems are commonly associated with complex habitats. Coral reefs are highly diverse ecosystems, but are under increasing pressure from numerous stressors, many of which reduce live coral cover and habitat complexity with concomitant effects on other organisms such as reef fishes. While previous studies have highlighted the importance of habitat complexity in structuring reef fish communities, they employed gradient or meta-analyses which lacked a controlled experimental design over broad spatial scales to explicitly separate the influence of live coral cover from overall habitat complexity. Here a natural experiment using a long term (20 year), spatially extensive (∼ 115,000 kms(2)) dataset from the Great Barrier Reef revealed the fundamental importance of overall habitat complexity for reef fishes. Reductions of both live coral cover and habitat complexity had substantial impacts on fish communities compared to relatively minor impacts after major reductions in coral cover but not habitat complexity. Where habitat complexity was substantially reduced, species abundances broadly declined and a far greater number of fish species were locally extirpated, including economically important fishes. This resulted in decreased species richness and a loss of diversity within functional groups. Our results suggest that the retention of habitat complexity following disturbances can ameliorate the impacts of coral declines on reef fishes, so preserving their capacity to perform important functional roles essential to reef resilience. These results add to a growing body of evidence about the importance of habitat complexity for reef fishes, and represent the first large-scale examination of this question on the Great Barrier Reef.

Ongoing effects of no-take marine reserves on commercially exploited coral trout populations on the Great Barrier Reef.

Networks of no-take marine reserves (NTMRs) are widely used for managing marine resources. Because they restrict fishing, managers need to monitor reserves to reassure stakeholders that they are achieving the intended results. In 2004, the Great Barrier Reef (GBR) Marine Park was rezoned and the area of NTMRs was greatly increased. Using manta tow we assessed the effectiveness of the new NTMRs in conserving coral trout (Plectropomus and Variola spp.), the principle targets of the GBR reef line fishery. Over a six year period, we sampled regional groups of matched pairs of similar reefs, ones closed to fishing under the rezoning and ones that remained open. Coral trout populations were significantly higher in NTMRs. While coral trout populations declined on reefs open to fishing, stocks were maintained in NTMRs, highlighting the ongoing benefits of marine reserves.

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).