Prioritizing Key Resilience Indicators to Support Coral Reef Management in a Changing Climate

Managing coral reefs for resilience to climate change is a popular concept but has been difficult to implement because the empirical scientific evidence has either not been evaluated or is sometimes unsupportive of theory, which leads to uncertainty when considering methods and identifying priority reefs. We asked experts and reviewed the scientific literature for guidance on the multiple physical and biological factors that affect the ability of coral reefs to resist and recover from climate disturbance. Eleven key factors to inform decisions based on scaling scientific evidence and the achievability of quantifying the factors were identified. Factors important to resistance and recovery, which are important components of resilience, were not strongly related, and should be assessed independently. The abundance of resistant (heat-tolerant) coral species and past temperature variability were perceived to provide the greatest resistance to climate change, while coral recruitment rates, and macroalgae abundance were most influential in the recovery process. Based on the 11 key factors, we tested an evidence-based framework for climate change resilience in an Indonesian marine protected area. The results suggest our evidence-weighted framework improved upon existing un-weighted methods in terms of characterizing resilience and distinguishing priority sites. The evaluation supports the concept that, despite high ecological complexity, relatively few strong variables can be important in influencing ecosystem dynamics. This is the first rigorous assessment of factors promoting coral reef resilience based on their perceived importance, empirical evidence, and feasibility of measurement. There were few differences between scientists\u27 perceptions of factor importance and the scientific evidence found in journal publications but more before and after impact studies will be required to fully test the validity of all the factors. The methods here will increase the feasibility and defensibility of including key resilience metrics in evaluations of coral reefs, as well as reduce costs. Adaptation, marine protected areas, priority setting, resistance, recovery

Age and growth of an outbreaking Acanthaster cf. solaris population within the Great Barrier Reef

Despite having been studied for more than 40 years, much about the basic life history of crown-of-thorns starfish (CoTS; Acanthaster spp.) remains poorly understood. Size at age-a key metric of productivity for any animal population-has yet to be clearly defined, primarily due to difficulties in obtaining validated ages and potentially indeterminate growth due to factors such as starvation; within-population variability is entirely unknown. Here we develop age and growth estimates for an outbreaking CoTS population in Australian waters by integrating prior information with data from CoTS collected from multiple outbreaking reefs. Age estimates were made from un-validated band counts of 2038 individual starfish. Results from our three-parameter von Bertalanffy Bayesian hierarchical model show that, under 2013-2014 outbreak conditions, CoTS on the GBR grew to a 349 ( 326, 380) mm (posterior median (95% uncertainty interval)) total diameter at a 0.54 (0.43, 0.66) intrinsic rate of increase. However, we also found substantial evidence (Delta DIC > 200) for inter-reef variability in both maximum size (SD 38 (19, 76)) and intrinsic rate of increase (SD 0.32 (0.20, 0.49)) within the CoTS outbreak initiation area. These results suggest that CoTS demography can vary widely with reef-scale environmental conditions, supporting location-based mechanisms for CoTS outbreaks generally. These findings should help improve population and metapopulation models of CoTS dynamics and better predict the potential damage they may cause in the future

Visual versus video methods for estimating reef fish biomass

Estimates of fish biomass collated at the community level are reliable indicators of fish and ecosystem health. Data to calculate fish biomass is routinely collected using either underwater visual census (UVC) or stereo diver operated video (DOV), although the compatibility of UVC and DOV based estimates are yet to be assessed. Accordingly, we calculated and compared community level measures of coral reef fish biomass at Ningaloo reef (Western Australia) using both UVC and DOV. The UVC based biomass estimates were 788 kg/Ha, which was ∼50% greater than those from DOV (500 kg/Ha). Differences between the methods were primarily due to DOV measuring the length of only ∼40% of fish detected by video, preventing fish specific weight calculations for all fish encountered. When the size of unmeasured fish was assumed to be the median value of fish measured by DOV, revised DOV+ estimates of community biomass (778 kg/Ha) were similar to those from UVC. However, even when unmeasured fish were included in DOV calculations, biomass of some families (serranids) were still higher when using UVC. Conversely, DOV adjusted estimates of pomacentrid biomass were higher than those from UVC, due to DOV measuring fewer small bodied fish (<3 cm), thus having a larger median size for the high number of unmeasured pomacentrids compared to UVC. Our results suggest that community measures of fish biomass from DOV and UVC are broadly comparable once weights of unmeasured fish are incorporated into DOV estimates. This may increase the spatial and temporal scales at which fish biomass can be monitored, although compatibility of data will depend on the composition and size distribution of the fish assemblages

Ecosystem regime shifts disrupt trophic structure

Regime shifts between alternative stable ecosystem states are becoming commonplace due to the combined effects of local stressors and global climate change. Alternative states are characterised as substantially different in form and function to pre-disturbance states, disrupting the delivery of ecosystem services and functions. On coral reefs, regime shifts are typically characterised by a change in the benthic composition from coral- to macroalgal-dominance. Such fundamental shifts in the benthos are anticipated to impact associated fish communities that are reliant on the reef for food and shelter, yet there is limited understanding of how regime shifts propagate through the fish community over time, relative to initial or recovery conditions. This study addresses this knowledge gap using long-term data of coral reef regime shifts and recovery on Seychelles reefs following the 1998 mass bleaching event. It shows how trophic structure of the reef fish community becomes increasingly dissimilar between alternative reef ecosystem states (regime-shifted vs recovering) with time since disturbance. Regime-shifted reefs developed a concave trophic structure, with increased biomass in base trophic levels as herbivorous species benefitted from increased algal resources. Mid trophic level species, including specialists such as corallivores, declined with loss of coral habitat, while biomass was retained in upper trophic levels by large-bodied, generalist invertivores. Recovering reefs also experienced an initial decline in mid trophic level biomass, but moved towards a bottom-heavy pyramid shape, with a wide range of feeding groups (e.g. planktivores, corallivores, omnivores) represented at mid trophic levels. Given the importance of coral reef fishes in maintaining the ecological function of coral reef ecosystems and their associated fisheries, understanding the effects of regime shifts on these communities is essential to inform decisions that enhance ecological resilience and economic sustainability

Mesopredator trophodynamics on thermally stressed coral reefs

Ecosystems are becoming vastly modified through disturbance. In coral reef ecosystems, the differential susceptibility of coral taxa to climate-driven bleaching is predicted to shift coral assemblages towards reefs with an increased relative abundance of taxa with high thermal tolerance. Many thermally tolerant coral species are characterised by low structural complexity, with reduced habitat niche space for the small-bodied coral reef fishes on which piscivorous mesopredators feed. This study used a patch reef array to investigate the potential impacts of climate-driven shifts in coral assemblages on the trophodynamics of reef mesopredators and their prey communities. The ‘tolerant’ reef treatment consisted only of coral taxa of low susceptibility to bleaching, while ‘vulnerable’ reefs included species of moderate to high thermal vulnerability. ‘Vulnerable’ reefs had higher structural complexity, and the fish assemblages that established on these reefs over 18 months had higher species diversity, abundance and biomass than those on ‘tolerant’ reefs. Fish assemblages on ‘tolerant’ reefs were also more strongly influenced by the introduction of a mesopredator (Cephalopholis boenak). Mesopredators on ‘tolerant’ reefs had lower lipid content in their muscle tissue by the end of the 6-week experiment. Such sublethal energetic costs can compromise growth, fecundity, and survivorship, resulting in unexpected population declines in long-lived mesopredators. This study provides valuable insight into the altered trophodynamics of future coral reef ecosystems, highlighting the potentially increased vulnerability of reef fish assemblages to predation as reef structure declines, and the cost of changing prey availability on mesopredator condition

Joint estimation of crown of thorns (Acanthaster planci) densities on the Great Barrier Reef

Crown-of-thorns starfish (CoTS; Acanthaster spp.) are an outbreaking pest among many Indo-Pacific coral reefs that cause substantial ecological and economic damage. Despite ongoing CoTS research, there remain critical gaps in observing CoTS populations and accurately estimating their numbers, greatly limiting understanding of the causes and sources of CoTS outbreaks. Here we address two of these gaps by (1) estimating the detectability of adult CoTS on typical underwater visual count (UVC) surveys using covariates and (2) inter-calibrating multiple data sources to estimate CoTS densities within the Cairns sector of the Great Barrier Reef (GBR). We find that, on average, CoTS detectability is high at 0.82 [0.77, 0.87] (median highest posterior density (HPD) and [95% uncertainty intervals]), with CoTS disc width having the greatest influence on detection. Integrating this information with coincident surveys from alternative sampling programs, we estimate CoTS densities in the Cairns sector of the GBR averaged 44 [41, 48] adults per hectare in 2014

Human disruption of coral reef trophic structure

The distribution of biomass among trophic levels provides a theoretical basis for understanding energy flow and the hierarchical structure of animal communities. In the absence of energy subsidies [1], bottom-heavy trophic pyramids are expected to predominate, based on energy transfer efficiency [2] and empirical evidence from multiple ecosystems [3]. However, the predicted pyramid of biomass distribution among trophic levels may be disrupted through trophic replacement by alternative organisms in the ecosystem, trophic cascades, and humans preferentially impacting specific trophic levels [4, 5 and 6]. Using empirical data spanning >250 coral reefs, we show how trophic pyramid shape varies given human-mediated gradients along two orders of magnitude in reef fish biomass. Mean trophic level of the assemblage increased modestly with decreasing biomass, contrary to predictions of fishing down the food web [7]. The mean trophic level pattern is explained by trophic replacement of herbivorous fish by sea urchins at low biomass and the accumulation of slow-growing, large-bodied, herbivorous fish at high biomass. Further, at high biomass, particularly where fishers are not selectively removing higher trophic level individuals, a concave trophic distribution emerges. The concave trophic distribution implies a more direct link between lower and upper trophic levels, which may confer greater energy efficiency. This trophic distribution emerges when community biomass exceeds ∼650 kg/ha, suggesting that fisheries for upper trophic level species will only be supported under lightly fished scenarios

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change

Moray eels are more common on coral reefs subject to higher human pressure in the greater Caribbean

Proximity and size of the nearest market (‘market gravity’) have been shown to have strong negative effects on coral reef fish communities that can be mitigated by the establishment of closed areas. However, moray eels are functionally unique predators that are generally not subject to targeted fishing and should therefore not directly be affected by these factors. We used baited remote underwater video systems to investigate associations between morays and anthropogenic, habitat, and ecological factors in the Caribbean region. Market gravity had a positive effect on morays, while the opposite pattern was observed in a predator group subject to exploitation (sharks). Environmental DNA analyses corroborated the positive effect of market gravity on morays. We hypothesize that the observed pattern could be the indirect result of the depletion of moray competitors and predators near humans. Environmental science; ecology; biological sciences; zoology; animals; etholog

Rights and representation support justice across aquatic food systems

Injustices are prevalent in food systems, where the accumulation of vast wealth is possible for a few, yet one in ten people remain hungry. Here, for 194 countries we combine aquatic food production, distribution and consumption data with corresponding national policy documents and, drawing on theories of social justice, explore whether barriers to participation explain unequal distributions of benefits. Using Bayesian models, we find economic and political barriers are associated with lower wealth-based benefits; countries produce and consume less when wealth, formal education and voice and accountability are lacking. In contrast, social barriers are associated with lower welfare-based benefits; aquatic foods are less affordable where gender inequality is greater. Our analyses of policy documents reveal a frequent failure to address political and gender-based barriers. However, policies linked to more just food system outcomes centre principles of human rights, specify inclusive decision-making processes and identify and challenge drivers of injustice