Consumers decrease variability across space and turnover through time during coral reef succession.

Consumers play an integral role in mediating ecological succession-the change in community composition over time. As consumer populations are facing rapid decline in ecosystems around the world, understanding of their ecological role is becoming increasingly urgent. Increased understanding of how changes in consumer populations may influence community variability across space and turnover through time during succession is particularly important for coral reefs, which are among the most threatened ecosystems globally, and where fishes play vital roles in structuring benthic succession. Here, we examine how consumers influence coral reef succession by deploying 180 paired settlement tiles, caged (to exclude fishes larger than approximately 15 cm) and uncaged, within Palmyra Atoll, a remote marine wildlife refuge with previously documented high fish abundance, and monitored benthic community development one and three years after deployment. We found that excluding large fishes lead to lower alpha diversity and divergent community states across space (i.e.,, high beta diversity among caged tiles), suggesting that benthic fish feeding maintains local diversity but tends to homogenize community composition with dominance by crustose coralline algae. In addition, when fish were experimentally excluded, the developing benthic community exhibited a greater change in species composition over time (i.e., high temporal beta diversity), indicating that fish feeding tends to canalize community successional trajectories. Finally, the caged and uncaged tiles became more similar over time, suggesting that fish feeding plays a more important role during early succession. Our results demonstrate that the loss of large fishes, for example from overfishing, may result in benthic communities that are more variable across space and time. Increased variability could have important implications for ecosystem function and coral reef resilience in the face of escalating global stressors.

Coupled beta diversity patterns among coral reef benthic taxa.

Unraveling the processes that drive diversity patterns remains a central challenge for ecology, and an increased understanding is especially urgent to address and mitigate escalating diversity loss. Studies have primarily focused on singular taxonomic groups, but recent research has begun evaluating spatial diversity patterns across multiple taxonomic groups and suggests taxa may have congruence in their diversity patterns. Here, we use surveys of the coral reef benthic groups: scleractinian corals, macroalgae, sponges and gorgonians conducted in the Bahamian Archipelago across 27 sites to determine if there is congruence between taxonomic groups in their site-level diversity patterns (i.e. alpha diversity: number of species, and beta diversity: differences in species composition) while accounting for environmental predictors (i.e. depth, wave exposure, market gravity (i.e. human population size and distance to market), primary productivity, and grazing). Overall, we found that the beta diversities of these benthic groups were significant predictors of each other. The most consistent relationships existed with algae and coral, as their beta diversity was a significant predictor of every other taxa's beta diversity, potentially due to their strong biotic interactions and dominance on the reef. Conversely, we found no congruence patterns in the alpha diversity of the taxa. Market gravity and exposure showed the most prevalent correlation with both alpha and beta diversity for the taxa. Overall, our results suggest that coral reef benthic taxa can have spatial congruence in species composition, but not number of species, and that future research on biodiversity trends should consider that taxa may have non-independent patterns.

An index to assess the health and benefits of the global ocean.

The ocean plays a critical role in supporting human well-being, from providing food, livelihoods and recreational opportunities to regulating the global climate. Sustainable management aimed at maintaining the flow of a broad range of benefits from the ocean requires a comprehensive and quantitative method to measure and monitor the health of coupled human­ocean systems. We created an index comprising ten diverse public goals for a healthy coupled human­ocean system and calculated the index for every coastal country. Globally, the overall index score was 60 out of 100 (range 36­86), with developed countries generally performing better than developing countries, but with notable exceptions. Only 5% of countries scored higher than 70, whereas 32% scored lower than 50. The index provides a powerful tool to raise public awareness, direct resource management, improve policy and prioritize scientific research.

Dynamic interplay: disentangling the temporal variability of fish effects on coral recruitment.

Ecosystems around the world are continuously undergoing recovery from anthropogenic disturbances like climate change, overexploitation, and habitat destruction. Coral reefs are a prime example of a threatened ecosystem and coral recruitment is a critical component of reef recovery from disturbances. Reef fishes structure this recruitment by directly consuming macroalgae and coral recruits or by indirectly altering the substrate to facilitate coral settlement (e.g., grazing scars). However, how these direct and indirect mechanisms vary through time remains largely unknown. Here, we quantified coral recruitment on settlement tiles with divots that mimic grazing scars and caging treatments to exclude or allow fish feeding over 3 years at Palmyra Atoll in the Pacific Ocean. We found that the positive and negative effects of fishes on coral recruitment varies through time. After 3 years, both grazing scars and fish grazing no longer predicted coral recruitment, suggesting that the role of fishes decreases over time. Our results emphasize that reef fish populations are important in promoting initial coral recovery after disturbances. However, over time, factors like the environment may become more important. Future work should continue to explore how the strength and direction of top-down control by consumers varies through time across multiple ecosystems.

Tropical coastal habitats as surrogates of fish community structure, grazing, and fisheries value.

Habitat maps are frequently invoked as surrogates of biodiversity to aid the design of networks of marine reserves. Maps are used to maximize habitat heterogeneity in reserves because this is likely to maximize the number of species protected. However, the technique's efficacy is limited by intra-habitat variability in the species present and their abundances. Although communities are expected to vary among patches of the same habitat, this variability is poorly documented and rarely incorporated into reserve planning. To examine intra-habitat variability in coral-reef fishes, we generated a data set from eight tropical coastal habitats and six islands in the Bahamian archipelago using underwater visual censuses. Firstly, we provide further support for habitat heterogeneity as a surrogate of biodiversity as each predefined habitat type supported a distinct assemblage of fishes. Intra-habitat variability in fish community structure at scales of hundreds of kilometers (among islands) was significant in at least 75% of the habitats studied, depending on whether presence/absence, density, or biomass data were used. Intra-habitat variability was positively correlated with the mean number of species in that habitat when density and biomass data were used. Such relationships provide a proxy for the assessment of intra-habitat variability when detailed quantitative data are scarce. Intra-habitat variability was examined in more detail for one habitat (forereefs visually dominated by Montastraea corals). Variability in community structure among islands was driven by small, demersal families (e.g., territorial pomacentrid and labrid fishes). Finally, we examined the ecological and economic significance of intra-habitat variability in fish assemblages on Montastraea reefs by identifying how this variability affects the composition and abundances of fishes in different functional groups, the key ecosystem process of parrotfish grazing, and the ecosystem service of value of commercially important finfish. There were significant differences in a range of functional groups and grazing, but not fisheries value. Variability at the scale of tens of kilometers (among reefs around an island) was less than that among islands. Caribbean marine reserves should be replicated at scales of hundreds of kilometers, particularly for species-rich habitats, to capture important intra-habitat variability in community structure, function, and an ecosystem process.

Coral reef habitats as surrogates of species, ecological functions, and ecosystem services.

Habitat maps are often the core spatially consistent data set on which marine reserve networks are designed, but their efficacy as surrogates for species richness and applicability to other conservation measures is poorly understood. Combining an analysis of field survey data, literature review, and expert assessment by a multidisciplinary working group, we examined the degree to which Caribbean coastal habitats provide useful planning information on 4 conservation measures: species richness, the ecological functions of fish species, ecosystem processes, and ecosystem services. Approximately one-quarter to one-third of benthic invertebrate species and fish species (disaggregated by life phase; hereafter fish species) occurred in a single habitat, and Montastraea-dominated forereefs consistently had the highest richness of all species, processes, and services. All 11 habitats were needed to represent all 277 fish species in the seascape, although reducing the conservation target to 95% of species approximately halved the number of habitats required to ensure representation. Species accumulation indices (SAIs) were used to compare the efficacy of surrogates and revealed that fish species were a more appropriate surrogate of benthic species (SAI = 71%) than benthic species were for fishes (SAI = 42%). Species of reef fishes were also distributed more widely across the seascape than invertebrates and therefore their use as a surrogate simultaneously included mangroves, sea grass, and coral reef habitats. Functional classes of fishes served as effective surrogates of fish and benthic species which, given their ease to survey, makes them a particularly useful measure for conservation planning. Ecosystem processes and services exhibited great redundancy among habitats and were ineffective as surrogates of species. Therefore, processes and services in this case were generally unsuitable for a complementarity-based approach to reserve design. In contrast, the representation of species or functional classes ensured inclusion of all processes and services in the reserve network.

The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes.

Caribbean coral reef habitats, seagrass beds and mangroves provide important goods and services both individually and through functional linkages. A range of anthropogenic factors are threatening the ecological and economic importance of these habitats and it is vital to understand how ecosystem processes vary across seascapes. A greater understanding of processes will facilitate further insight into the effects of disturbances and assist with assessing management options. Despite the need to study processes across whole seascapes, few spatially explicit ecosystem-scale assessments exist. We review the empirical literature to examine the role of different habitat types for a range of processes. The importance of each of 10 generic habitats to each process is defined as its "functional value" (none, low, medium or high), quantitatively derived from published data wherever possible and summarised in a single figure. This summary represents the first time the importance of habitats across an entire Caribbean seascape has been assessed for a range of processes. Furthermore, we review the susceptibility of each habitat to disturbances to investigate spatial patterns that might affect functional values. Habitat types are considered at the scale discriminated by remotely-sensed imagery and we envisage that functional values can be combined with habitat maps to provide spatially explicit information on processes across ecosystems. We provide examples of mapping the functional values of habitats for populations of three commercially important species. The resulting data layers were then used to generate seascape-scale assessments of "hot spots" of functional value that might be considered priorities for conservation. We also provide an example of how the literature reviewed here can be used to parameterise a habitat-specific model investigating reef resilience under different scenarios of herbivory. Finally, we use multidimensional scaling to provide a basic analysis of the overall functional roles of different habitats. The resulting ordination suggests that each habitat has a unique suite of functional values and, potentially, a distinct role within the ecosystem. This review shows that further data are required for many habitat types and processes, particularly forereef and escarpment habitats on reefs and for seagrass beds and mangroves. Furthermore, many data were collected prior to the regional mass mortality of Diadema and Acropora, and subsequent changes to benthic communities have, in many cases, altered a habitat's functional value, hindering the use of these data for parameterising maps and models. Similarly, few data exist on how functional values change when environmental parameters, such as water clarity, are altered by natural or anthropogenic influences or the effects of a habitat's spatial context within the seascape. Despite these limitations, sufficient data are available to construct maps and models to better understand tropical marine ecosystem processes and assist more effective mitigation of threats that alter habitats and their functional values.

Grouper as a natural biocontrol of invasive lionfish.

Lionfish (Pterois volitans/miles) have invaded the majority of the Caribbean region within five years. As voracious predators of native fishes with a broad habitat distribution, lionfish are poised to cause an unprecedented disruption to coral reef diversity and function. Controls of lionfish densities within its native range are poorly understood, but they have been recorded in the stomachs of large-bodied Caribbean groupers. Whether grouper predation of lionfish is sufficient to act as a biocontrol of the invasive species is unknown, but pest biocontrol by predatory fishes has been reported in other ecosystems. Groupers were surveyed along a chain of Bahamian reefs, including one of the region's most successful marine reserves which supports the top one percentile of Caribbean grouper biomass. Lionfish biomass exhibited a 7-fold and non-linear reduction in relation to the biomass of grouper. While Caribbean grouper appear to be a biocontrol of invasive lionfish, the overexploitation of their populations by fishers, means that their median biomass on Caribbean reefs is an order of magnitude less than in our study. Thus, chronic overfishing will probably prevent natural biocontrol of lionfishes in the Caribbean.

Acute effects of removing large fish from a near-pristine coral reef.

Large animals are severely depleted in many ecosystems, yet we are only beginning to understand the ecological implications of their loss. To empirically measure the short-term effects of removing large animals from an ocean ecosystem, we used exclosures to remove large fish from a near-pristine coral reef at Palmyra Atoll, Central Pacific Ocean. We identified a range of effects that followed from the removal of these large fish. These effects were revealed within weeks of their removal. Removing large fish (1) altered the behavior of prey fish; (2) reduced rates of herbivory on certain species of reef algae; (3) had both direct positive (reduced mortality of coral recruits) and indirect negative (through reduced grazing pressure on competitive algae) impacts on recruiting corals; and (4) tended to decrease abundances of small mobile benthic invertebrates. Results of this kind help advance our understanding of the ecological importance of large animals in ecosystems.

Trophic cascade facilitates coral recruitment in a marine reserve.

Reduced fishing pressure and weak predator-prey interactions within marine reserves can create trophic cascades that increase the number of grazing fishes and reduce the coverage of macroalgae on coral reefs. Here, we show that the impacts of reserves extend beyond trophic cascades and enhance the process of coral recruitment. Increased fish grazing, primarily driven by reduced fishing, was strongly negatively correlated with macroalgal cover and resulted in a 2-fold increase in the density of coral recruits within a Bahamian reef system. Our conclusions are robust because four alternative hypotheses that may generate a spurious correlation between grazing and coral recruitment were tested and rejected. Grazing appears to influence the density and community structure of coral recruits, but no detectable influence was found on the overall size-frequency distribution, community structure, or cover of corals. We interpret this absence of pattern in the adult coral community as symptomatic of the impact of a recent disturbance event that masks the recovery trajectories of individual reefs. Marine reserves are not a panacea for conservation but can facilitate the recovery of corals from disturbance and may help sustain the biodiversity of organisms that depend on a complex three-dimensional coral habitat.

Fishing, trophic cascades, and the process of grazing on coral reefs.

Since the mass mortality of the urchin Diadema antillarum in 1983, parrotfishes have become the dominant grazer on Caribbean reefs. The grazing capacity of these fishes could be impaired if marine reserves achieve their long-term goal of restoring large consumers, several of which prey on parrotfishes. Here we compare the negative impacts of enhanced predation with the positive impacts of reduced fishing mortality on parrotfishes inside reserves. Because large-bodied parrotfishes escape the risk of predation from a large piscivore (the Nassau grouper), the predation effect reduced grazing by only 4 to 8%. This impact was overwhelmed by the increase in density of large parrotfishes, resulting in a net doubling of grazing. Increased grazing caused a fourfold reduction in the cover of macroalgae, which, because they are the principal competitors of corals, highlights the potential importance of reserves for coral reef resilience.