Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs.

Around the globe, coral reefs and other marine ecosystems are increasingly overfished. Conventionally, studies of fishing impacts have focused on the population size and dynamics of targeted stocks rather than the broader ecosystem-wide effects of harvesting. Using parrotfishes as an example, we show how coral reef fish populations respond to escalating fishing pressure across the Indian and Pacific Oceans. Based on these fish abundance data, we infer the potential impact on four key functional roles performed by parrotfishes. Rates of bioerosion and coral predation are highly sensitive to human activity, whereas grazing and sediment removal are resilient to fishing. Our results offer new insights into the vulnerability and resilience of coral reefs to the ever-growing human footprint. The depletion of fishes causes differential decline of key ecosystem functions, radically changing the dynamics of coral reefs and setting the stage for future ecological surprises.

Coral reef diversity refutes the neutral theory of biodiversity.

The global decline of coral reefs highlights the need to understand the mechanisms that regulate community structure and sustain biodiversity in these systems. The neutral theory, which assumes that individuals are demographically identical regardless of species, seeks to explain ubiquitous features of community structure and biodiversity patterns. Here we present a test of neutral-theory predictions with the use of an extensive species-level data set of Indo-Pacific coral communities. We show that coral assemblages differ markedly from neutral-model predictions for patterns of community similarity and the relative abundance of species. Within local communities, neutral models do not fit relative abundance distributions as well as the classical log-normal distribution. Relative abundances of species across local communities also differ markedly from neutral-theory predictions: coral communities exhibit community similarity values that are far more variable, and lower on average, than the neutral theory can produce. Empirical community similarities deviate from the neutral model in a direction opposite to that predicted in previous critiques of the neutral theory. Instead, our results support spatio-temporal environmental stochasticity as a major driver of diversity patterns on coral reefs.

Spatial variance in abundance and occupancy of corals across broad geographic scales.

Species assemblages vary in structure due to a wide variety of processes operating at ecological and much broader biogeographical scales. Cross-scale studies of assemblage structure are necessary to fully understand this variability. Here, we evaluate the abundance and occupancy patterns of hierarchically sampled coral assemblages in three habitats (reef flat, crest, and slope) and five regions (Indonesia, Papua New Guinea, the Solomon Islands, American Samoa, and the Society Islands) across the west-central Pacific Ocean. Specifically, we compare two alternative models that unify spatial variance and occupancy via the negative binomial distribution. The first assumes a power-law scaling between the mean and variance of abundance; the second assumes a quadratic variance-mean relationship and a constant abundance-invariant aggregation parameter. Surprisingly, the well-established power-law model performs worse than the model assuming abundance-invariant aggregation, for both variance-mean and occupancy-abundance relationships. We also find strong evidence for regional and habitat variation in these relationships and in the levels of aggregation estimated by the abundance-invariant aggregation model. Among habitats, corals on reef flats exhibited lower occupancy and higher levels of aggregation compared to reef crests and slopes. Among regions, low occupancy and high aggregation were most pronounced across all habitats in American Samoa. These patterns may be related to habitat and regional differences in disturbance and recovery processes. Our results suggest that the spatial scaling of abundance and occupancy is sensitive to processes operating among these habitats and at regional scales. However, the consistency of these relationships across species within assemblages suggests that a theoretical unification of spatial variance and occupancy patterns is indeed possible.

Phase shifts, herbivory, and the resilience of coral reefs to climate change.

Many coral reefs worldwide have undergone phase shifts to alternate, degraded assemblages because of the combined effects of over-fishing, declining water quality, and the direct and indirect impacts of climate change. Here, we experimentally manipulated the density of large herbivorous fishes to test their influence on the resilience of coral assemblages in the aftermath of regional-scale bleaching in 1998, the largest coral mortality event recorded to date. The experiment was undertaken on the Great Barrier Reef, within a no-fishing reserve where coral abundances and diversity had been sharply reduced by bleaching. In control areas, where fishes were abundant, algal abundance remained low, whereas coral cover almost doubled (to 20%) over a 3 year period, primarily because of recruitment of species that had been locally extirpated by bleaching. In contrast, exclusion of large herbivorous fishes caused a dramatic explosion of macroalgae, which suppressed the fecundity, recruitment, and survival of corals. Consequently, management of fish stocks is a key component in preventing phase shifts and managing reef resilience. Importantly, local stewardship of fishing effort is a tractable goal for conservation of reefs, and this local action can also provide some insurance against larger-scale disturbances such as mass bleaching, which are impractical to manage directly.

Coral communities are regionally enriched along an oceanic biodiversity gradient.

Ecological communities are influenced by processes operating at multiple scales. Thus, a better understanding of how broad- as well as local-scale processes affect species diversity and richness is increasingly becoming a central focus in modern community ecology. Here, in a study of unprecedented geographical scope, we show significant regional and local variation in the species richness of coral assemblages across an oceanic biodiversity gradient. The gradient that we sampled extends 10,000 km eastwards from the world's richest coral biodiversity hotspot in the central Indo-Pacific. Local richness and the size of regional species pools decline significantly across 15 islands spanning the gradient. In addition, richness declines across three adjacent habitats (reef slopes, crests and flats). In each habitat, a highly consistent linear relationship between local and regional species richness indicates strong regional enrichment. Thus, even on the most diverse coral reefs in the world, local coral assemblages are profoundly affected by regional-scale processes. Understanding these historical and biogeographical influences is essential for the effective management and preservation of these endangered communities.

Community-level density dependence: an example from a shallow coral assemblage.

While density dependence is a popular topic of research in population ecology, it has received much less attention at the community level. Using 27 years of data from Heron Island, on Australia's Great Barrier Reef, we develop a matrix model of coral community dynamics that shows that community-level density dependence does occur and that it is fairly common, being found in 38% of the model parameters for which it was tested. In particular, colonization of free space (through either recruitment or growth of existing colonies) was nearly always density dependent. There were no consistent patterns in the results for mortality, persistence, or species interactions. Most transitions were found to be dependent on the cover of the incoming species group, with only a few dependent on that of the outgoing species group. In addition, few of the transitions representing species interactions were dependent on the amount of free space present, suggesting that the cover of other species does not influence encounters. When these results were combined into a model of community dynamics, it was found that density dependence resulted in a moderate increase in coral cover, which was spread over most species groups. The dynamics of the density-dependent assemblage were also a lot noisier than those of an assemblage without density dependence. Sensitivity analysis indicated that it was density dependence in the colonization probabilities, particularly of encrusting acroporids, bushy Acropora and staghorn Acropora, which had the main influence on the model, although persistence of free space was also important. Transitions representing mortality were only of minor importance, and those representing species interactions were of no importance.

Testing species abundance models: a new bootstrap approach applied to Indo-Pacific coral reefs.

Patterns in the commonness and rarity of species are a fundamental characteristic of ecological assemblages; however, testing between alternative models for such patterns remains an important challenge. Conventional approaches to fitting or testing species abundance models often assume that species, not individuals, are the units that are sampled and that species' abundances are independent of one another. Here we test three different models (the Poisson lognormal, the negative binomial, and the neutral, "zero-sum multinomial" [ZSM]) against species abundance distributions of Indo-Pacific corals and reef fishes. We derive and apply several alternative bootstrap analyses of model fit, each of which makes different assumptions about how species abundance data are sampled, and we assess the extent to which tests of model fit are sensitive to such assumptions. For all models, goodness of fit is remarkably consistent, regardless of whether one assumes that species or individuals are the units that are sampled or whether or not one assumes that species' abundances are statistically independent of one another. However, goodness-of-fit estimates are approximately twice as precise and detect lack of model fit more frequently, when based on sampling of individuals, rather than species. Bootstrap analyses indicate that the Poisson lognormal distribution exhibits substantially better fit to species abundance patterns, consistent with model selection analyses. In particular, heterogeneity in species abundances (many rare and few highly abundant species) is too great to be captured by the ZSM model or the negative binomial model and is best explained by models that predict species abundance patterns that are much closer, but not identical, to the lognormal distribution. More broadly, our bootstrap analyses suggest that estimates of model fit are likely to be robust to assumptions about the statistical interdependence of species abundances, but that tests of model fit are more powerful when they assume sampling of individuals, rather than species. Such individual-based tests therefore may be able to identify lack of model fit where previous tests have been inconclusive.

Aggregation influences coral species richness at multiple spatial scales.

The spatial dispersion of individuals across multiple spatial scales can significantly influence biodiversity patterns. Here we characterize the dispersion of corals in reef assemblages distributed across a 10000-km longitudinal biodiversity gradient from Indonesia to the Society Islands, using a multiscale sampling design. Our results indicate that most coral species were aggregated among 10-m transect samples across this vast distance. Using observed and randomized species sampling curves, we show that aggregation reduced the number of species per transect, site, and island sample on average by 13-27%. Across site, island, and regional scales, aggregation also reduced the area under species sampling curves by an average of 2.7-6.5%. The level of aggregation was relatively constant across spatial scales within regions and did not vary among habitats. However, there was significant variation among regions using transect samples across individual sites. Specifically, aggregation reduced the species richness per transect and the area under species sampling curves nearly twice as much in the Indonesian biodiversity hotspot than in the Society Islands. As a significant component of the spatial structure of coral assemblages, aggregation should be integrated into our understanding of coral community dynamics and the development of conservation strategies designed to protect these communities.

Scale-dependent variation in coral community similarity across sites, islands, and island groups.

Community similarity is the proportion of species richness in a region that is shared on average among communities within that region. The slope of local richness (alpha diversity) regressed on regional richness (gamma diversity) can serve as an index of community similarity across regions with different regional richness. We examined community similarity in corals at three spatial scales (among transects at a site, sites on an island, and islands within an island group) across a 10 000-km longitudinal diversity gradient in the west-central Pacific Ocean. When alpha diversity was regressed on gamma diversity, the slopes, and thus community similarity, increased with scale (0.085, 0.261, and 0.407, respectively) because a greater proportion of gamma diversity was subsumed within alpha diversity as scale increased. Using standard randomization methods, we also examined how community similarity differed between observed and randomized assemblages and how this difference was affected by spatial separation of species within habitat types and specialization of species to three habitat types (reef flats, crests, and slopes). If spatial separation within habitat types and/or habitat specialization (i.e., underdispersion) occurs, fewer species are shared among assemblages than the random expectation. When the locations of individual coral colonies were randomized within and among habitat types, community similarity was 46-47% higher than that for observed assemblages at all three scales. We predicted that spatial separation of coral species within habitat types should increase with scale due to dispersal/extinction dynamics in this insular system, but that specialization of species to different habitat types should not change because habitat differences do not change with scale. However, neither habitat specialization nor spatial separation within habitat types differed among scales. At the two larger scales, each accounted for 22-24% of the difference in community similarity between observed and randomized assemblages. At the smallest scale (transect-site), neither spatial separation within habitat types nor habitat specialization had significant effects on community similarity, probably due to the small size of transect samples. The results suggest that coral species can disperse among islands in an island group as easily as they can among sites on an island over time scales that are relevant to their establishment and persistence on reefs.

Adaptive management of the Great Barrier Reef and the Grand Canyon world heritage areas.

Conventional perceptions of the interactions between people and their environment are rapidly transforming. Old paradigms that view humans as separate from nature, natural resources as inexhaustible or endlessly substitutable, and the world as stable, predictable, and in balance are no longer tenable. New conceptual frameworks are rapidly emerging based on an adaptive approach that focuses on learning and flexible management in a dynamic social-ecological landscape. Using two iconic World Heritage Areas as case studies (the Great Barrier Reef and the Grand Canyon) we outline how an improved integration of the scientific and social aspects of natural resource management can guide the evolution of multiscale systems of governance that confront and cope with uncertainty, risk, and change in an increasingly human-dominated world.

Linking social and ecological systems to sustain coral reef fisheries.

The ecosystem goods and services provided by coral reefs are critical to the social and economic welfare of hundreds of millions of people, overwhelmingly in developing countries [1]. Widespread reef degradation is severely eroding these goods and services, but the socioeconomic factors shaping the ways that societies use coral reefs are poorly understood [2]. We examine relationships between human population density, a multidimensional index of socioeconomic development, reef complexity, and the condition of coral reef fish populations in five countries across the Indian Ocean. In fished sites, fish biomass was negatively related to human population density, but it was best explained by reef complexity and a U-shaped relationship with socioeconomic development. The biomass of reef fishes was four times lower at locations with intermediate levels of economic development than at locations with both low and high development. In contrast, average biomass inside fishery closures was three times higher than in fished sites and was not associated with socioeconomic development. Sustaining coral reef fisheries requires an integrated approach that uses tools such as protected areas to quickly build reef resources while also building capacities and capital in societies over longer time frames to address the complex underlying causes of reef degradation.

New paradigms for supporting the resilience of marine ecosystems.

Resource managers and scientists from disparate disciplines are rising to the challenge of understanding and moderating human impacts on marine ecosystems. Traditional barriers to communication between marine ecologists, fisheries biologists, social scientists and economists are beginning to break down, and the distinction between applied and basic research is fading. These ongoing trends arise, in part, from an increasing awareness of the profound influence of people on the functioning of all marine ecosystems, an increased focus on spatial and temporal scale, and a renewed assessment of the role of biodiversity in the sustainability of ecosystem goods and services upon which human societies depend. Here, we highlight the emergence of a complex systems approach for sustaining and repairing marine ecosystems, linking ecological resilience to governance structures, economics and society.

Global trajectories of the long-term decline of coral reef ecosystems.

Degradation of coral reef ecosystems began centuries ago, but there is no global summary of the magnitude of change. We compiled records, extending back thousands of years, of the status and trends of seven major guilds of carnivores, herbivores, and architectural species from 14 regions. Large animals declined before small animals and architectural species, and Atlantic reefs declined before reefs in the Red Sea and Australia, but the trajectories of decline were markedly similar worldwide. All reefs were substantially degraded long before outbreaks of coral disease and bleaching. Regardless of these new threats, reefs will not survive without immediate protection from human exploitation over large spatial scales.