Terence P. Hughes

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.

Governance and the Capacity to Manage Resilience in Regional Social-Ecological Systems

The sustainability of regional development can be usefully explored through several different lenses. In situations in which uncertainties and change are key features of the ecological landscape and social organization, critical factors for sustainability are resilience, the capacity to cope and adapt, and the conservation of sources of innovation and renewal. However, interventions in social-ecological systems with the aim of altering resilience immediately confront issues of governance. Who decides what should be made resilient to what? For whom is resilience to be managed, and for what purpose? In this paper we draw on the insights from a diverse set of case studies from around the world in which members of the Resilience Alliance have observed or engaged with sustainability problems at regional scales. Our central question is: How do certain attributes of governance function in society to enhance the capacity to manage resilience? Three specific propositions were explored: (1) participation builds trust, and deliberation leads to the shared understanding needed to mobilize and self-organize; (2) polycentric and multilayered institutions improve the fit between knowledge, action, and social-ecological contexts in ways that allow societies to respond more adaptively at appropriate levels; and (3) accountable authorities that also pursue just distributions of benefits and involuntary risks enhance the adaptive capacity of vulnerable groups and society as a whole. Some support was found for parts of all three propositions. In exploring the sustainability of regional social-ecological systems, we are usually faced with a set of ecosystem goods and services that interact with a collection of users with different technologies, interests, and levels of power. In this situation in our roles as analysts, facilitators, change agents, or stakeholders, we not only need to ask: The resilience of what, to what? We must also ask: For whom?

A 30‐YEAR STUDY OF CORAL ABUNDANCE, RECRUITMENT, AND DISTURBANCE AT SEVERAL SCALES IN SPACE AND TIME

Observations over a 30-yr period revealed a considerable degree of natural variation in the abundance of corals on Heron Island, Great Barrier Reef, Queensland, Australia. Cover ranged from 80%, with a similar large range in colony density, at several temporal and spatial scales. Much of this variation was due to the type, intensity, and spatial scale of disturbances that occurred. Coral assemblages usually recovered from acute disturbances, both on Heron Island and on other Indo-Pacific reefs. In contrast, corals did not recover from chronic disturbances of either natural or human origins, or from gradual declines. Recovery was slower after acute disturbances that altered the physical environment than after disturbances that simply killed or damaged corals. The space and time scales of declines and recoveries in abundance were much smaller on the wave-exposed side of the reef than on the side protected from storms. Recruitment rates were reduced by preemption of space by corals or macroalgae, and by storms that altered the substratum. Thus, the dynamics of abundance in this coral community can be largely understood through the variation in types and scales of disturbances that occurred, and the processes that took place where disturbances were rare.

RECRUITMENT FAILURE, LIFE HISTORIES, AND LONG‐TERM DECLINE OF CARIBBEAN CORALS

Population decline, local extinction, and recovery are profoundly influenced by variation in demography and life-history traits. In open populations, changes in patterns of recruitment may also have a major influence on the size of local populations, particularly for short-lived organisms. We examine here the demographic processes underlying a slow decline of corals on Jamaican reefs, where coral cover has decreased by fourfold over a 16-yr period. We divided the study into three approximately equal intervals (1977–1982, 1982–1987, and 1987–1993) and constructed size-based transition matrices for each of three abundant species of corals (Montastrea annularis, Agaricia agaricites, and Leptoseris cucullata) that differ substantially in life history: Montastrea is slower-growing, longer-lived, and has lower rates of recruitment than the other two species. Rates of survival, population growth (λ), and recruitment declined substantially over time for all species and the stable size structures became increasingly dominated by small colonies. Elasticity and life table response analysis showed that changes in the persistence of large colonies had the biggest impact on population growth in all species. Simulations indicated that the levels of larval recruitment required to maintain populations at 1977 levels increased sharply over time, even as the actual recruitment rate declined. Recruitment failure was much more important to A. agaricites and L. cucullata than to M. annularis, which could survive long periods with minimal larval input. Recovery of these populations will require an increase in both survival and recruitment. The likelihood of the latter will depend on the scale of larval dispersal, and on the impact of large-scale mortality of adults on stock-recruitment relationships. Differences in connectivity and life histories of corals will determine future patterns of recovery or further decline.

GENOTYPIC DIVERSITY AND GENE FLOW IN BROODING AND SPAWNING CORALS ALONG THE GREAT BARRIER REEF, AUSTRALIA

Abstract Marine organisms exhibit great variation in reproductive modes, larval types, and other life‐history traits that may have major evolutionary consequences. We measured local and regional patterns of genetic variation in corals along Australias Great Barrier Reef to determine the relative contributions of sexual and asexual reproduction to recruitment and to infer levels of gene flow both locally (among adjacent sites, < 5 km apart) and regionally (among reefs separated by 500–1200 km). We selected five common brooding species (Acropora cuneata, A. palifera, Pocillopora damicornis, Seriatopora hystrix, and Stylophora pistillata) and four broadcast spawners (Acropora hyacinthus, A. cytherea, A. millepora, and A. valida), which encompassed a wide range of larval types and potential dispersal capabilities. We found substantial genotypic diversity at local scales in six of the nine species (four brooders, two spawners). For these six, each local population displayed approximately the levels of multilocus genotypic diversity (Go) expected for outcrossed sexual reproduction (mean values of Go:Ge ranged from 0.85 to 1.02), although consistent single‐locus heterozygous deficits indicate that inbreeding occurs at the scale of whole reefs. The remaining three species, the brooder S. hystrix and the spawners A. valida and A. millepora displayed significantly less multilocus genotypic diversity (Go) than was expected for outcrossed sexual reproduction (Ge) within each of several sites. Acropora valida and A. millepora showed evidence of extensive localized asexual replication: (1) a small number of multilocus (clonal) genotypes were numerically dominant within some sites (Go:Ge values were as low as 0.17 and 0.20): (2) single‐locus genotype frequencies were characterized by both excesses and deficits of heterozygotes (cf. Hardy‐Weinberg expectations), and (3) significant linkage disequilibria occurred. For the brooding S. hystrix Go:Ge values were also low within each of four sites (x̄= 0.48). However, this result most likely reflects the highly restricted dispersal of gametes or larvae, because levels of genetic variation among sites within reefs were extremely high (FSR= 0.28).

Population dynamics based on individual size rather than age: a general model with a reef coral example

Models of population dynamics based on age-related parameters do not provide accurate predictions if within-age-class variance in those parameters is high. Often the demographic fate of an individual or population may be predicted more accurately using size rather than age classifications. I describe here a general model of size-related population dynamics, based on a modified Leslie matrix. The model is designed to include demographic processes, such as fragmentation and shrinkage, which are excluded from conventional age-related demographic analysis. The parameters of the model were measured during a calm and a stormy year in a field study of a colonial, sessile coral. These data were used in computer simulations to predict the fate of a cohort over long periods of time. Measured differences in individual rates of growth and shrinkage resulted in huge long-term variations in calculated colony size, fecundity, and mortality rates, between corals of equal age. Therefore, individuals of the same age will have widely differing probabilities of obtaining representation in subsequent generations. Population growth was simulated by adding a constant number of juvenile corals every year to the smallest size class. Although the model has no density-dependent parameters, population growth stops. The population size attained depends on the number of settling juveniles. Local populations of sessile organisms may be regulated by larval input, as well as by recurring disturbances or density-dependent interactions.

Herbivory on coral reefs: community structure following mass mortalities of sea urchins

The community structure of Jamaican coral reefs has undergone drastic change since mass mortalities of the long-spined black sea urchin Diadema antillarum Philippi occurred in 1983. In the absence of Diadema, algal abundance has increased enormously, up to a mean of 95% cover or 4.6 kg wet weight · m −2. Coral cover, which was already low on some reefs following Hurricane Allen in 1980, has been further reduced by as much as 60% since 1983 by competition with algae. Densities of D. antillarum at 10 sites in 1986 ranged from 0 to 12% of pre-1983 levels. Other echinoids, which might potentially compensate for the lack of herbivory from D. antillarum, have not increased significantly in density. Numbers of herbivorous scarids and acanthurids also remain at relatively low levels, because of overfishing. In the absence of high densities of fish and sea urchins, it is likely that recent changes in community structure will continue, resulting in further replacement of corals by algae in shallow water. The impact of the urchin mass mortalities is qualitatively similar to previous experimental removals of this species. In both cases, removal of echinoids resulted in substantial increases in macroalgae. However, quantitatively, the responses of algal and coral communities to the natural die-off were significantly greater, probably due to wide differences in spatial and temporal scales of the respective perturbations.

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.

The evolutionary ecology of corals.

Corals display a wide range of complex life histories. The evolutionary consequences of factors such as clonality, indeterminate growth, asexual reproduction coupled with various (sexual) breeding systems, different levels of gene flow, and strongly overlapping generations have only just begun to be explored. We identify a series of problems and areas for new research that may be resolved b y the application of novel theoretical approaches (including nonequilibrium population genetic models and demographic models incorporating modular processes such as colony fission and polyp mortality), greater in situ experimentation, long-term monitoring of population dynamics and the use of new genetic techniques.

Recruitment limitation, mortality, and population regulation in open systems: a case-study

In most populations of mammals and birds offspring live with (and initally may depend upon) their parents. Consequently, population size is strongly influenced by local fecundity. In contrast, most species of marine invertebrates have a dispersive larval stage, so that local fecundity has little or no effect on the establishment of new individuals. Similarly, many insects, amphibians, and fish have multiple life stages that live apart. Population regulation in such open systems is fundamentally different from more closed populations. I investigated the role of recruits in determining and regulating local population size of a sessile colonial invertebrate, Cellepora pumicosa (Bryozoa, Ascophora). Recruitment into a field population of C. pumicosa over an 18—mo period was less than post—recruitment mortality, causing a decline from 230 to 64 colonies (6.1 to 2.3% cover). The mortality rate was density independent. Colony growth rate declined among larger individuals, which usually regressed in size (shrank) before they died. The mechanics of recruitment limitation was further investigated using a simple demographic model. The model was designed to mimic an open population in which recruits were added to the local adult population at a rate independent of local fecundity or density. After they recruited, colonies could grow, shrink, or die at rates determined in the field. There were no density—dependent terms in the model, yet the population attained an equilibrium size and structure that was determined by a balance between rates of recruitment and size—specific mortality (i.e., storage) of recruited individuals. The equilibrium occurred because the per capita number of recruits declined as more and more individuals became established. Modelling based on the measured demography of C. pumicosa demonstrates that the observed levels of recruitment and mortality will limit the population size to very low levels, although relatively small increases in numbers of recruits would yield a substantially large population. In comparison, post—recruitment mortality would have to decrease greatly and remain density independent to achieve the same result. In contrast to the result for short—lived animals such as C. pumicosa, the population size of longer lived organisms is more sensitive to changes in mortality than recruitment, even when mortality is density independent and populations are recruitment regulated.