Jason E. Tanner

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.

Supply-side ecology works both ways : the link between benthic adults, fecundity, and larval recruits

Supply-side ecology recognizes the potential role that recruitment plays in the local population dynamics of open systems. Apart from the applied fisheries literature, the converse link between adults and the production of cohorts of recruits has received much less attention. We used a hierarchical sampling design to investigate the relationships between adult abundance, fecundity, and rates of larval recruitment by acroporid corals on 33 reefs in five sectors (250-400 km apart) stretching from north to south along the length of the Great Barrier Reef, Australia. Our goal was to quantify patterns of recruitment at multiple scales, and to explore the underlying mechanisms. Specifically, we predicted that large-scale patterns of recruitment could be driven by changes in the abundance of adults and/or their fecundity, i.e., that corals exhibit a stock-recruitment relationship. The amount of recruitment by acroporids in each of two breeding seasons varied by more than 35-fold among the five sectors. Adult density varied only twofold among sectors and was not correlated with recruitment at the sector or reef scale. In contrast, fecundity levels (the proportion of colonies on each reef that contained ripe eggs) varied from 15% to 100%, depending on sector, year, and species. Spatial and temporal variation in the fecundity of each of three common Acropora species explained most of the variation (72%) in recruitment by acroporids, indicating that the production of larvae is a major determinant of levels of recruitment at large scales. Once fecundity was accounted for, none of the other variables we examined (sector, reef area, abundance of adults, or year) contributed significantly to variation in recruitment. The relationship between fecundity and recruitment was nonlinear, i.e., rates of recruitment increased disproportionately when and where the proportion of gravid colonies approached 100%. This pattern is consistent with the hypothesis that enhanced fertilization success and/or predator satiation occurs during mass-spawning events. Furthermore, it implies that small, sublethal changes in fecundity of corals could result in major reductions in recruitment.

Patterns of recruitment and abundance of corals along the Great Barrier Reef

Different physical and biological processes prevail at different scales. As a consequence, small-scale experiments or local observations provide limited insights into regional or global phenomena. One solution is to incorporate spatial scale explicitly into the experimental and sampling design of field studies, to provide a broader, landscape view of ecology. Here we examine spatial patterns in corals on the Great Barrier Reef, across a spectrum of scales ranging from metres to more than 1,700u2009km. Our study is unusual because we explore large-scale patterns of a process (recruitment by juveniles) as well as patterns of adult abundance, revealing the relationship between the two. We show that coral-reef assemblages that are similar in terms of abundance may nonetheless show profound differences in dynamics and turnover, with major implications for their ecology, evolution and management.

Competition between scleractinian corals and macroalgae: An experimental investigation of coral growth, survival and reproduction

Abstract Macroalgae are a major component of many coral reef flat communities, and are potentially major competitors with corals. The influence of macroalgae on several demographic parameters of four species of scleractinian coral by means of an algal clearance experiment was examined to determine specifically if macroalgae are affecting coral cover, growth, fecundity, fission, survivorship and recruitment. Also investigated were patterns of natural encounters between corals and algae. Algal cover at the study site ranged from 41 to 56%, and coral cover from 8 to 10%. In total, 92 ± 4 ( se )% of coral colonies were in contact with one or more species of macroalgae. Changes in coral cover were significantly affected by the presence of macroalgae, with cover of Acropora species increasing faster in areas from which algae had been cleared compared to control areas where algae had not been removed, although this pattern did not occur for Pocillopora damicornis (Linnaeus). Similarly, growth of individual colonies was faster when macroalgae were absent for three Acropora species but not for P. damicornis . There were no differences detected in rates of fission or survivorship of corals between algal clearance and control treatments, although there were high levels of variability in both of these parameters. Fecundity of Acropora palifera (Lamarck), the only species examined, was approximately double in colonies in cleared plots compared to those in control plots with macroalgae present. As no recruitment occurred throughout the 2-yr study, it remains to be determined how macroalgae effect the settlement of coral larvae. The results show that macroalgae can have a major influence on the demography of scleractinian corals.

Species Coexistence, Keystone Species, and Succession: A Sensitivity Analysis

One of the major questions in ecology is, what controls the structure of communities? We used projection matrix models to examine community dynamics and patterns of succession. The inputs of the model are transition probabilities of species replacements that were measured repeatedly during a long-term (1962-1989) study of diverse coral assemblages on Heron Island, Great Barrier Reef. Transitions varied strikingly among species and sites, reflecting differences in recruitment, growth, longevity (persis- tence), and the rate of replacement of one species by another. Species that had a poor ability to persist (e.g., algae and Pocilloporid corals) were generally good colonists. The observed number of transitions expressed as a proportion of the maximum number possible provides an index of the complexity of interactions in an assemblage, analogous to the concept of connectance in food-web analysis. Transitions occurred to and from nearly every species group, indicating that there was no competitive dominant in this system. We use the models in simulations to track transitory changes in species abundance and community composition following a major disturbance (e.g., due to a cyclone or outbreak of crown-of-thorns starfish). Some species showed a rapid initial increase followed by a decline to lower equilibrium levels, while others increased smoothly to a generally higher equilibrial abundance. The length of time required to reach a climax assemblage using the same matrix recurrently (_20 yr) is far greater than the observed interval between major disturbances, supporting nonequilibrium theories of coral reef communities. Climax as- semblages were highly diverse and varied in composition from site to site. The inter- mediate disturbance hypothesis does not fully predict successional changes in these shal- low-water coral assemblages since diversity remained very high at equilibrium (i.e., long after a major disturbance). Competitively inferior species were not eliminated because routine mortality ensured that some space always remained available for colonization. We also present a novel method for quantifying the relative importance of each species interaction to community composition and the rate of succession, based on a sensitivity analysis of the transition matrix. The analysis shows that the importance of a species to the dynamics of a community may be unrelated to its abundance at equilibrium, with some rare species groups having a greater impact than more common ones. Sensitivity analysis of this type will provide a powerful means of identifying keystone species in complex assemblages where experimental manipulation of each species is impossible.

A LONG‐TERM STUDY OF COMPETITION AND DIVERSITY OF CORALS

Variations in interspecific competition, abundance, and alpha and beta diversities of corals were studied from 1962 to 2000 at different localities on the reef at Heron Island, Great Barrier Reef, Australia. Reductions in abundance and diversity were caused by direct damage by storms and elimination in competition. Recovery after such reductions was influenced by differences in the size of the species pools of recruits, and in contrasting competitive processes in different environments. In some places, the species pool of coral larval recruits is very low, so species richness (S) and diversity (D) never rise very high. At other sites, this species pool of recruits is larger, and S and D soon rise to high levels. After five different hurricanes destroyed corals at some sites during the 38- year period, recovery times of S and D ranged from 3 to 25 years. One reason for the variety of recovery times is that the physical environment was sometimes so drastically changed during the hurricane that a long period was required to return it to a habitat suitable for corals. Once S and D have peaked during recolonization, they may either remain at a high level, or decline. In shallow water, with no deleterious changes in environmental conditions, S and D may not decline over time, because superior competitors cannot overtop inferior competitors without exposing themselves to deleterious aerial exposure at low tide. At other times and places, S and D did decline over time. One cause of this was a gradual deterioration of the physical environment, as corals grew upward into the intertidal region and died of exposure. S and D also fell because the wave action in hurricanes either killed colonies in whole or part, or changed the drainage patterns over the reef crest, leaving corals high and dry at low tide. At deeper sites, declines in S and D were sometimes caused by heavy wave action, or by interspecific competition, as some corals overgrew or overtopped their neighbors and eliminated them.

Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment

Regional-scale variation of recruitment by marine organisms may reflect geographic patterns in adult stock sizes or fecundities, large-scale hydrodynamic features that influence the transport of larvae (e.g., currents, upwelling), and patterns of early mortality. In turn, recruitment may play a vital role in determining patterns of adult abundance and community structure, from local to biogeographic scales. We examined spatial variation in recruitment by corals at a regional scale, along 3300 km of the tropical and subtropical coast of eastern Australia (10°–31° S). We used two complementary approaches: (1) a metaanalysis of 21 different studies undertaken over a 16-yr period, each of which was generally conducted at a single reef, and (2) a large-scale sampling effort in which recruitment was measured in two years on 33 reefs arrayed along the length of the Great Barrier Reef (GBR). Our goal is to compare the emergent large-scale picture derived from many small-scale studies with patterns revealed by shorter-term regional sampling. The two approaches show very similar large-scale patterns. Recruitment by spawning ncorals (mainly acroporids) was highest in the central GBR and declined steadily with increasing latitude by up to more than 20-fold. A smaller decline occurred on the northern GBR between Australian and Papua New Guinea. Recruitment by brooding corals (mostly pocilloporids) was greatest in the northern GBR and also declined to the south. The latitudinal decline in brooders was three-to fivefold, i.e., not as great as for spawners. Consequently, nthe proportion of brooded recruits increased to the south, and they generally exceeded spawners on the southern GBR and on isolated subtropical reefs at higher latitudes. nOur meta-analysis shows that fully half of the variation in the ratio of spawners to brooders is attributable to one of 11 variables that we extracted from the published studies: the month when the recruitment panels were deployed. This result suggests that the intensity and timing of spawning have a crucial impact on large-scale patterns of recruitment. Elsewhere, we tested this hypothesis in the field, and confirmed that regional variation in recruitment by spawning acroporid corals was driven by spatial and temporal variation in the extent of mass spawning. Together, large-scale sampling and meta-analyses provide a npowerful, combined approach for investigating large-scale patterns and the mechanisms underlying them.

Seasonality and lunar periodicity in the reproduction of Pocilloporid corals

Reproductive seasonality and lunar periodicity of planula release were investigated for the three brooding coralsPocillopora damicornis, Seriatopora hystrix, andStylophora pistillata at Heron Island in the southern Great Barrier Reef. Branch fragments collected from undisturbed colonies in the field were used to determine when planulae were present for all three species, and direct observations of planula release were made on colonies ofPocillopora kept in aquaria. All three species displayed marked seasonal variation in reproductive output, with nearly all reproductive activity occurring over the summer months.Pocillopora exhibited distinct lunar periodicity in planulation, with planula release occurring around three quarter moon, and no planulae being present in samples collected between new and full moons.Seriatopora also displayed lunar periodicity of planula release, although it was not as distinct as forPocillopora, whileStylophora did not show any lunar periodicity.

The Role of History in Community Dynamics: A Modelling Approach

Recent history plays an important role in the physiology, behavior, and ecology of individuals, and in the dynamics of populations and assemblages of species. In this paper, we examine the impact of history on the species composition of intertidal reef corals, by comparing simulation models that incorporate four different levels of knowledge about the recent past (over a time scale of 1-27 yr). The models are Markov or semi-Markov transition probability matrix models, based on rates of colonization, persistence, and species replacement measured from a long-term study spanning three decades at Heron Island, Great Barrier Reef. n nRates of colonization (transitions from free space) varied 20-fold for different species groups, while mortality (transitions to free space) ranged fivefold, reflecting a wide range of life histories among the coral assemblage. Virtually all species groups could undergo reciprocal transitions (e.g., from A to B, and B to A) in a single time interval, indicating the lack of a single competitive dominant that was capable of outcompeting all or most other species. n nTransition probabilities changed markedly as a function of history. For most species groups, the probability of persisting (i.e., transitions from A to A) increased with time. Thus, a colony that had occupied space for some time was generally more likely to continue to do so than a new arrival. This result is consistent with an escape in size for older colonies from mortality agents such as competition and predation. However, three species groups showed the opposite pattern. Algae, Pocilloporid corals, and fragile tabular Acroporn showed marked increases in transitions to free space after 3-5 yr, reflecting a more ephemeral suite of life history traits. Similarly, free space that had recently been generated had a higher rate of colonization than substratum that had been unoccupied for some time. These results falsify a major assumption of standard first-order models, i.e., that transition probabilities are constant, and that history is irrelevant. n nAlthough the changes in transition probabilities as a function of history were often striking, the four different models we employed show only minor variation in community composition in both transitory and climax (equilibrium) phases. Thus, while recent history was important in determining transition probabilities, it had little effect on community dynamics and structure in this system. This discrepancy is due to the rapid turnover of corals and algae on shallow reef crests, where only a small proportion of colonies survive long enough to display effects of history. All models agreed that the length of time required for this system to reach an equilibrium community structure is far longer than the observed interval between recurrent disturbances from tropical cyclones.

Assembly Rules of Reef Corals Are Flexible along a Steep Climatic Gradient

Coral reefs, one of the worlds most complex and vulnerable ecosystems, face an uncertain future in coming decades as they continue to respond to anthropogenic climate change, overfishing, pollution, and other human impacts [1, 2]. Traditionally, marine macroecology is based on presence/absence data from taxonomic checklists or geographic ranges, providing a qualitative overview of spatial shifts in species richness that treats rare and common species equally [3, 4]. As a consequence, regional and long-term shifts in relative abundances of individual taxa are poorly understood. Here we apply a more rigorous quantitative approach to examine large-scale spatial variation in the species composition and abundance of corals on midshelf reefs along the length of Australias Great Barrier Reef, a biogeographic region where species richness is high and relatively homogeneous [5]. We demonstrate that important functional components of coral assemblages sample space differently at 132 sites separated by up to 1740 km, leading to complex latitudinal shifts in patterns of absolute and relative abundance. The flexibility in community composition that we document along latitudinal environmental gradients indicates that climate change is likely to result in a reassortment of coral reef taxa rather than wholesale loss of entire reef ecosystems.