Towards an understanding of resilience in isolated coral reefs

In 1998, seawater temperature anomalies led to unprecedented levels of coral bleaching on reefs worldwide. We studied the direct effects of this thermal event on benthic communities and its indirect effects on their associated coral reef fish communities at a group of remote reefs off NW Australia. Long‐term monitoring of benthic and fish assemblages on these reefs allowed us to compare the responses of these communities to coral bleaching using a data series that included 4 years before, and 6 years following, this bleaching event. While bleaching mortality was evident to >30 m depth, it was patchy among the shallower survey sites with decreases in live coral cover ranging from 30% to 90% across seven surveyed locations Within 2 years of the bleaching, hard coral recovery had begun at all sites and by 2003 reef‐wide coral cover had increased to ～39% of its preimpact levels. We exploited this pattern of differential survival of corals among sites, the associated changes in these benthic communities, and their patterns of recovery, to better understand links between benthic community dynamics and their associated fish communities. Temporal changes in the resident fish communities strongly reflected the differential shifts in the benthic communities, but were lagged by 12–18 months. Five years after the bleaching event, the fish communities on five of the seven surveyed locations showed evidence of recovery, however, none had regained their preimpact structures. Analyses of these communities by taxonomic family revealed a range of responses to the disturbance reflective of their life‐histories and trophic and habitat affiliations. The slow but recognizable recovery of this isolated reef system has parallels with other relatively isolated systems that displayed resilience to the 1998 bleaching event, e.g. the Chagos archipelago, but it also contrasts sharply with low levels of resilience documented in other isolated reef systems subject to the same disturbance, e.g. the Seychelles. In this context, our results highlight the significant knowledge gaps remaining in understanding the resilience of these ecosystems to disturbance.     

Connectivity,regime shifts and the resilience of coral reefs

Connectivity of larvae among metapopulations in open marine systems can be a double-edged sword, allowing for the colonization and replenishment of both desirable and undesirable elements of interacting species-rich assemblages. This article studies the effect of recruitment by coral and macroalgae on the resilience of grazed reef ecosystems. In particular, we focus on how larval connectivity affects regime shifts between alternative assemblages that are dominated either by corals or by macroalgae. Using a model with bistability dynamics, we show that recruitment of coral larvae erodes the resilience of a macroalgae-dominated ecosystem when grazing is high, but has negligible effect when grazing is low. Conversely, recruitment by macroalgae erodes the resilience of a coral-dominated ecosystem when grazing is low, leading to a regime shift to macroalgae. Thus, spillover of coral recruits from highly protected areas will not restore coral cover or prevent flips to macroalgae in the surrounding seascape if grazing levels in these areas are depleted, but may be pivotal for re-building coral populations if grazing is high. Fishing restrictions and the re-introduction of herbivores should therefore be a prime conservation objective for preventing undesirable regime shifts. Connectivity by some components of coral reef assemblages (e.g., macroalgae, pathogens, crown-of-thorns starfish) may be detrimental to sustaining reefs, especially where overfishing and other drivers have eroded their resilience, making them more vulnerable to a regime shift.     

Synergistic impacts of global warming on the resilience of coral reefs

Recent epizootics have removed important functional species from Caribbean coral reefs and left communities vulnerable to alternative attractors. Global warming will impact reefs further through two mechanisms. A chronic mechanism reduces coral calcification, which can result in depressed somatic growth. An acute mechanism, coral bleaching, causes extreme mortality when sea temperatures become anomalously high. We ask how these two mechanisms interact in driving future reef state (coral cover) and resilience (the probability of a reef remaining within a coral attractor). We find that acute mechanisms have the greatest impact overall, but the nature of the interaction with chronic stress depends on the metric considered. Chronic and acute stress act additively on reef state but form a strong synergy when influencing resilience by intensifying a regime shift. Chronic stress increases the size of the algal basin of attraction (at the expense of the coral basin), whereas coral bleaching pushes the system closer to the algal attractor. Resilience can change faster—and earlier—than a change in reef state. Therefore, we caution against basing management solely on measures of reef state because a loss of resilience can go unnoticed for many years and then become disproportionately more difficult to restore.     

Phase shifts and the role of herbivory in the resilience of coral reefs

Cousin Island marine reserve (Seychelles) has been an effectively protected no-take marine protected area (MPA) since 1968 and was shown in 1994 to support a healthy herbivorous fish assemblage. In 1998 Cousin Island reefs suffered extensive coral mortality following a coral bleaching event, and a phase shift from coral to algal dominance ensued. By 2005 mean coral cover was <1%, structural complexity had fallen and there had been a substantial increase in macroalgal cover, up to 40% in some areas. No clear trends were apparent in the overall numerical abundance and biomass of herbivorous fishes between 1994 and 2005, although smaller individuals became relatively scarce, most likely due to the loss of reef structure. Analysis of the feeding habits of six abundant and representative herbivorous fish species around Cousin Island in 2006 demonstrated that epilithic algae were the preferred food resource of all species and that macroalgae were avoided. Given the current dominance of macroalgae and the apparent absence of macroalgal consumers, it is suggested that the increasing abundance of macroalgae is reducing the probability of the system reverting to a coral dominated state.     

Coral bleaching, reef fish community phase shifts and the resilience of coral reefs

The 1998 global coral bleaching event was the largest recorded historical disturbance of coral reefs and resulted in extensive habitat loss. Annual censuses of reef fish community structure over a 12-year period spanning the bleaching event revealed a marked phase shift from a prebleach to postbleach assemblage. Surprisingly, we found that the bleaching event had no detectable effect on the abundance, diversity or species richness of a local cryptobenthic reef fish community. Furthermore, there is no evidence of regeneration even after 5–35 generations of these short-lived species. These results have significant implications for our understanding of the response of coral reef ecosystems to global warming and highlight the importance of selecting appropriate criteria for evaluating reef resilience.     

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.     

Biological destruction of coral reefs

The major agents of biological destruction of coral reefs can be divided into grazers, etchers and borers. Each of these groups is reviewed on a world wide basis, together with the mechanisms by which they destroy the coral substrate. Rates of bioerosion attributed to major agents of grazers, etchers and borers are given, together with limitations of some of the measurements. Recent work is highlighting the variability in rates of bioerosion both over time and space. Factors which may be responsible for this variability are discussed. Bioerosion is a major factor influencing reef morphology and the ways in which this is achieved is discussed in some detail. Although the review concentrates mainly on present day reefs, some attempt is made to consider the impact of bioerosion on older reefs.     

Marine pollution and coral reefs

Coral reefs are exposed to many anthropogenic stresses increasing in impact and range, both on local and regional scales. The main ones discussed here are nutrient enrichment, sewage disposal, sedimentation, oil-related pollution, metals and thermal pollution. The stress comprising the main topic of this article, eutrophication, is examined from the point of view of its physiological and ecological mechanisms of action, on a number of levels. Nutrient enrichment can introduce an imbalance in the exchange of nutrients between the zooxanthellae and the host coral, it reduces light penetration to the reef due to nutrient- stimulated phytoplankton growth, and, most harmful of all, may bring about proliferation of seaweeds. The latter rapidly outgrow, smother and eventually replace, the slow-growing coral reef, adapted to cope with the low nutrient concentrations typical in tropical seas.
Eutrophication seldom takes place by itself. Sewage disposal invariably results in nutrient enrichment, but it also enriches the water with organic matter which stimulates proliferation of oxygen-consuming microbes. These may kill corals and other reef organisms, either directly by anoxia, or by related hydrogen sulfide production. Increased sediment deposition is in many cases associated with other human activities leading to eutrophication, such as deforestation and topsoil erosion.
Realistically achievable goals to ensure conservation, and in some instances, rehabilitation of coral reefs are listed.     

Black reefs: iron-induced phase shifts on coral reefs

The Line Islands are calcium carbonate coral reef platforms located in iron-poor regions of the central Pacific. Natural terrestrial run-off of iron is non-existent and aerial deposition is extremely low. However, a number of ship groundings have occurred on these atolls. The reefs surrounding the shipwreck debris are characterized by high benthic cover of turf algae, macroalgae, cyanobacterial mats and corallimorphs, as well as particulate-laden, cloudy water. These sites also have very low coral and crustose coralline algal cover and are call black reefs because of the dark-colored benthic community and reduced clarity of the overlying water column. Here we use a combination of benthic surveys, chemistry, metagenomics and microcosms to investigate if and how shipwrecks initiate and maintain black reefs. Comparative surveys show that the live coral cover was reduced from 40 to 60% to <10% on black reefs on Millennium, Tabuaeran and Kingman. These three sites are relatively large (>0.75 km²). The phase shift occurs rapidly; the Kingman black reef formed within 3 years of the ship grounding. Iron concentrations in algae tissue from the Millennium black reef site were six times higher than in algae collected from reference sites. Metagenomic sequencing of the Millennium Atoll black reef-associated microbial community was enriched in iron-associated virulence genes and known pathogens. Microcosm experiments showed that corals were killed by black reef rubble through microbial activity. Together these results demonstrate that shipwrecks and their associated iron pose significant threats to coral reefs in iron-limited regions.     

Atlantic coral reefs: the transplantation alternative

Although all of the world’s coral reef regions have suffered degradation due to direct and indirect human influences, only the Western Atlantic reefs have declined to the extent that their continued existence appears to be in jeopardy. Of a once flourishing reef system, only about 10% is still alive and it is depauperate in terms of the food web diversity necessary to maintain a stable and productive ecosystem. The large carnivores and herbivores have become so scarce that they have failed to control the populations of smaller animals and plants, so that almost all the trophic levels have been disrupted. At the same time, the impacts of many other factors have contributed to the process of degradation resulting in a true crisis. The extent of damage, and the general impairment of regeneration, is such that a hope for natural recovery appears to be unrealistic. It is suggested that a recovery could be achieved through transplantation of corals and other reef species from areas where more diverse, relatively stable ecosystems still exist. Available data on the introduction of exotic species into marine ecosystems indicate that such species are generally accommodated and do not cause extinctions among the native species. Although some introduced species are considered to be pests, others have proved to be beneficial, and all have apparently increased the biodiversity of the invaded areas.     

Boring Forminifera in French Polynesian coral reefs

The discovery of epipsammitic Foraminifera in sediments of Moorea and Scilly (French Polynesia) and the study of close relationships between embedded specimens and host-grains indicate that some species participate in the weakening and subsequent breakdown of skeletal grains and consequently contribute to the production of silt-sized particles. The study of 36 stations around the islands shows the factors that control the distribution and abundance of this incrusted microfauna. Specimens are more abundant on sand particles larger than 1,000 microns and in the high energy areas; this abundance decreases with depth. The physiological mechanism of penetrations is presumably chemical, but each species apparently has its own process: complete dissolution with removal of ions for the cytoplasm of calcareous species; partial dissolution with transport of silt-size aggregates on the test of agglutinated species. The purpose of such penetration may be to protect themselves against water turbulence and to provide material for test construction.     

Role of coral reefs in global ocean production

Coral reefs cover some 600 thousand square kilometres of the earth's surface (0.17% of the ocean surface). First order estimates show coral reefs to contribute about 0.05% of the estimated net CO₂ fixation rate of the global oceans. Gross CO₂ fixation is relatively high (of the order 700×10¹² g C year^-1), but most of this material is recycled within the reefs. Excess (net) production of organic material (E) is much smaller, of the order 20×10¹² g C year^-1. We estimate that 3×10¹² g C year^-1 (15% ofE) is buried in reef structure, 2×10¹² g C year^-1 (10% ofE) is available for sustained human harvest, and the remaining 75% ofE is available for export from coral reefs to adjacent areas. Comparison of estimates for net production by reefs and their surrounding oceans indicates that the excess production by coral reefs is similar to new production in the photic zone of oligotrophic oceans. Consequently, estimates for global ocean production should as a first approximation include reefal areas with the surrounding ocean when assigning average net production rates. While there are significant uncertainties in these numbers, it can be concluded that organic production by reefs plays a relatively minor role in the global scale of fluxes and storage of elements. In comparison, the companion process of biologically-mediated inorganic carbon precipitation represents a major role for reefs. While reef production does respond on local scales to variation in ocean climate, neither the absolute rates nor the amount accumulated into organic pools appear to be either sensitive indicators or accurate recorders of climatic change in most reef systems. Similarly, the productivity of most reefs should be little affected by currently predicted environmental changes resulting from the Greenhouse effect.Authorship sequence does not imply seniority, it is deliberately alphabetical     

Historical reconstruction reveals recovery in Hawaiian coral reefs

Coral reef ecosystems are declining worldwide, yet regional differences in the trajectories, timing and extent of degradation highlight the need for in-depth regional case studies to understand the factors that contribute to either ecosystem sustainability or decline. We reconstructed social-ecological interactions in Hawaiian coral reef environments over 700 years using detailed datasets on ecological conditions, proximate anthropogenic stressor regimes and social change. Here we report previously undetected recovery periods in Hawaiian coral reefs, including a historical recovery in the MHI (~AD 1400-1820) and an ongoing recovery in the NWHI (~AD 1950-2009+). These recovery periods appear to be attributed to a complex set of changes in underlying social systems, which served to release reefs from direct anthropogenic stressor regimes. Recovery at the ecosystem level is associated with reductions in stressors over long time periods (decades+) and large spatial scales (>10(3) km(2)). Our results challenge conventional assumptions and reported findings that human impacts to ecosystems are cumulative and lead only to long-term trajectories of environmental decline. In contrast, recovery periods reveal that human societies have interacted sustainably with coral reef environments over long time periods, and that degraded ecosystems may still retain the adaptive capacity and resilience to recover from human impacts.     

Taphonomy of coral reefs: a review

This review summarises the major factors that affect the post-mortem history of skeletons in a coral reef environment. Skeletal material is traced from life, through death, breakdown, transport, burial and diagenesis to its final fossil form. The fact that most reef sediments are of skeletal composition poses problems of concentration or dilution of individual grain types in taphonomic analysis of reefs. Rates of supply of grains vary, not only with organism abundance and skeletal growth rates, but also with rates of physical and biological breakdown to transportable sediment. Physical and organic processes affect sedimentary structures and textures by mixing or segregating skeletal grains, though biogenic processes normally dominate in the protected setting of reef lagoons. The soft and hard substrates associated with reefs present different media for calcium carbonate accumulation and post-depositional disturbance, for example, loose sediments suffer bioturbation and rocks surfaces suffer bioerosion. The wide range of durability of skeletons and their susceptibility to diagenesis contribute further to the complexities of the preservation of coral reefs.