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.     

Mass coral bleaching causes biotic homogenization of reef fish assemblages

Global climate change is altering community composition across many ecosystems due to nonrandom species turnover, typically characterized by the loss of specialist species and increasing similarity of biological communities across spatial scales. As anthropogenic disturbances continue to alter species composition globally, there is a growing need to identify how species responses influence the establishment of distinct assemblages, such that management actions may be appropriately assigned. Here, we use trait‐based analyses to compare temporal changes in five complementary indices of reef fish assemblage structure among six taxonomically distinct coral reef habitats exposed to a system‐wide thermal stress event. Our results revealed increased taxonomic and functional similarity of previously distinct reef fish assemblages following mass coral bleaching, with changes characterized by subtle, but significant, shifts toward predominance of small‐bodied, algal‐farming habitat generalists. Furthermore, while the taxonomic or functional richness of fish assemblages did not change across all habitats, an increase in functional originality indicated an overall loss of functional redundancy. We also found that prebleaching coral composition better predicted changes in fish assemblage structure than the magnitude of coral loss. These results emphasize how measures of alpha diversity can mask important changes in the structure and functioning of ecosystems as assemblages reorganize. Our findings also highlight the role of coral species composition in structuring communities and influencing the diversity of responses of reef fishes to disturbance. As new coral species configurations emerge, their desirability will hinge upon the composition of associated species and their capacity to maintain key ecological processes in spite of ongoing disturbances.     

Thermal stress induces persistently altered coral reef fish assemblages

Ecological communities are reorganizing in response to warming temperatures. For continuous ocean habitats this reorganization is characterized by large‐scale species redistribution, but for tropical discontinuous habitats such as coral reefs, spatial isolation coupled with strong habitat dependence of fish species imply that turnover and local extinctions are more significant mechanisms. In these systems, transient marine heatwaves are causing coral bleaching and profoundly altering habitat structure, yet despite severe bleaching events becoming more frequent and projections indicating annual severe bleaching by the 2050s at most reefs, long‐term effects on the diversity and structure of fish assemblages remain unclear. Using a 23‐year time series spanning a thermal stress event, we describe and model structural changes and recovery trajectories of fish communities after mass bleaching. Communities changed fundamentally, with the new emergent communities dominated by herbivores and persisting for >15 years, a period exceeding realized and projected intervals between thermal stress events on coral reefs. Reefs which shifted to macroalgal states had the lowest species richness and highest compositional dissimilarity, whereas reefs where live coral recovered exceeded prebleaching fish richness, but remained dissimilar to prebleaching compositions. Given realized and projected frequencies of bleaching events, our results show that fish communities historically associated with coral reefs will not re‐establish, requiring substantial adaptation by managers and resource users.     

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.     

Bleaching response of coral species in the context of assemblage response

Caribbean coral reefs are declining due to a mosaic of local and global stresses, including climate change-induced thermal stress. Species and assemblage responses differ due to factors that are not easily identifiable or quantifiable. We calculated a novel species-specific metric of coral bleaching response, taxon-α and -β, which relates the response of a species to that of its assemblages for 16 species over 18 assemblages. By contextualizing species responses within the response of their assemblages, the effects of environmental factors are removed and intrinsic differences among taxa are revealed. Most corals experience either a saturation response, overly sensitive to weak stress (α > 0) but under-responsive compared to assemblage bleaching (β < 1), or a threshold response, insensitive to weak stress (α < 0) but over-responsive compared to assemblage bleaching (β > 1). This metric may help reveal key factors of bleaching susceptibility and identify species as targets for conservation.     

Long-lived groupers require structurally stable reefs in the face of repeated climate change disturbances

Benthic recovery from climate-related disturbances does not always warrant a commensurate functional recovery for reef-associated fish communities. Here, we examine the distribution of benthic groupers (family Serranidae) in coral reef communities from the Lakshadweep archipelago (Arabian Sea) in response to structural complexity and long-term habitat stability. These coral reefs that have been subject to two major El Niño Southern Oscillation-related coral bleaching events in the last decades (1998 and 2010). First, we employ a long-term (12-yr) benthic-monitoring dataset to track habitat structural stability at twelve reef sites in the archipelago. Structural stability of reefs was strongly driven by exposure to monsoon storms and depth, which made deeper and more sheltered reefs on the eastern aspect more stable than the more exposed (western) and shallower reefs. We surveyed groupers (species richness, abundance, biomass) in 60 sites across the entire archipelago, representing both exposures and depths. Sites were selected along a gradient of structural complexity from very low to high. Grouper biomass appeared to vary with habitat stability with significant differences between depth and exposure; sheltered deep reefs had a higher grouper biomass than either sheltered shallow or exposed (deep and shallow) reefs. Species richness and abundance showed similar (though not significant) trends. More interestingly, average grouper biomass increased exponentially with structural complexity, but only at the sheltered deep (high stability) sites, despite the availability of recovered structure at exposed deep and shallow sites (lower-stability sites). This trend was especially pronounced for long-lived groupers (life span >10 yrs). These results suggest that long-lived groupers may prefer temporally stable reefs, independent of the local availability of habitat structure. In reefs subject to repeated disturbances, the presence of structurally stable reefs may be critical as refuges for functionally important, long-lived species like groupers.     

Life histories predict coral community disassembly under multiple stressors

Climate change is reshaping biological communities against a background of existing human pressure. Evaluating the impacts of multiple stressors on community dynamics can be particularly challenging in species‐rich ecosystems, such as coral reefs. Here, we investigate whether life‐history strategies and cotolerance to different stressors can predict community responses to fishing and temperature‐driven bleaching using a 20‐year time series of coral assemblages in Kenya. We found that the initial life‐history composition of coral taxa largely determined the impacts of bleaching and coral loss. Prior to the 1998 bleaching event, coral assemblages within no‐take marine reserves were composed of three distinct life histories – competitive, stress‐tolerant and weedy– and exhibited strong declines following bleaching with limited subsequent recovery. In contrast, fished reefs had lower coral cover, fewer genera and were composed of stress‐tolerant and weedy corals that were less affected by bleaching over the long term. Despite these general patterns, we found limited evidence for cotolerance as coral genera and life histories were variable in their sensitivities to fishing and bleaching. Overall, fishing and bleaching have reduced coral diversity and led to altered coral communities of ‘survivor’ species with stress‐tolerant and weedy life histories. Our findings are consistent with expectations that climate change interacting with existing human pressure will result in the loss of coral diversity and critical reef habitat.     

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.     

Size-structural shifts reveal intensity of exploitation in coral reef fisheries

Fisheries exploitation represents a considerable threat to coral reef fish resources because even modest levels of extraction can alter ecological dynamics via shifts of stock size, species composition, and size-structure of the fish assemblage. Although species occupying higher trophic groups are known to suffer the majority of exploitative effects, changes in composition among lower trophic groups may be major, though are not frequently explored. Using size-based biomass spectrum analysis, we investigate the effects of fishing on the size-structure of coral reef fish assemblages spanning four geopolitical regions and determine if patterns of exploitation vary across trophic groups. Our analyses reveal striking evidence for the variety of effects fisheries exploitation can have on coral reef fish assemblages. When examining biomass spectra across the entire fish assemblage we found consistent evidence of size-specific exploitation, in which large-bodied individuals experience disproportionate reductions. The pattern was paralleled by and likely driven by, strongly size-specific reductions among top predators. In contrast, evidence of exploitation patterns was variable among lower trophic groups, in many cases including evidence of reductions across all size classes. The breadth of size classes and trophic groups that showed evidence of exploitation related positively to local human population density and diversity of fishing methods employed. Our findings highlight the complexity of coral reef fisheries and that the effects of exploitation on coral reefs can be realized throughout the entire fish assemblage, across multiple trophic groups and not solely restricted to large-bodied top-predators. Size-specific changes among fishes of lower trophic groups likely lead to altered ecological functioning of heavily exploited coral reefs. Together these findings reinforce the value of taking a multi-trophic group approach to monitoring and managing coral reef fisheries.     

Multiscale habitat associations of detrivorous blennies (Blenniidae: Salariini)

The distribution and habitat associations of detrivorous blennies on a tropical coral reef were investigated at several spatial scales and compared with other fish that feed on the epilithic algal matrix to assess density and biomass contributions of small detrivorous fishes to these assemblages. At broad spatial scales total blenny abundance and biomass were highest on the tops of reefs exposed to prevailing winds. On the finer scale of microhabitat use, all species showed a preference for non-living corals, although the type of coral utilised differed between species. The high abundance of blennies on reef tops and non-living corals may be partially related to the quality and availability of detritus in these habitats. Comparisons of total blenny abundance and biomass with other territorial detrivores found that blennies accounted for approximately 60% of this functional group's density and 21% of their biomass on exposed reef tops. Overall, territorial detrivores were found to constitute approximately 37% of the density and 26% of the biomass of the detrivorous/herbivorous fish assemblage on exposed reef tops. Small detrivorous fish therefore represent a substantial proportion of fish assemblages that feed on epilithic algae and associated detritus on coral reefs.     

The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblage

The fish assemblage from the Eocene deposits of Monte Bolca, Northern Italy, are compared with those of Recent coral reefs. A family-level taxonomic definition of a Recent coral reef fish assemblage is formulated to permit direct comparisons. On this basis, the Monte Bolca fishes represent the earliest clearly defined coral reef fish assemblage. Quantitative analyses of the relative abundance of fish families revealed significant differences between the two assemblages. The Bolca assemblage has Mesozoic links (Pycnodontiformes) and non-perciform taxa are relatively abundant, particularly the Beryciformes (Holocentridae). However, Bolca represents the earliest record of a perciform-dominated benthic fish assemblage (68.4% of all non-clupeid taxa). Within the Perciformes, the abundance of the major reef fish lineages (higher squamipinnes and Labroidei) differs markedly between the two assemblages. The numerical dominance of labroid fishes on coral reefs appears to have been a relatively recent occurrence.     

A Positive Trajectory for Corals at Little Cayman Island

Coral reefs are damaged by natural disturbances and local and global anthropogenic stresses. As stresses intensify, so do debates about whether reefs will recover after significant damage. True headway in this debate requires documented temporal trajectories for coral assemblages subjected to various combinations of stresses; therefore, we report relevant changes in coral assemblages at Little Cayman Island. Between 1999 and 2012, spatiotemporal patterns in cover, densities of juveniles and size structure of assemblages were documented inside and outside marine protected areas using transects, quadrats and measurements of maximum diameters. Over five years, bleaching and disease caused live cover to decrease from 26% to 14%, with full recovery seven years later. Juvenile densities varied, reaching a maximum in 2010. Both patterns were consistent within and outside protected areas. In addition, dominant coral species persisted within and outside protected areas although their size frequency distributions varied temporally and spatially. The health of the coral assemblage and the similarity of responses across levels of protection suggested that negligible anthropogenic disturbance at the local scale was a key factor underlying the observed resilience.     

Anthropogenic Stressors,Inter-Specific Competition and ENSO Effects on a Mauritian Coral Reef

Much of the western Indian Ocean suffered widespread loss of live coral in 1998 and interest is now focussed on the indirect effects of this coral loss on other components of the ecosystem, in particular fishes. However, it is just as important to identify changes in fish assemblages at locations that did not suffer coral mortality to understand local versus regional drivers. We surveyed benthic and fish communities on a reef flat in Mauritius five times between 1994 and 2005. The design allowed for comparison through time, along the coast and between inshore and offshore reef locations. The benthic community demonstrates a clear trend along the coast, likely in response to a dredged water ski lane, but little change through time. Branching Acropora colonies dominate much of the live coral and best explain patterns in the fish assemblage (P < 0.01). Few changes in overall fish species richness through time were identified, and observed changes were within fishery target families rather than species reliant on live coral. Departure from expected levels of taxonomic distinctness suggests degradation in the community associated with the dredged ski lane. Non-metric multi-dimensional scaling of the fish assemblage demonstrates a similar pattern to that seen in the benthos; greater differences along the coast (Global R = 0.34) than through time (Global R = 0.17) and no trend between reef positions. SIMPER analysis identified two species of Stegastes as the main drivers of trends in the MDS plot and the most dominant of these, S. lividus, appears to be reducing species richness of the remaining fish community. The study highlights Mauritius as a regional refugia of thermally-sensitive corals and specialised fish, suggesting a need for careful management.     

Coexisting mangrove-coral habitat use by reef fishes in the Caribbean

We conducted visual fish surveys in coexisting mangrove-coral (CMC) habitats in Panama to analyze the effect of coral presence in mangrove habitats on the fish assemblage. Our study revealed that CMC habitats harbor distinct fish assemblages compared to mangrove habitats without coral, with greater species richness and increased herbivore abundance. Abstract in Spanish is available with online material.     

Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa

Large-scale coral bleaching episodes are potentially major disturbances to coral reef systems, yet a definitive picture of variation in assemblage response and species susceptibilities is still being compiled. Here, we provide a detailed analysis of the bleaching response of 4160 coral colonies, representing 45 genera and 15 families, from two depths at four sites on reefs fringing inshore islands on the Great Barrier Reef. Six weeks after the onset of large-scale bleaching in 1998, between 11 and 83% of colonies along replicate transects were affected by bleaching, and mortality was 1 to 16%. There were significant differences in bleaching response between sites, depths and taxa. Cyphastrea, Turbinaria and Galaxea were relatively unaffected by bleaching, while most acroporids and pocilloporids were highly susceptible. The hydrocorals (Millepora spp.) were the most susceptible taxa, with 85% mortality. Spatial variation in assemblage response was linked to the taxonomic composition of reef sites and their bleaching history. We suggest, therefore, that much of the spatial variation in bleaching response was due to assemblage composition and thermal acclimation. Accepted: 14 January 2000     

Effects of habitat,wave exposure,and marine protected area status on coral reef fish assemblages in the Hawaiian archipelago

The relationships between fish assemblages, their associated habitat, and degree of protection from fishing were evaluated over a broad spatial scale throughout the main Hawaiian islands. Most fish assemblage characteristics showed positive responses to protection whether it was physical (e.g. habitat complexity), biological (e.g. coral cover growth forms), or human-induced (e.g. marine reserves). Fish biomass was lowest in areas of direct wave exposure and highest in areas partially sheltered from swells. Higher values for fish species richness, number of individuals, biomass, and diversity were observed in locations with higher substrate complexity. Areas completely protected from fishing had distinct fish assemblages with higher standing stock and diversity than areas where fishing was permitted or areas that were partially protected from fishing. Locations influenced by customary stewardship harbored fish biomass that was equal to or greater than that of no-take protected areas. Marine protected areas in the main Hawaiian islands with high habitat complexity, moderate wave disturbance, a high percentage of branching and/or lobate coral coupled with legal protection from fishing pressure had higher values for most fish assemblage characteristics.     

Taxonomic patterns of bleaching within a South African coral assemblage

In 1998, the Indian Ocean coral reefs suffered a severe and extensive mass bleaching event. The thermal tolerances of corals were exceeded and their photosynthetic symbionts (zooxanthellae) lost. Mortalities of up to 90% were recorded on the reefs of Seychelles, Maldives, Kenya and Tanzania. South African coral reefs were among the few that largely escaped the 1998 mass bleaching event, but may be threatened in the future if global warming increases. This study assessed the extent of coral bleaching and partial recovery at Sodwana Bay, South Africa during 2000 and 2001. Bleaching levels in this study varied over the course of a year, which suggested that seasonally varying parameters such as sea temperature were the most likely cause of bleaching. Bleaching levels were highest at the shallowest site. However, these bleaching levels were very low in comparison with those of reefs elsewhere in the Indian Ocean. The greater volume of water over the relatively deeper reefs of Sodwana Bay may have protected the reefs from severe bleaching. Field measurements on the three reefs indicated that, although the reefs at Sodwana Bay are still healthy, bleaching increased from <1% in 1998 to 5–10% in 2002. Bleaching occurred in 26 coral genera. The Alcyonacea were highly susceptible to bleaching, especially Sarcophyton sp. Among the hard corals, Montipora spp. were the species most susceptible to bleaching. The sensitivity of these genera to early and slight increases in temperature suggests that they can forewarn of a possible greater bleaching event. In contrast, the coral genera Turbinaria and Stylophora were most resistant to bleaching.     

Corals escape bleaching in regions that recently and historically experienced frequent thermal stress

The response of coral-reef ecosystems to contemporary thermal stress may be in part a consequence of recent or historical sea-surface temperature (SST) variability. To test this hypothesis, we examined whether: (i) there was a relationship between the historical frequency of SST variability and stress experienced during the most recent thermal-stress events (in 1998 and 2005–2006) and (ii) coral reefs that historically experienced frequent thermal anomalies were less likely to experience coral bleaching during these recent thermal-stress events. Examination of nine detrended coral δ¹⁸O and Sr/Ca anomaly records revealed a high- (5.7-year) and low-frequency (>54-year) mode of SST variability. There was a positive relationship between the historical frequency of SST anomalies and recent thermal stress; sites historically dominated by the high-frequency mode experienced greater thermal stress than other sites during both events, and showed extensive coral bleaching in 1998. Nonetheless, in 2005–2006, corals at sites dominated by high-frequency variability showed reduced bleaching, despite experiencing high thermal stress. This bleaching resistance was most likely a consequence of rapid directional selection that followed the extreme thermal event of 1998. However, the benefits of regional resistance could come at the considerable cost of shifts in coral species composition.