Operationalizing resilience for adaptive coral reef management under global environmental change

Cumulative pressures from global climate and ocean change combined with multiple regional and local‐scale stressors pose fundamental challenges to coral reef managers worldwide. Understanding how cumulative stressors affect coral reef vulnerability is critical for successful reef conservation now and in the future. In this review, we present the case that strategically managing for increased ecological resilience (capacity for stress resistance and recovery) can reduce coral reef vulnerability (risk of net decline) up to a point. Specifically, we propose an operational framework for identifying effective management levers to enhance resilience and support management decisions that reduce reef vulnerability. Building on a system understanding of biological and ecological processes that drive resilience of coral reefs in different environmental and socio‐economic settings, we present an Adaptive Resilience‐Based management (ARBM) framework and suggest a set of guidelines for how and where resilience can be enhanced via management interventions. We argue that press‐type stressors (pollution, sedimentation, overfishing, ocean warming and acidification) are key threats to coral reef resilience by affecting processes underpinning resistance and recovery, while pulse‐type (acute) stressors (e.g. storms, bleaching events, crown‐of‐thorns starfish outbreaks) increase the demand for resilience. We apply the framework to a set of example problems for Caribbean and Indo‐Pacific reefs. A combined strategy of active risk reduction and resilience support is needed, informed by key management objectives, knowledge of reef ecosystem processes and consideration of environmental and social drivers. As climate change and ocean acidification erode the resilience and increase the vulnerability of coral reefs globally, successful adaptive management of coral reefs will become increasingly difficult. Given limited resources, on‐the‐ground solutions are likely to focus increasingly on actions that support resilience at finer spatial scales, and that are tightly linked to ecosystem goods and services.     

Mechanical vulnerability explains size‐dependent mortality of reef corals

Understanding life history and demographic variation among species within communities is a central ecological goal. Mortality schedules are especially important in ecosystems where disturbance plays a major role in structuring communities, such as coral reefs. Here, we test whether a trait‐based, mechanistic model of mechanical vulnerability in corals can explain mortality schedules. Specifically, we ask whether species that become increasingly vulnerable to hydrodynamic dislodgment as they grow have bathtub‐shaped mortality curves, whereas species that remain mechanically stable have decreasing mortality rates with size, as predicted by classical life history theory for reef corals. We find that size‐dependent mortality is highly consistent between species with the same growth form and that the shape of size‐dependent mortality for each growth form can be explained by mechanical vulnerability. Our findings highlight the feasibility of predicting assemblage‐scale mortality patterns on coral reefs with trait‐based approaches.     

A comparison of line transect versus linear percentage sampling for evaluating stony coral (Scleractinia andMilleporina) community similarity and area coverage on reefs of the central Bahamas

Three methods of evaluating stony coral communities were used on selected reefs in the Exuma Cays Land and Sea Park (24°22N, 77°30W) in the central Bahamas. Shallow reefs (< 4 meters depth) were selected from aerial surveys based on size, location, and physical setting, and grouped into three community types: (1) channel patch reefs, (2) soft-coral-sponge patch reefs and (3) fringing reefs. Three survey techniques used to evaluate the stony coral communities were a) species presence and absence lists, b) linear percentage and c) line transects using 1 mx1 m grids. Data collected from these survey methods was used to calculate coral colony density, species area coverage, and species diversity based on colony number and based on linear (cm) coral cover. The linear percentage sampling was considered too convervative in determining distribution patterns of a reef community; this technique takes into account the massive reef framework species such asM. annularis. The line transect technique can account for both colony number and area coverage, thus is a better method for characterizing reef communities. Sample size considerations are discussed for future applications of survey techniques for ground-truthing digital images of small, shallow reef communities.     

珊瑚礁生态脆弱性评价--以泰国思仓岛为例

珊瑚礁生态系统受到环境变化、人类活动等各种因素的严重威胁,保护珊瑚礁生态系统是目前全球海洋生态保护的热点,对珊瑚礁开展定量的生态脆弱性评估能够为保护管理对策的制定提供重要科学依据。本研究选取泰国思仓岛作为研究区域,结合空间分析技术建立了具有通用性的珊瑚礁生态脆弱性评估方法。基于ESA模型构建了珊瑚礁生态脆弱性综合指数和评价指标体系,系统分析了思仓岛珊瑚礁脆弱性的来源、构成,并直观展现了脆弱性的区域空间分布。结果表明:思仓岛研究区东北侧的珊瑚礁生态脆弱性大于西南侧,当地珊瑚礁的关键影响因子分别为驳船排污、港口码头、水体透明度等。根据脆弱性评价的结果,提出了当地珊瑚礁保护与修复的空间分区管理对策。本研究为印度-太平洋区系珊瑚礁生态脆弱性评价提供了可行的示例,也为中国的珊瑚礁可持续管理研究提供了借鉴和参照。     

Extinction vulnerability of coral reef fishes

With rapidly increasing rates of contemporary extinction, predicting extinction vulnerability and identifying how multiple stressors drive non-random species loss have become key challenges in ecology. These assessments are crucial for avoiding the loss of key functional groups that sustain ecosystem processes and services. We developed a novel predictive framework of species extinction vulnerability and applied it to coral reef fishes. Although relatively few coral reef fishes are at risk of global extinction from climate disturbances, a negative convex relationship between fish species locally vulnerable to climate change vs. fisheries exploitation indicates that the entire community is vulnerable on the many reefs where both stressors co-occur. Fishes involved in maintaining key ecosystem functions are more at risk from fishing than climate disturbances. This finding is encouraging as local and regional commitment to fisheries management action can maintain reef ecosystem functions pending progress towards the more complex global problem of stabilizing the climate.     

Comparisons of macrofaunal assemblages on restored and non-restored oyster reefs in mesohaline regions of Chesapeake Bay in Maryland

Maryland's recently created oyster restored reefs provide us with a unique opportunity to observe the abundance and species composition of macrofauna assemblages on unexploited reefs with high concentrations of mature oysters and undisturbed reef architecture. They might thus be used to better understand the magnitude of losses to reef dwelling macrofauna communities, and the associated loss of ecological functions resulting from reef destruction. We sampled reef macrofaunal assemblages on restored plots at four restored oyster reefs and adjacent non-restored plots located outside restored boundaries. We then compared the effects of study site location, and habitat quality (restored versus non-restored) on macrofaunal density using thirteen response variables. Density of macrofauna was an order of magnitude higher on restored reefs, epifaunal density was more than twice as high on restored reefs and sessile macrofaunal density was two orders of magnitude higher on restored reefs. Three out of the five dominant taxonomic groups were much more abundant on restored plots. Mean amphipod density was 20 times higher on restored plots and densities of xanthid crabs and demersal fish were both four times greater on restored plots. Two out of four functional feeding groups: suspension feeders and carnivore/omnivores, were more abundant on restored plots. Since reef macrofauna include many important fish prey species, oyster reef restoration may have the potential to augment fish production by increasing fish prey densities and fish foraging efficiency.     

Passive colonization and asexual colony multiplication in the massive coral Porites lutea Milne Edwards & Haime

Heads of the reef-building coral Porites lutea Milne Edwards & Haime are occasionally separated or torn loose from the substratum by bioerosion or mechanical stresses. Detached heads may survive and colonize down-slope or down-stream soft bottoms, forming incipient reefs in habitats unsuitable for colonization by larval settlement. One important result of this process is reef consolidation and growth on the lagoonward edge of truncated, inter-island reef flats on atolls. In some cases, portions of the detached colonies remain attached at the original site; thus there is asexual colony multiplication.     

The influence of prey communities on fish species assemblages on artificial reefs in Puget Sound,Washington

Synopsis Research on eleven artificial reefs in Puget Sound, Washington examined the relative importance of reef-produced prey items to recreationally important reef fish species assemblages. The colonization of potential prey items, and fish species assemblages to ten artificial reefs were examined for the reefs first two to five years, and observations were conducted on an eleventh reef during its forty-ninth productive year. Fish species became more abundant, or were seen more frequently on reef habitats whose substrates had successionally developed from barnalces to algal mats. Fish species most affected by this successional change foraged heavily on organisms which were associated with reef algae. Starfish and nudibranchs. who preyed on the barnacles, were identified as the ‘keystone’ predators of these subtidal reef habitats.     

Ecological structure of assemblages of coral reef fishes on isolated patch reefs

A 9-year study of the structure of assemblages of fish on 20 coral patch reefs, based on 20 non-manipulative censuses, revealed a total of 141 species from 34 families, although 40 species accounted for over 95% of sightings of fish. The average patch reef was 8.5 m² in surface area, and supported 125 fish of 20 species at a census. All reefs showed at least a two-fold variation among censuses in total numbers of fish present, and 12 showed ten-fold variations. There was also substantial variation in the composition and relative abundances of species present on each patch reef, such that censuses of a single patch reef were on average about 50% different from each other in percent similarity of species composition (Czekanowski's index). Species differed substantially in the degree to which their numbers varied from census to census, and in the degree to which their dispersion among patch reefs was modified from census to census. We characterize the 40 most common species with respect to these attributes. The variations in assemblage structure cannot be attributed to responses of fish to a changing physical structure of patch reefs, nor to the comings and goings of numerous rare species. Our results support and extend earlier reports on this study, which have stressed the lack of persistant structure for assemblages on these patch reefs. While reef fishes clearly have microhabitat preferences which are expressed at settlement, the variations in microhabitat offered by the patch reefs are insufficient to segregate many species of fish by patch reef. Instead, at the scale of single patch reefs, and, to a degree, at the larger scale of the 20 patch reefs, most of the 141 species of fish are distributed without regard to differences in habitat structure among reefs, and patterns of distribution change over time. Implications for general understanding of assemblage dynamics for fish over more extensive patches of reef habitat are considered.     

Population Structure of Montastraea cavernosa on Shallow versus Mesophotic Reefs in Bermuda

Mesophotic coral reef ecosystems remain largely unexplored with only limited information available on taxonomic composition, abundance and distribution. Yet, mesophotic reefs may serve as potential refugia for shallow-water species and thus understanding biodiversity, ecology and connectivity of deep reef communities is integral for resource management and conservation. The Caribbean coral, Montastraea cavernosa, is considered a depth generalist and is commonly found at mesophotic depths. We surveyed abundance and size-frequency of M. cavernosa populations at six shallow (10m) and six upper mesophotic (45m) sites in Bermuda and found population structure was depth dependent. The mean surface area of colonies at mesophotic sites was significantly smaller than at shallow sites, suggesting that growth rates and maximum colony surface area are limited on mesophotic reefs. Colony density was significantly higher at mesophotic sites, however, resulting in equal contributions to overall percent cover. Size-frequency distributions between shallow and mesophotic sites were also significantly different with populations at mesophotic reefs skewed towards smaller individuals. Overall, the results of this study provide valuable baseline data on population structure, which indicate that the mesophotic reefs of Bermuda support an established population of M. cavernosa.     

Boring sponges,an increasing threat for coral reefs affected by bleaching events

Coral bleaching is a stress response of corals induced by a variety of factors, but these events have become more frequent and intense in response to recent climate‐change‐related temperature anomalies. We tested the hypothesis that coral reefs affected by bleaching events are currently heavily infested by boring sponges, which are playing a significant role in the destruction of their physical structure. Seventeen reefs that cover the entire distributional range of corals along the Mexican Pacific coast were studied between 2005/2006, and later between 2009/2010. Most of these coral reefs were previously impacted by bleaching events, which resulted in coral mortalities. Sponge abundance and species richness was used as an indicator of bioerosion, and coral cover was used to describe the present condition of coral reefs. Coral reefs are currently highly invaded (46% of the samples examined) by a very high diversity of boring sponges (20 species); being the coral reef framework the substrate most invaded (56%) followed by the rubbles (45%), and the living colonies (36%). The results also indicated that boring sponges are promoting the dislodgment of live colonies and large fragments from the framework. In summary, the eastern coral reefs affected by bleaching phenomena, mainly provoked by El Niño, present a high diversity and abundance of boring sponges, which are weakening the union of the colony with the reef framework and promoting their dislodgment. These phenomena will probably become even more intense and severe, as temperatures are projected to continue to rise under the scenarios for future climate change, which could place many eastern coral reefs beyond their survival threshold.     

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change.     

Hurricanes and coral reefs: The intermediate disturbance hypothesis revisited

A review of research on the effects of hurricanes on coral reefs suggests that the intermediate disturbance hypothesis may be applicable to shallow reef zones dominated by branching or foliaceous coral species that are especially susceptible to mechanical damage from storms. Diversity (H') increases because of an increase in evenness following destruction or removal of the species that was monopolizing the space. The intermediate disturbance hypothesis as presented by Connell focuses on changes in number of species, but should be expanded to include diversity (H') and evenness. It should also be modified to incorporate changes in living cover and the time elapsed since disturbances of varying intensities. This hypothesis predicts that when cover is high, diversity will be low. However, research on coral reefs does not consistently demonstrate an inverse correlation of coral diversity, and coral cover. An increase in cover and decrease in diversity with depth would also be expected because deeper reef zones generally experience less disturbance. However, higher diversity (both H' and species richness) is often associated with deeper zones. The effects of hurricanes on coral reefs will depend on the temporal and spatial scales under consideration, the life history characteristics and morphology of the dominant species, the depth of the reef zone, the ecological history of the site, and the influence of any additional natural or human stresses.     

Extreme spatial heterogeneity in carbonate accretion potential on a Caribbean fringing reef linked to local human disturbance gradients

The capacity of coral reefs to maintain their structurally complex frameworks and to retain the potential for vertical accretion is vitally important to the persistence of their ecological functioning and the ecosystem services they sustain. However, datasets to support detailed along‐coast assessments of framework production rates and accretion potential do not presently exist. Here, we estimate, based on gross bioaccretion and bioerosion measures, the carbonate budgets and resultant estimated accretion rates (EAR) of the shallow reef zone of leeward Bonaire – between 5 and 12 m depth – at unique fine spatial resolution along this coast (115 sites). Whilst the fringing reef of Bonaire is often reported to be in a better ecological condition than most sites throughout the wider Caribbean region, our data show that the carbonate budgets of the reefs and derived EAR varied considerably across this ~58 km long fringing reef complex. Some areas, in particular the marine reserves, were indeed still dominated by structurally complex coral communities with high net carbonate production (>10 kg CaCO₃ m^?2 year^?1), high live coral cover and complex structural topography. The majority of the studied sites, however, were defined by relatively low budget states (<2 kg CaCO₃ m^?2 year^?1) or were in a state of net erosion. These data highlight the marked spatial heterogeneity that can occur in budget states, and thus in reef accretion potential, even between quite closely spaced areas of individual reef complexes. This heterogeneity is linked strongly to the degree of localized land‐based impacts along the coast, and resultant differences in the abundance of reef framework building coral species. The major impact of this variability is that those sections of reef defined by low‐accretion rates will have limited capacity to maintain their structural integrity and to keep pace with current projections of climate change induced sea‐level rise (SLR), thus posing a threat to reef functioning and biodiversity, potentially leading to trophic cascades. Since many Caribbean reefs are more severely degraded than those found around Bonaire, it is to be expected that the findings presented here are rather the rule than the exception, but the study also highlights the need for similar high spatial resolution (along‐coast) assessments of budget states and accretion rates to meaningfully explore increasing coastal risk at the country level. The findings also more generally underline the significance of reducing local anthropogenic disturbance and restoring framework building coral assemblages. Appropriately focussed local preservation efforts may aid in averting future large‐scale above reef water depth increases on Caribbean coral reefs and will limit the social and economic implications associated with the loss of reef goods and services.     

The influence of colony size and coral health on the occupation of coral-associated gobies (Pisces: Gobiidae)

Fishes of the genus Gobiodon are habitat specialists by their association with Acropora corals. Little is known about the parameters that define host coral quality for these fishes, in particular their breeding pairs. Data were collected in the northern Red Sea using 10 × 1-m belt transects in different reefs and zones. Gobiid density was highly correlated with coral density over all sites and zones, and the more specialized goby species preferred coral species that are less vulnerable to environmental stress. Moreover, the occupation rate of corals by goby breeding pairs significantly increased with colony size and decreased with partial mortality of colonies. Logistic regression showed that both coral size (being most important) and partial mortality are key factors influencing the occupation by breeding pairs. This study provides the first evidence that breeding pairs of coral-associated gobiids have more advanced habitat requirements than con-specifics in other social states. As coral reefs are threatened worldwide and habitat loss and degradation increase, this information will help predict the potential effects on those reef fishes obligatorily associated with live corals.     

Higher species richness of octocorals in the upper mesophotic zone in Eilat (Gulf of Aqaba) compared to shallower reef zones

Mesophotic coral-reef ecosystems (MCEs), which comprise the light-dependent communities of corals and other organisms found at depths between 30 and ~ 150 m, have received very little study to date. However, current technological advances, such as remotely operated vehicles and closed-circuit rebreather diving, now enable their thorough investigation. Following the reef-building stony corals, octocorals are the second most common benthic component on many shallow reefs and a major component on deep reefs, the Red Sea included. This study is the first to examine octocoral community features on upper MCEs based on species-level identification and to compare them with the shallower reef zones. The study was carried out at Eilat (Gulf of Aqaba, northern Red Sea), comparing octocoral communities at two mesophotic reefs (30–45 m) and two shallow reef zones (reef flat and upper fore-reef) by belt transects. A total of 30 octocoral species were identified, with higher species richness on the upper MCEs compared to the shallower reefs. Although the MCEs were found to host a higher number of species than the shallower reefs, both featured a similar diversity. Each reef zone revealed a unique octocoral species composition and distinct community structure, with only 16% of the species shared by both the MCEs and the shallower reefs. This study has revealed an almost exclusive dominance of zooxanthellate species at the studied upper MCE reefs, thus indicating an adequate light regime for photosynthesis there. The findings should encourage similar studies on other reefs, aimed at understanding the spatiotemporal features and ecological role of octocorals in reef ecosystems down to the deepest limit of the MCEs.     

The relationship between habitat structure and fish faunas on New Zealand reefs

Reef fish abundances were sampled at 11 shallow reef localities extending over 1000 km of coastline in northern New Zealand. Sampling was restricted to the 4–10-m depth stratum and included six coastal and five island localities. These were either coralline reef flats dominated by echinoids, or algal reefs with high densities of laminarian and fucoid algae. Reefs dominated by macroscopic algae supported large numbers of small fishes, mainly labrids, and few large benthic-feeding fishes. Echinoid-dominated reefs supported a different fish fauna with more large benthic-feeding species. Additional sampling of echinoiddominated reefs and algal stands in deeper water provided confirmation of these findings. A second sampling programme was carried out at a series of eight sites within a single locality covering 5 km of coastline. These spanned a moderate exposure gradient and ranged from algal dominated reefs to typical coralline reef flats with high densities of grazing invertebrates. The relationship between habitat structure and reef fish species composition and size frequency was similar to that of the large-scale sampling programme. Thirdly, observations on reef fish foraging and feeding patterns within a single reef site suggested that larger benthic-feeding reef fishes were less likely to feed within macroscopic algal stands. Experimental reductions of grazing invertebrates designed to produce brown algal stands on echinoid-dominated reef flats supported these observations. Larger individuals capable of removing echinoids and grazing gastropods did not frequent or feed in laminarian and fucoid algal stands. This pattern is discernible at several spatial scales. Our conclusion is that the type of shallow reef habitat, echinoid- as opposed to algal-dominated, will have an important rôle in determining the associated reef fish fauna.     

Ocean acidification and warming will lower coral reef resilience

Ocean warming and acidification from increasing levels of atmospheric CO₂ represent major global threats to coral reefs, and are in many regions exacerbated by local‐scale disturbances such as overfishing and nutrient enrichment. Our understanding of global threats and local‐scale disturbances on reefs is growing, but their relative contribution to reef resilience and vulnerability in the future is unclear. Here, we analyse quantitatively how different combinations of CO₂ and fishing pressure on herbivores will affect the ecological resilience of a simplified benthic reef community, as defined by its capacity to maintain and recover to coral‐dominated states. We use a dynamic community model integrated with the growth and mortality responses for branching corals (Acropora) and fleshy macroalgae (Lobophora). We operationalize the resilience framework by parameterizing the response function for coral growth (calcification) by ocean acidification and warming, coral bleaching and mortality by warming, macroalgal mortality by herbivore grazing and macroalgal growth via nutrient loading. The model was run for changes in sea surface temperature and water chemistry predicted by the rise in atmospheric CO₂ projected from the IPCC's fossil‐fuel intensive A1FI scenario during this century. Results demonstrated that severe acidification and warming alone can lower reef resilience (via impairment of coral growth and increased coral mortality) even under high grazing intensity and low nutrients. Further, the threshold at which herbivore overfishing (reduced grazing) leads to a coral–algal phase shift was lowered by acidification and warming. These analyses support two important conclusions: Firstly, reefs already subjected to herbivore overfishing and nutrification are likely to be more vulnerable to increasing CO₂. Secondly, under CO₂ regimes above 450–500 ppm, management of local‐scale disturbances will become critical to keeping reefs within an Acropora‐rich domain.     

Characterization of the mesophotic reef fish community in south Florida,USA

The southeastern coast of Florida, USA supports a substantial recreational fishery, yet little is known of the coral reef ecosystem or fisheries resources past 50 m depth. Fish assemblages associated with low‐relief substrate and three vessel reefs between 50 and 120 m depth off southeast Florida were surveyed by remotely operated vehicles providing the first characterization of the mesophotic fish assemblages in the region. Two distinct assemblages were observed on low‐relief substrate and high‐relief vessel reefs. A total of 560 fishes of 42 species was recorded on 27 dives on low‐relief substrate, and 50 152 fishes of 65 species were recorded on 24 dives on three vessel reefs. Small planktivorous Anthiinae fishes and several economically valuable species were common on vessel reefs but rare on low‐relief substrate. Fish assemblages on vessel reefs more closely resembled those found at similar depths in high‐relief natural areas off east‐central Florida and the Gulf of Mexico than those associated with adjacent low‐relief habitat or nearby coral reef tracts. From a fisheries perspective, these results provide limited support to the hypothesis that in deep‐water regions with limited relief, vessel reefs may provide an opportunity to increase fish diversity and abundance by creating high‐relief habitat without compromising adjacent fish assemblages.     

Kenyan coral reef lagoon fish: effects of fishing,substrate complexity,and sea urchins

Population density, number of species, diversity, and species-area relationships of fish species in eight common coral reef-associated families were studied in three marine parks receiving total protection from fishing, four sites with unregulated fishing, and one reef which recently received protection from fishing (referred to as a transition reef). Data on coral cover, reef topographic complexity, and sea urchin abundance were collected and correlated with fish abundance and species richness. The most striking result of this survey is a consistent and large reduction in the population density and species richness of 5 families (surgeonfish, triggerfish, butterflyfish, angelfish, and parrotfish). Poor recovery of parrotfish in the transition reef, relative to other fish families, is interpreted as evidence for competitive exclusion of parrotfish by sea urchins. Reef substrate complexity is significantly associated with fish abundance and diversity, but data suggest different responses for protected versus fished reefs, protected reefs having higher species richness and numbers of individuals than unprotected reefs for the same reef complexity. Sea urchin abundance is negatively associated with numbers of fish and fish species but the interrelationship between sea urchins, substrate complexity, coral cover, and management make it difficult to attribute a set percent of variance to each factor-although fishing versus no fishing appears to be the strongest variable in predicting numbers of individuals and species of fish, and their community similarity. Localized species extirpation is evident for many species on fished reefs (for the sampled area of 1.0 ha). Fifty-two of 110 species found on protected reefs were not found on unprotected reefs.