Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

Region‐wide temporal and spatial variation in Caribbean reef architecture: is coral cover the whole story?

The architectural complexity of coral reefs is largely generated by reef‐building corals, yet the effects of current regional‐scale declines in coral cover on reef complexity are poorly understood. In particular, both the extent to which declines in coral cover lead to declines in complexity and the length of time it takes for reefs to collapse following coral mortality are unknown. Here we assess the extent of temporal and spatial covariation between coral cover and reef architectural complexity using a Caribbean‐wide dataset of temporally replicated estimates spanning four decades. Both coral cover and architectural complexity have declined rapidly over time, with little evidence of a time‐lag. However, annual rates of change in coral cover and complexity do not covary, and levels of complexity vary greatly among reefs with similar coral cover. These findings suggest that the stressors influencing Caribbean reefs are sufficiently severe and widespread to produce similar regional‐scale declines in coral cover and reef complexity, even though reef architectural complexity is not a direct function of coral cover at local scales. Given that architectural complexity is not a simple function of coral cover, it is important that conservation monitoring and restoration give due consideration to both architecture and coral cover. This will help ensure that the ecosystem services supported by architectural complexity, such as nutrient recycling, dissipation of wave energy, fish production and diversity, are maintained and enhanced.     

The influence of coral reef benthic condition on associated fish assemblages

Accumulative disturbances can erode a coral reef's resilience, often leading to replacement of scleractinian corals by macroalgae or other non-coral organisms. These degraded reef systems have been mostly described based on changes in the composition of the reef benthos, and there is little understanding of how such changes are influenced by, and in turn influence, other components of the reef ecosystem. This study investigated the spatial variation in benthic communities on fringing reefs around the inner Seychelles islands. Specifically, relationships between benthic composition and the underlying substrata, as well as the associated fish assemblages were assessed. High variability in benthic composition was found among reefs, with a gradient from high coral cover (up to 58%) and high structural complexity to high macroalgae cover (up to 95%) and low structural complexity at the extremes. This gradient was associated with declining species richness of fishes, reduced diversity of fish functional groups, and lower abundance of corallivorous fishes. There were no reciprocal increases in herbivorous fish abundances, and relationships with other fish functional groups and total fish abundance were weak. Reefs grouping at the extremes of complex coral habitats or low-complexity macroalgal habitats displayed markedly different fish communities, with only two species of benthic invertebrate feeding fishes in greater abundance in the macroalgal habitat. These results have negative implications for the continuation of many coral reef ecosystem processes and services if more reefs shift to extreme degraded conditions dominated by macroalgae.     

Spatial dynamics of benthic competition on coral reefs

The community structure of sedentary organisms is largely controlled by the outcome of direct competition for space. Understanding factors defining competitive outcomes among neighbors is thus critical for predicting large-scale changes, such as transitions to alternate states within coral reefs. Using a spatially explicit model, we explored the importance of variation in two spatial properties in benthic dynamics on coral reefs: (1) patterns of herbivory are spatially distinct between fishes and sea urchins and (2) there is wide variation in the areal extent into which different coral species can expand. We reveal that the size-specific, competitive asymmetry of corals versus fleshy algae highlights the significance of spatial patterning of herbivory and of coral growth. Spatial dynamics that alter the demographic importance of coral recruitment and maturation have profound effects on the emergent structure of the reef benthic community. Spatially constrained herbivory (as by sea urchins) is more effective than spatially unconstrained herbivory (as by many fish) at opening space for the time needed for corals to settle and to recruit to the adult population. Further, spatially unconstrained coral growth (as by many branching coral species) reduces the number of recruitment events needed to fill a habitat with coral relative to more spatially constrained growth (as by many massive species). Our model predicts that widespread mortality of branching corals (e.g., Acropora spp) and herbivorous sea urchins (particularly Diadema antillarum) in the Caribbean has greatly reduced the potential for restoration across the region.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Competition between herbivourous fishes and urchins on Caribbean reefs

Summary When the common sea urchin Diadema antillarum was removed from a 50 m strip of reef in St. Thomas, US Virgin Islands, cover of upright algae and the grazing rates and densities of herbivorous parrotfish and surgeonfish increased significantly within 11–16 weeks when compared to immediately adjacent control areas. Sixteen months after removal, Diadema had recovered to 70% of original density, abundance of upright algae no longer differed between removal and control areas, and the abundance and grazing activity of herbivorous fish in the removal was approaching equivalence with control areas. On a patch reef in St. Croix that had been cleared of Diadema 10–11 years earlier (Ogden et al. 1973b), urchins had recovered to only 50–60% of original density. This reef still showed significantly higher rates of grazing by fish and a significantly greater density of parrotfish and surgeonfish than a nearby control reef where Diadema densities had not been altered. These results indicate that high Diadema densities (7–12/m² for this study) may suppress the densities of herbivorous fish on Caribbean reefs.     

Shifting ecological baselines and the demise of Acropora cervicornis in the western North Atlantic and Caribbean Province: a Pleistocene perspective

 In recent years, marine scientists have become increasingly alarmed over the decline of live coral cover throughout the Caribbean and tropical western Atlantic region. The Holocene and Pleistocene fossil record of coral reefs from this region potentially provides a wealth of long-term ecologic information with which to assess the historical record of changes in shallow water coral reef communities. Before fossil data can be applied to the modern reef system, critical problems involving fossil preservation must be addressed. Moreover, it must be demonstrated that the classic reef coral zonation patterns described in the early days of coral reef ecology, and upon which “healthy” versus “unhealthy” reefs are determined, are themselves representative of reefs that existed prior to any human influence. To address these issues, we have conducted systematic censuses of life and death assemblages on modern “healthy” patch reefs in the Florida reef tract that conform to the classic Caribbean model of reef coral zonation, and a patch reef in the Bahamas that is currently undergoing a transition in coral dominance that is part of a greater Caribbean-wide phenomenon. Results were compared to censuses of ancient reef assemblages preserved in Pleistocene limestones in close proximity to each modern reef. We have determined that the Pleistocene fossil record of coral reefs may be used to calibrate an ecological baseline with which to compare modern reef assemblages, and suggest that the current and rapid decline of Acropora cervicornis observed on a Bahamian patch reef may be a unique event that contrasts with the long-term persistence of this taxon during Pleistocene and Holocene time. Accepted: 19 May 1998     

Structure of Caribbean coral reef communities across a large gradient of fish biomass

The collapse of Caribbean coral reefs has been attributed in part to historic overfishing, but whether fish assemblages can recover and how such recovery might affect the benthic reef community has not been tested across appropriate scales. We surveyed the biomass of reef communities across a range in fish abundance from 14 to 593 g m⁻², a gradient exceeding that of any previously reported for coral reefs. Increased fish biomass was correlated with an increased proportion of apex predators, which were abundant only inside large marine reserves. Increased herbivorous fish biomass was correlated with a decrease in fleshy algal biomass but corals have not yet recovered.     

Habitat-dependent growth in a Caribbean sea urchin <Emphasis Type="Italic">Tripneustes ventricosus</Emphasis>: the importance of food type

The sea urchin Tripneustes ventricosus is a common, yet relatively poorly known, grazer of seagrass beds and coral reefs throughout the Caribbean. We compared the size and abundance of urchins between adjacent seagrass and coral reef habitats (where macroalgae are the dominant primary producers). We also conducted a laboratory experiment comparing the growth rate of juvenile urchins fed a diet of either macroalgae or seagrass. Reef urchins had significantly larger test diameter than those in the seagrass on some sampling dates. This size difference may be at least partially explained by diet, because laboratory-reared urchins fed macroalgae grew significantly faster than those fed seagrass. The seagrass population, however, was stable over time, whereas the reef population exhibited strong fluctuations in abundance. Overall, our study indicates that both the seagrass and coral reef habitats are capable of supporting healthy, reproductive populations of T. ventricosus. Each, however, appears to offer a distinct advantage: faster growth on the reef and greater population stability in the seagrass.     

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.     

Changing dynamics of Caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential

Coral cover has declined rapidly on Caribbean reefs since the early 1980s, reducing carbonate production and reef growth. Using a cross-regional dataset, we show that widespread reductions in bioerosion rates—a key carbonate cycling process—have accompanied carbonate production declines. Bioerosion by parrotfish, urchins, endolithic sponges and microendoliths collectively averages 2 G (where G = kg CaCO₃ m⁻² yr⁻¹) (range 0.96–3.67 G). This rate is at least 75% lower than that reported from Caribbean reefs prior to their shift towards their present degraded state. Despite chronic overfishing, parrotfish are the dominant bioeroders, but erosion rates are reduced from averages of approximately 4 to 1.6 G. Urchin erosion rates have declined further and are functionally irrelevant to bioerosion on most reefs. These changes demonstrate a fundamental shift in Caribbean reef carbonate budget dynamics. To-date, reduced bioerosion rates have partially offset carbonate production declines, limiting the extent to which more widespread transitions to negative budget states have occurred. However, given the poor prognosis for coral recovery in the Caribbean and reported shifts to coral community states dominated by slower calcifying taxa, a continued transition from production to bioerosion-controlled budget states, which will increasingly threaten reef growth, is predicted.     

Drivers of region-wide declines in architectural complexity on Caribbean reefs

Severe declines in the cover of live hard coral on reefs have been reported worldwide, and in the Caribbean region, the architectural complexity of coral reefs has also declined markedly. While the drivers of coral cover loss are relatively well understood, little is known about the drivers of regional-scale declines in architectural complexity. We have used a dataset of 49 time series reporting reef architectural complexity to explore the effect of hurricanes, coral bleaching and fishing on Caribbean-wide annual rates of change in reef complexity. Hurricane impacts greatly influence reef complexity, with the most rapid rates of decline in complexity occurring at sites impacted during their survey period, and with lower rates of loss occurring at unimpacted sites. Reef architectural complexity did not change significantly following mass bleaching events (in a time frame of <5 years) or positive thermal anomalies. Although the rates of change in architectural complexity were similar in and out of marine protected areas (MPAs), significant declines in complexity were observed inside but not outside of MPAs, possibly because reductions in fishing can lead to increased bioerosion by herbivores within MPAs. Our findings suggest that major drivers of coral mortality, such as coral bleaching, do not influence reef architectural complexity in the short term (<5 years). Instead, direct physical impacts and reef bioerosion appear to be important drivers of the widespread loss of architecturally complex reefs in the Caribbean.     

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.     

Maintenance of fish diversity on disturbed coral reefs

Habitat perturbations play a major role in shaping community structure; however, the elements of disturbance-related habitat change that affect diversity are not always apparent. This study examined the effects of habitat disturbances on species richness of coral reef fish assemblages using annual surveys of habitat and 210 fish species from 10 reefs on the Great Barrier Reef (GBR). Over a period of 11 years, major disturbances, including localised outbreaks of crown-of-thorns sea star (Acanthaster planci), severe storms or coral bleaching, resulted in coral decline of 46–96% in all the 10 reefs. Despite declines in coral cover, structural complexity of the reef framework was retained on five and species richness of coral reef fishes maintained on nine of the disturbed reefs. Extensive loss of coral resulted in localised declines of highly specialised coral-dependent species, but this loss of diversity was more than compensated for by increases in the number of species that feed on the epilithic algal matrix (EAM). A unimodal relationship between areal coral cover and species richness indicated species richness was greatest at approximately 20% coral cover declining by 3–4 species (6–8% of average richness) at higher and lower coral cover. Results revealed that declines in coral cover on reefs may have limited short-term impact on the diversity of coral reef fishes, though there may be fundamental changes in the community structure of fishes.     

Factors influencing spatial distribution of fish communities on a fringing reef at Mauritius, S.W. Indian Ocean

This paper analyses the spatial patterns of fish communities on a narrow fringing reef of Mauritius and identifies some controlling factors. Canonical Correspondence Analysis revealed that the location in the reef ecosystem, the living coral coverage, and the proximity to a dredged area were the major factors controlling the distribution and abundance of fish species. Two distinct communities were observed across the fringing reef, representing a land-ocean gradient. The low diversity of fish species, and also of invertebrates such as corals, molluscs, and echinoderms is probably a consequence of the narrowness of the fringing reef and of anthropogenic impacts, notably the high pollution by nutrients.     

Spatial patterns of Yucatan reef fish communities: Testing models using a multi-scale survey design

Using a hierarchical multi-scale survey design, we examined the spatial patterns of reef fish communities and tested ecological models concerning the relative importance of reef geomorphology and anthropogenic pressure possibly driving community structure. Canonical redundancy analysis was used as a form of multivariate analysis of variance (MANOVA) to asses differences in reef fish community composition at two spatial scales: broad (10⁵ m) and intermediate (10⁴ m). Surveys were conducted on the east coast of the Yucatan Peninsula (Mexican Caribbean fringing reef), including regions and reefs which differed in geomophologic structure and human use. Seven hundred and fourteen line transects were distributed among 13 reef localities belonging to different regions established a priori. Transects covered four types of reef habitat: lagoon, front, slope, and terrace. Tests of significance were based on permutation procedures. Significant differences among regions were found for the lagoon, slope, and terrace fish communities, consistent with the geomorphologic model, but it is only in the reef lagoon that they were consistent with the anthropogenic model, which may indicate an effect of coastal human activities. Significant differences among reefs within regions were observed, which could be associated with local environmental gradients. Canonical nested MANOVA was an appropriate method for testing ecological hypotheses about the functioning of complex biological systems. The use of a surveying strategy that explicitly incorporated the spatial structure represents an important contribution of this paper to coral reef fish ecology.     

Context-Dependent Diversity-Effects of Seaweed Consumption on Coral Reefs in Kenya

Consumers and prey diversity, their interactions, and subsequent effects on ecosystem function are important for ecological processes but not well understood in high diversity ecosystems such as coral reefs. Consequently, we tested the potential for diversity-effects with a series of surveys and experiments evaluating the influence of browsing herbivores on macroalgae in Kenya’s fringing reef ecosystem. We surveyed sites and undertook experiments in reefs subject to three levels of human fishing influence: open access fished reefs, small and recently established community-managed marine reserves, and larger, older government-managed marine reserves. Older marine reserves had a greater overall diversity of herbivores and browsers but this was not clearly associated with reduced macroalgal diversity or abundance. Experiments studying succession on hard substrata also found no effects of consumer diversity. Instead, overall browser abundance of either sea urchins or fishes was correlated with declines in macroalgal cover. An exception was that the absence of a key fish browser genus, Naso, which was correlated with the persistence of Sargassum in a marine reserve. Algal selectivity assays showed that macroalgae were consumed at variable rates, a product of strong species-specific feeding and low overlap in the selectivity of browsing fishes. We conclude that the effects of browser and herbivore diversity are less than the influences of key species, whose impacts emerge in different contexts that are influenced by fisheries management. Consequently, identifying key herbivore species and managing to protect them may assist protecting reef functions.     

The role of turtles as coral reef macroherbivores

Herbivory is widely accepted as a vital function on coral reefs. To date, the majority of studies examining herbivory in coral reef environments have focused on the roles of fishes and/or urchins, with relatively few studies considering the potential role of macroherbivores in reef processes. Here, we introduce evidence that highlights the potential role of marine turtles as herbivores on coral reefs. While conducting experimental habitat manipulations to assess the roles of herbivorous reef fishes we observed green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) showing responses that were remarkably similar to those of herbivorous fishes. Reducing the sediment load of the epilithic algal matrix on a coral reef resulted in a forty-fold increase in grazing by green turtles. Hawksbill turtles were also observed to browse transplanted thalli of the macroalga Sargassum swartzii in a coral reef environment. These responses not only show strong parallels to herbivorous reef fishes, but also highlight that marine turtles actively, and intentionally, remove algae from coral reefs. When considering the size and potential historical abundance of marine turtles we suggest that these potentially valuable herbivores may have been lost from many coral reefs before their true importance was understood.     

亚龙湾珊瑚礁大型礁栖生物的群落结构及生态警示

鱼类和大型底栖生物等礁栖生物是珊瑚礁生态系统的重要组成部分,其群落信息是全面评价珊瑚礁生态系统健康状况的必要基础数据。基于录像样带法,分析了2018年12月底海南省三亚市亚龙湾珊瑚礁区17个站位礁栖鱼类和大型底栖生物的群落结构、数量分布及相似性,揭示了其中的生态警示,并提出相应的监管建议,旨在保护和恢复亚龙湾的珊瑚礁。结果表明:亚龙湾西岸及东排、西排共发现鱼类8科21属35种,以雀鲷科、隆头鱼科为主,平均密度为0.20尾·m^-2,金尾雀鲷、斑棘眶锯雀鲷和细鳞光鳃鱼为优势种;最近15年来,亚龙湾的鱼类资源持续衰退,目前已近于枯竭。另一方面,调查区的大型底栖生物以软珊瑚、大型底栖藻类、海百合和海胆为主,各类群的数量分布有所不同;造礁珊瑚的敌害生物小核果螺和长棘海星密度皆很低,目前尚不会对珊瑚礁构成威胁;整体而言,大型礁栖生物群落在亚龙湾西岸与东排、西排有较大的差异,间接反映出岛礁与岸礁环境存在差别,不过亚龙湾西岸湾口段的环境条件可能更接近岛礁;由于部分海区大型底栖藻类较多及可能存在的富营养化趋势,维持金尾雀鲷或其他植食性鱼类与藻类规模两者间的平衡,对恢复和保持亚龙湾珊瑚礁生态系统的健康尤为重要;同时,管控来自青梅河等的陆源污染,也是控制亚龙湾大型海藻增殖的关键;相比于海参,海百合对大型底栖藻类的依赖程度较低。调查区造礁珊瑚覆盖率与礁栖生物数量之间没有显著相关,可能与亚龙湾珊瑚礁退化严重及现存的种类以团块状造礁珊瑚为主,其构建的珊瑚礁生境空间异质性相对较低有关。为更好地保护亚龙湾的珊瑚礁,建议关注亚龙湾的水质,加强对捕鱼、潜水观光等旅游活动的监督管理,特别是应该立即实施长时间的渔业禁捕来恢复亚龙湾的渔业资源,并定期监控关键种群的数量变动。