Temporal changes in the sponge holobiont during the course of infection with Aplysina Red Band Syndrome

Coral Reefs - Diseases of marine organisms, including sponges on coral reefs, are being reported with increasing frequency worldwide. Aplysina Red Band Syndrome (ARBS) occurs across the Caribbean...     

Exploring Individual- to Population-Level Impacts of Disease on Coral Reef Sponges: Using Spatial Analysis to Assess the Fate,Dynamics, and Transmission of Aplysina Red Band Syndrome (ARBS)

Background

Marine diseases are of increasing concern for coral reef ecosystems, but often their causes, dynamics and impacts are unknown. The current study investigated the epidemiology of Aplysina Red Band Syndrome (ARBS), a disease affecting the Caribbean sponge Aplysina cauliformis, at both the individual and population levels. The fates of marked healthy and ARBS-infected sponges were examined over the course of a year. Population-level impacts and transmission mechanisms of ARBS were investigated by monitoring two populations of A. cauliformis over a three year period using digital photography and diver-collected data, and analyzing these data with GIS techniques of spatial analysis. In this study, three commonly used spatial statistics (Ripley’s K, Getis-Ord General G, and Moran’s Index) were compared to each other and with direct measurements of individual interactions using join-counts, to determine the ideal method for investigating disease dynamics and transmission mechanisms in this system. During the study period, Hurricane Irene directly impacted these populations, providing an opportunity to assess potential storm effects on A. cauliformis and ARBS.

Results

Infection with ARBS caused increased loss of healthy sponge tissue over time and a higher likelihood of individual mortality. Hurricane Irene had a dramatic effect on A. cauliformis populations by greatly reducing sponge biomass on the reef, especially among diseased individuals. Spatial analysis showed that direct contact between A. cauliformis individuals was the likely transmission mechanism for ARBS within a population, evidenced by a significantly higher number of contact-joins between diseased sponges compared to random. Of the spatial statistics compared, the Moran’s Index best represented true connections between diseased sponges in the survey area. This study showed that spatial analysis can be a powerful tool for investigating disease dynamics and transmission in a coral reef ecosystem.     

Extinction rate, historical population structure and ecological role of the Caribbean monk seal

The productivity and biomass of pristine coral reef ecosystems is poorly understood, particularly in the Caribbean where communities have been impacted by overfishing and multiple other stressors over centuries. Using historical data on the spatial distribution and abundance of the extinct Caribbean monk seal (Monachus tropicalis), this study reconstructs the population size, structure and ecological role of this once common predator within coral reef communities, and provides evidence that historical reefs supported biomasses of fishes and invertebrates up to six times greater than those found on typical modern Caribbean reefs. An estimated 233,000-338,000 monk seals were distributed among 13 colonies across the Caribbean. The biomass of reef fishes and invertebrates required to support historical seal populations was 732-1018 gm(-2) of reefs, which exceeds that found on any Caribbean reef today and is comparable with those measured in remote Pacific reefs. Quantitative estimates of historically dense monk seal colonies and their consumption rates on pristine reefs provide concrete data on the magnitude of decline in animal biomass on Caribbean coral reefs. Realistic reconstruction of these past ecosystems is critical to understanding the profound and long-lasting effect of human hunting on the functioning of coral reef ecosystems.     

Status and progress in coral reef disease research

Recent findings on the ecology, etiology and pathology of coral pathogens, host resistance mechanisms, previously unknown disease/syndromes and the global nature of coral reef diseases have increased our concern about the health and future of coral reef communities. Much of what has been discovered in the past 4 years is presented in this special issue. Among the significant findings, the role that various Vibrio species play in coral disease and health, the composition of the 'normal microbiota' of corals, and the possible role of viruses in the disease process are important additions to our knowledge. New information concerning disease resistance and vectors, variation in pathogen composition for both fungal diseases of gorgonians and black band disease across oceans, environmental effects on disease susceptibility and resistance, and temporal and spatial disease variations among different coral species is presented in a number of papers. While the Caribbean may still be the 'disease hot spot' for coral reefs, it is now clear that diseases of coral reef organisms have become a global threat to coral reefs and a major cause of reef deterioration.     

A clear human footprint in the coral reefs of the Caribbean

The recent degradation of coral reefs worldwide is increasingly well documented, yet the underlying causes remain debated. In this study, we used a large-scale database on the status of coral reef communities in the Caribbean and analysed it in combination with a comprehensive set of socioeconomic and environmental databases to decouple confounding factors and identify the drivers of change in coral reef communities. Our results indicated that human activities related to agricultural land use, coastal development, overfishing and climate change had created independent and overwhelming responses in fishes, corals and macroalgae. While the effective implementation of marine protected areas (MPAs) increased the biomass of fish populations, coral reef builders and macroalgae followed patterns of change independent of MPAs. However, we also found significant ecological links among all these groups of organisms suggesting that the long-term stability of coral reefs as a whole requires a holistic and regional approach to the control of human-related stressors in addition to the improvement and establishment of new MPAs.     

Variability in chemical defense across a shallow to mesophotic depth gradient in the Caribbean sponge <Emphasis Type="Italic">Plakortis angulospiculatus</Emphasis>

The transition between shallow and mesophotic coral reef communities in the tropics is characterized by a significant gradient in abiotic and biotic conditions that could result in potential trade-offs in energy allocation. The mesophotic reefs in the Bahamas and the Cayman Islands have a rich sponge fauna with significantly greater percent cover of sponges than in their respective shallow reef communities, but relatively low numbers of spongivores. Plakortis angulospiculatus, a common sponge species that spans the depth gradient from shallow to mesophotic reefs in the Caribbean, regenerates faster following predation and invests more energy in protein synthesis at mesophotic depths compared to shallow reef conspecifics. However, since P. angulospiculatus from mesophotic reefs typically contain lower concentrations of chemical feeding deterrents, they are not able to defend new tissue from predation as efficiently as conspecifics from shallow reefs. Nonetheless, following exposure to predators on shallow reefs, transplanted P. angulospiculatus from mesophotic depths developed chemical deterrence to predatory fishes. A survey of bioactive extracts indicated that a specific defensive metabolite, plakortide F, varied in concentration with depth, producing altered deterrence between shallow and mesophotic reef P. angulospiculatus. Different selective pressures in shallow and mesophotic habitats have resulted in phenotypic plasticity within this sponge species that is manifested in variable chemical defense and tissue regeneration at wound sites.     

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     

Low natural repopulation of marginal coral communities under the influence of upwelling

The study of coral repopulation in marginal communities may provide a useful analog for understanding the dynamics of coral reefs subjected to deleterious environmental changes. Repopulation of scleractinian reef corals may strongly impact the community structure on tropical reefs; however, the extent of this process on coral communities influenced by upwelling is unknown, especially in the Caribbean. In this study, the potential for natural repopulation of coral communities subjected to wind-driven upwelling was evaluated at three sites on the island of Cubagua, Venezuela. Coral spawning behavior was recorded and both larval settlement and juvenile abundance were estimated. Upwelling did not appear to affect coral spawning behavior, since at this locality spawning occurred at dates and times similar to those reported for well-developed reefs in the Caribbean. Also, juveniles produced by brooding corals were six times more abundant than those of broadcasting species, similar to patterns on other Caribbean reefs that are not under the influence of upwelling. By contrast, mean larval settlement (4 settlers m⁻²) and juvenile abundance (0.1 juveniles m⁻²) in Cubagua were both lower than those elsewhere in the Caribbean and on Pacific reefs. Thus, the potential for repopulation of these marginal communities seems lower than for well-developed coral reefs in other regions. These results suggest that more fully developed coral reefs also may have reduced repopulation potential, as they become influenced by suboptimal environmental conditions. Handling editor: I. Nagelkerken     

Habitat complexity and consumer-mediated positive feedbacks on a Caribbean coral reef

Theoretical and empirical evidence suggest that positive feedbacks can increase resilience in ecological communities. On Caribbean coral reefs, there have been striking shifts from physically complex communities with high coral cover to relatively homogenous communities dominated by macroalgae, which have persisted for decades. However, little is known about positive feedbacks that may maintain coral reef community states. Here, I explore a potential consumer-mediated feedback on a Jamaican reef by examining how grazing by a keystone herbivore ( Diadema antillarum ) is enhanced by physical structure, which offer refugia from predation. Surveys revealed that habitat complexity and Diadema density were positively related. Increasing habitat complexity by adding physical structure significantly decreased macroalgal cover and increased the proportion of urchins in algal habitats in field manipulations. Experimental increases in urchin density also decreased macroalgal cover, but did not affect the proportion of urchins in algal habitats. These results suggest that the low habitat complexity of macroalgal-dominated reefs may inhibit an urchin-mediated shift to coral dominance and that positive feedbacks must be considered in reef restoration efforts.     

Mangrove and coral reef sponge faunas: untold stories about shallow water Porifera in the Caribbean

Sponge faunas from coral reefs and mangrove ecosystems in the Caribbean have mostly been studied from an ecological perspective, with researchers considering the effects of physical and biological factors on their species distribution. To discern evolutionary patterns, this study analyzed the systematic composition, taxonomic diversity, and ecological properties (reproductive strategies, size, shape, endosymbiosis) of mangrove and reef sponge assemblages from seven distant Caribbean localities. Species composition was compared by use of cluster analysis (Sørensen’s), and taxonomic diversity by use of the biodiversity index average taxonomic distinctness (AvTD). Mangrove and reef-associated sponge faunas were found to be statistically dissimilar, with the AvTD values suggesting stronger taxonomic bias toward specific groups in mangroves, irrespective of geographic distance. Most Demospongiae orders have 30–50% more species in coral reefs than in mangroves. The richest reef genera (Agelas, Aplysina, Callyspongia, Petrosia, and Xestospongia) rarely colonize contiguous mangrove formations. The distribution and diversity of suprageneric taxa suggest that coral reef sponge assemblages might represent an older fauna. This historical interpretation would place mangrove subtidal habitats as the youngest marine ecosystem, rather than a below-optimum ecosystem. Life history traits support a biological split discussed here from the perspective of distinct evolutionary histories and different environmental conditions.     

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

The transformation of Caribbean coral communities since humans

The mass die‐off of Caribbean corals has transformed many of this region’s reefs to macroalgal‐dominated habitats since systematic monitoring began in the 1970s. Although attributed to a combination of local and global human stressors, the lack of long‐term data on Caribbean reef coral communities has prevented a clear understanding of the causes and consequences of coral declines. We integrated paleoecological, historical, and modern survey data to track the occurrence of major coral species and life‐history groups throughout the Caribbean from the prehuman period to the present. The regional loss of Acropora corals beginning by the 1960s from local human disturbances resulted in increases in the occurrence of formerly subdominant stress‐tolerant and weedy scleractinian corals and the competitive hydrozoan Millepora beginning in the 1970s and 1980s. These transformations have resulted in the homogenization of coral communities within individual countries. However, increases in stress‐tolerant and weedy corals have slowed or reversed since the 1980s and 1990s in tandem with intensified coral bleaching and disease. These patterns reveal the long history of increasingly stressful environmental conditions on Caribbean reefs that began with widespread local human disturbances and have recently culminated in the combined effects of local and global change.     

Phase shift to algal dominated communities at mesophotic depths associated with lionfish (<Emphasis Type="Italic">Pterois volitans</Emphasis>) invasion on a Bahamian coral reef

Mesophotic coral reefs (30–150 m) have been assumed to be physically and biologically connected to their shallow-water counterparts, and thus may serve as refugia for important taxonomic groups such as corals, sponges, and fish. The recent invasion of the Indo–Pacific lionfish (Pterois volitans) onto shallow reefs of the Caribbean and Bahamas has had significant, negative, effects on shallow coral reef fish populations. In the Bahamas, lionfish have extended their habitat range into mesophotic depths down to 91 m where they have reduced the diversity of several important fish guilds, including herbivores. A phase shift to an algal dominated (>50% benthic cover) community occurred simultaneously with the loss of herbivores to a depth of 61 m and caused a significant decline in corals and sponges at mesophotic depths. The effects of this invasive lionfish on mesophotic coral reefs and the subsequent changes in benthic community structure could not be explained by coral bleaching, overfishing, hurricanes, or disease independently or in combination. The significant ecological effects of the lionfish invasion into mesophotic depths of coral reefs casts doubt on whether these communities have the resilience to recover themselves or contribute to the recovery of their shallow water counterparts as refugia for key coral reef taxa.     

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.     

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.     

Persistence and Change in Community Composition of Reef Corals through Present,Past, and Future Climates

The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past.     

Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta

Sponges are a prominent component of coral reef ecosystems. Like reef-building corals, some sponges have been reported to bleach and die. The giant barrel sponge Xestospongia muta is one of the largest and most important components of Caribbean coral reef communities. Tissues of X. muta contain cyanobacterial symbionts of the Synechococcus group. Two types of bleaching have been described: cyclic bleaching, from which sponges recover, and fatal bleaching, which usually results in sponge death. We quantified hsp70 gene expression as an indicator of stress in X. muta undergoing cyclic and fatal bleaching and in response to thermal and salinity variability in both field and laboratory settings. Chlorophyll a content of sponge tissue was estimated to determine whether hsp70 expression was related to cyanobacterial abundance. We found that fatally bleached sponge tissue presented significantly higher hsp70 gene expression, but cyclically bleached tissue did not, yet both cyclic and fatally bleached tissues had lower chlorophyll a concentrations than nonbleached tissue. These results corroborate field observations suggesting that cyclic bleaching is a temporary, nonstressful state, while fatal bleaching causes significant levels of stress, leading to mortality. Our results support the hypothesis that Synechococcus symbionts are commensals that provide no clear advantage to their sponge host. In laboratory experiments, sponge pieces incubated at 30 °C exhibited significantly higher hsp70 expression than control pieces after 1.5 h, with sponge mortality after less than 15 h. In contrast, sponges at different salinities were not significantly stressed after the same period of time. Stress associated with increasing seawater temperatures may result in declining sponge populations in coral reef ecosystems.     

The abundance of herbivorous fish on an inshore Red Sea reef following a mass coral bleaching event

A healthy herbivore community is critical for the ability of a reef to resist and recover from severe disturbances and to regain lost coral cover (i.e., resilience). The densities of the two major herbivorous fish groups (the family Acanthuridae and scarine labrids) were comparatively studied for an inshore reef that was severely impacted by a mass coral bleaching event in 2010 and an unaffected reef within the same region. Densities were found to be significantly higher on the affected reef, most likely due to the high algal densities on that reef. However, densities of herbivores on both reefs were found to be on average about 1–2 orders of magnitude lower than previously published reports from some Pacific reefs and from Red Sea reefs in the Gulf of Aqaba and only slightly higher than Caribbean reefs. Thus, it is predicted that recovery for this reef and similarly affected reefs may be very slow. The protection of herbivores from overfishing and the introduction of other management strategies that maximize reef resilience in Saudi Arabian waters are highly recommended.