Outcomes of Infections of Sea Anemone Aiptasia pallida with Vibrio spp. Pathogenic to Corals

Incidents of coral disease are on the rise. However, in the absence of a surrogate animal host, understanding of the interactions between coral pathogens and their hosts remains relatively limited, compared to other pathosystems of similar global importance. A tropical sea anemone, Aiptasia pallida, has been investigated as a surrogate model to study certain aspects of coral biology. Therefore, to test whether the utility of this surrogate model can be extended to study coral diseases, in the present study, we tested its susceptibility to common coral pathogens (Vibrio coralliilyticus and Vibrio shiloi) as well as polymicrobial consortia recovered from the Caribbean Yellow Band Disease (CYBD) lesions. A. pallida was susceptible to each of the tested pathogens. A. pallida responded to the pathogens with darkening of the tissues (associated with an increased melanization) and retraction of tentacles, followed by complete disintegration of polyp tissues. Loss of zooxanthellae was not observed; however, the disease progression pattern is consistent with the behavior of necrotizing pathogens. Virulence of some coral pathogens in Aiptasia was paralleled with their glycosidase activities.     

A 3000 year record of Caribbean reef urchin communities reveals causes and consequences of long‐term decline in Diadema antillarum

Urchins are the last abundant grazers of macroalgae on most Caribbean reefs following the historical overexploitation of herbivorous fishes. The long‐spined urchin Diadema antillarum was particularly effective at controlling macroalgae and facilitating coral dominance on Caribbean reefs until its ecological extinction from a catastrophic disease epidemic in the early 1980s. Despite their important role in the structure and functioning of Caribbean reef ecosystems, the natural dynamics of Caribbean reef urchin communities are poorly known due to the paucity of ecological survey data prior to large‐scale human disturbances and the Diadema dieoff. To help resolve the baseline abundances and ecological roles of common urchin taxa, we track changes in urchin abundance and composition over the past 3000 yr from analysis of subfossil urchin spines preserved in reef matrix cores collected in Caribbean Panama. Echinometra consistently dominated the subfossil spine assemblage, while Diadema was consistently rare in the subfossil record in this region. Rather than increasing during a period of heightened human exploitation of their fish competitors and predators, Diadema began declining over a millennium ago. Convergent cross mapping (CCM) causality analyses reveal that Diadema abundance is causally related to coral community composition. Diadema is negatively affected by Acropora cervicornis dominance, likely due to the tight association between this coral and the threespot damselfish, an effective Diadema competitor. Conversely, Diadema positively affects the abundance of the coral Madracis mirabilis, possibly via its control of macroalgae. Causal relationships were not detected among abundances of individual urchin taxa, indicating that inter‐specific echinoid competition is not a factor limiting Diadema recovery. Our detailed record of prehistorical and historical urchin community dynamics suggests that the failure of Diadema to recover over 30 yr after its mass mortality event may be due in part to the prey release of damselfish following the long‐term overfishing of piscivorous fishes.     

Algae as Reservoirs for Coral Pathogens

Benthic algae are associated with coral death in the form of stress and disease. It''s been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.     

Conservation, precaution, and Caribbean reefs

Some authors argue that overfishing is an important reason that reef corals have declined in recent decades. Their reasoning is that overfishing removes herbivores, releasing macroalgae to overgrow and kill the corals. The evidence suggests, however, that global climate change and emergent marine diseases make a far greater contribution to coral mortality, and that macroalgae generally grow on the exposed skeletal surfaces of corals that are already dead. Macroalgal dominance, therefore, is an effect rather than a cause of coral mortality. Marine protected areas (MPAs), which are usually established to protect stocks of reef fish, foster populations of herbivorous fish under at least some circumstances. Increased herbivory can reduce algal cover, potentially accelerating the recovery of coral populations inside MPAs; however, establishing MPAs will have only a limited impact on coral recovery unless policymakers confront the accelerating negative effects of the global-scale sources of coral mortality.     

White plague disease outbreak in a coral reef at Los Roques National Park, Venezuela

Coral diseases have been reported as a major problem affecting Caribbean coral reefs. During August 2000, a coral mortality event of White Plague Disease-II (WPD-II) was observed at Madrizqui Reef in Los Roques National Park, Venezuela. This disease was identified as the major cause of coral mortality, affecting 24% of all colonies surveyed (n = 1 439). Other diseases such as Black Band Disease (BBD), Yellow Blotch Disease (YBD), Dark Spots Disease (DSD) and White Band Disease (WBD) were also recorded, but showed a lower incidence (0.14-0.97%). Two depth intervals, D1 (5.5-6.5 m) and D2 (9-9.5 m) were surveyed with two sets of three band transects 50 x 2 m long, placed parallel to the long axis of the reef. All healthy and injured corals, along each band transect, were counted and identified to species level. Additionally, all diseases and recent mortality that were still identifiable on each colony also were recorded. The incidence of colonies affected by WPD-II ranged from 12.8 to 33% among transects, where thirteen species of scleractinian corals showed several degrees of mortality. The species most affected were Montastraea annularis (39.13%), M. faveolata (26.67%), M. franksi (9.86%), Stephanocoenia intersepta (7.25%), Colpophyllia natans (6.96%), Diploria labyrinthiformis (2.99%), Mycetophyllia aliciae (2.03%), M. cavernosa (1.74%), and D. strigosa (1.45%). WPD-II was more common in the deeper strata (9-9.5 m), where 63% of the surveyed colonies were affected, although the disease was present along the entire reef. Presently, it is imperative to determine how fast the disease is spreading across the reef, how the disease spreads across the affected colonies and what the long-term effects on the reef will be.     

Algal contact as a trigger for coral disease

Diseases are causing alarming declines in reef‐building coral species, the foundation blocks of coral reefs. The emergence of these diseases has occurred simultaneously with large increases in the abundance of benthic macroalgae. Here, we show that physical contact with the macroalga Halimeda opuntia can trigger a virulent disease known as white plague type II that has caused widespread mortality in most Caribbean coral species. Colonies of the dominant coral Montastraea faveolata exposed to algal transplants developed the disease whereas unexposed colonies did not. The bacterium Aurantimonas coralicida, causative agent of the disease, was present on H. opuntia sampled close to, and away from diseased corals, indicating that the alga serves as a reservoir for this pathogen. Our results suggest that the spread of macroalgae on coral reefs could account for the elevated incidence of coral diseases over past decades and that reduction of macroalgal abundance could help control coral epizootics.     

Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms

Coral populations have precipitously declined on Caribbean reefs while algal abundance has increased, leading to enhanced competitive damage to corals, which likely is mediated by the potent allelochemicals produced by both macroalgae and benthic cyanobacteria. Allelochemicals may affect the composition and abundance of coral-associated microorganisms that control host responses and adaptations to environmental change, including susceptibility to bacterial diseases. Here, we demonstrate that extracts of six Caribbean macroalgae and two benthic cyanobacteria have both inhibitory and stimulatory effects on bacterial taxa cultured from the surfaces of Caribbean corals, macroalgae, and corals exposed to macroalgal extracts. The growth of 54 bacterial isolates was monitored in the presence of lipophilic and hydrophilic crude extracts derived from Caribbean macroalgae and cyanobacteria using 96-well plate bioassays. All 54 bacterial cultures were identified by ribotyping. Lipophilic extracts from two species of Dictyota brown algae inhibited >50% of the reef coral bacteria assayed, and hydrophilic compounds from Dictyota menstrualis particularly inhibited Vibrio bacteria, a genus associated with several coral diseases. In contrast, both lipo- and hydrophilic extracts from 2 species of Lyngbya cyanobacteria strongly stimulated bacterial growth. The brown alga Lobophora variegata produced hydrophilic compounds with broad-spectrum antibacterial effects, which inhibited 93% of the bacterial cultures. Furthermore, bacteria cultured from different locations (corals vs. macroalgae vs. coral surfaces exposed to macroalgal extracts) responded differently to algal extracts. These results reveal that extracts from macroalgae and cyanobacteria have species-specific effects on the composition of coral-microbial assemblages, which in turn may increase coral host susceptibility to disease and result in coral mortality.     

Natural Disease Resistance in Threatened Staghorn Corals

Disease epidemics have caused extensive damage to tropical coral reefs and to the reef-building corals themselves, yet nothing is known about the abilities of the coral host to resist disease infection. Understanding the potential for natural disease resistance in corals is critically important, especially in the Caribbean where the two ecologically dominant shallow-water corals, Acropora cervicornis and A. palmata, have suffered an unprecedented mass die-off due to White Band Disease (WBD), and are now listed as threatened under the US Threatened Species Act and as critically endangered under the IUCN Red List criteria. Here we examine the potential for natural resistance to WBD in the staghorn coral Acropora cervicornis by combining microsatellite genotype information with in situ transmission assays and field monitoring of WBD on tagged genotypes. We show that six percent of staghorn coral genotypes (3 out of 49) are resistant to WBD. This natural resistance to WBD in staghorn corals represents the first evidence of host disease resistance in scleractinian corals and demonstrates that staghorn corals have an innate ability to resist WBD infection. These resistant staghorn coral genotypes may explain why pockets of Acropora have been able to survive the WBD epidemic. Understanding disease resistance in these corals may be the critical link to restoring populations of these once dominant corals throughout their range.     

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.     

Connectivity,regime shifts and the resilience of coral reefs

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

Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean

Since the 1970s, macroalgae have become considerably more abundant on many Caribbean reefs and overfishing of grazing fishes has been implicated as a contributory factor. We explored relationships between algal cover and grazers (biomass of herbivorous fishes and abundance of the sea-urchin Diadema antillarum) on mid-depth reefs (12-15 m) in 19 areas at seven locations in Jamaica, Barbados, Belize, Grand Cayman and Cuba, between April 1997 and April 1998. Diadema antillarum density was never >0.01 m^-2, while herbivorous fish biomass (acanthurids and scarids ⁸ cm total length) varied from 2-5 g m^-2 in Jamaica to 17.1 g m^-2 in Barbados, and was strongly correlated, negatively with macroalgal cover and positively with 'cropped' substratum (sum of 'bare', turf and crustose-coralline substrata) cover. However, overfishing of herbivorous fishes alone cannot explain the widespread abundance of macroalgae, as even on lightly fished reefs, macroalgal cover was mostly >20%. Herbivorous fish populations on those reefs were apparently only able to maintain approximately 40-60% of reef substratum in cropped states, but due to low space-occupation by coral and other invertebrates, 70-90% of substratum was available to algae. The abundance of macroalgae on lightly fished reefs may therefore be a symptom of low coral cover in combination with the continuing absence of Diadema antillarum.     

Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease

Microbial community structure on coral reefs is strongly influenced by coral–algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae), such as Stegastes, mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages and coral health, we determined the benthic community composition (epilithic algal matrix and prokaryotes) and coral disease prevalence inside and outside of damselfish territories in the Great Barrier Reef, Australia. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes''s territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans''s territories. These findings demonstrate the first link between fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease.     

Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef

Herbivory is an important mechanism affecting algal succession, particularly on coral reefs where the relationship between algae and corals is largely controlled by herbivores. However, different functional groups of herbivores may have contrasting effects on succession, which may explain different trajectories of coral reef recovery after disturbance. Here, the effects of different herbivore groups (roving herbivores = foragers and territorial damselfish = farmers) were isolated by a multi-factorial experiment carried out on a coastal coral reef with high macroalgal cover, high farmer densities and relatively low forager abundance. The effects of foragers and farmers were distinguished by monitoring algal succession on settlement tiles placed inside and outside exclusion cages, with orthogonal treatments established inside and outside damselfish territories (with appropriate cage controls). Within 12 months, algal assemblages on ungrazed tiles inside exclusion cages proceeded rapidly from fine filamentous turfs, to corticated algae, to tough erect (e.g. Amphiroa spp.) and foliose (e.g. Peyssonnellidae) calcified algae. Farmers had a dramatic impact on succession, essentially arresting the development of the algal community at a point where it was dominated by palatable filamentous algae of the genus Polysiphonia. Fleshy macroalgae such as Sargassum spp. were excluded from farmer territories. In contrast, foragers did not suppress fleshy macroalgae, but rather, appeared to decelerate succession and promote a relatively diverse assemblage. In contrast to forager-dominated reefs, farmer territories did not appear to function solely as forager exclusion areas or promote algal diversity as a result of intermediate grazing pressure. The relatively strong effects of farmers observed here may represent a future scenario for coral reefs that are increasingly subject to overfishing of large grazing fishes.     

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral-CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs.     

Vibrio sp. as a potentially important member of the Black Band Disease (BBD) consortium in Favia sp. corals

Black Band Disease (BBD) is a well-described disease plaguing corals worldwide. It has been established that ecological and environmental stress factors contribute to the appearance and progression of the disease, believed to be caused by a diverse microbial consortium. We have identified and characterized Vibrio sp. associated with BBD in Eilat reef corals using both culture-dependent and -independent methods. Direct sampling using 16S rRNA gene clone libraries showed seasonal dynamics in the diversity of BBD-associated Vibrios . In the two sampling periods, BBD-associated Vibrio clones showed similarities to different groups: October samples were similar to known pathogens, while December samples were similar to general aquatic Vibrio sp. Cultured bacterial isolates of Vibrio sp. were highly homologous (≥99%) to previously documented BBD-associated bacteria from the Caribbean, Bahamas and Red Seas, and were similar to several known coral pathogens, such as Vibrio coralliilyticus . The proteolytic activity of Vibrio sp., as measured using casein- and azocasein-based assays, directly correlated with temperature elevation and peaked at 26–28 °C, with the microorganisms producing more proteases per bacterial cell or increasing the rate of proteolytic activity of the same proteases (potentially metalloproteases). This activity may promote coral tissue necrosis and aid in ensuing progression of the coral BBD.     

Competitors as accomplices: seaweed competitors hide corals from predatory sea stars

Indirect biotic effects arising from multispecies interactions can alter the structure and function of ecological communities—often in surprising ways that can vary in direction and magnitude. On Pacific coral reefs, predation by the crown-of-thorns sea star, Acanthaster planci, is associated with broad-scale losses of coral cover and increases of macroalgal cover. Macroalgal blooms increase coral–macroalgal competition and can generate further coral decline. However, using a combination of manipulative field experiments and observations, we demonstrate that macroalgae, such as Sargassum polycystum, produce associational refuges for corals and dramatically reduce their consumption by Acanthaster. Thus, as Acanthaster densities increase, macroalgae can become coral mutualists, despite being competitors that significantly suppress coral growth. Field feeding experiments revealed that the protective effects of macroalgae were strong enough to cause Acanthaster to consume low-preference corals instead of high-preference corals surrounded by macroalgae. This highlights the context-dependent nature of coral–algal interactions when consumers are common. Macroalgal creation of associational refuges from Acanthaster predation may have important implications for the structure, function and resilience of reef communities subject to an increasing number of biotic disturbances.     

Genetic Susceptibility,Colony Size,and Water Temperature Drive White-Pox Disease on the Coral Acropora palmata

Outbreaks of coral diseases are one of the greatest threats to reef corals in the Caribbean, yet the mechanisms that lead to coral diseases are still largely unknown. Here we examined the spatial-temporal dynamics of white-pox disease on Acropora palmata coral colonies of known genotypes. We took a Bayesian approach, using Integrated Nested Laplace Approximation algorithms, to examine which covariates influenced the presence of white-pox disease over seven years. We showed that colony size, genetic susceptibility of the coral host, and high-water temperatures were the primary tested variables that were positively associated with the presence of white-pox disease on A. palmata colonies. Our study also showed that neither distance from previously diseased individuals, nor colony location, influenced the dynamics of white-pox disease. These results suggest that white-pox disease was most likely a consequence of anomalously high water temperatures that selectively compromised the oldest colonies and the most susceptible coral genotypes.     

Hysteresis in coral reefs under macroalgal toxicity and overfishing

Macroalgae and corals compete for the available space in coral reef ecosystems.While herbivorous reef fish play a beneficial role in decreasing the growth of macroalgae, macroalgal toxicity and overfishing of herbivores leads to proliferation of macroalgae. The abundance of macroalgae changes the community structure towards a macroalgae-dominated reef ecosystem. We investigate coral-macroalgal phase shifts by means of a continuous time model in a food chain. Conditions for local asymptotic stability of steady states are derived. It is observed that in the presence of macroalgal toxicity and overfishing, the system exhibits hysteresis through saddle-node bifurcation and transcritical bifurcation. We examine the effects of time lags in the liberation of toxins by macroalgae and the recovery of algal turf in response to grazing of herbivores on macroalgae by performing equilibrium and stability analyses of delay-differential forms of the ODE model. Computer simulations have been carried out to illustrate the different analytical results.

Electronic Supplementary Material

The online version of this article (doi:10.1007/s10867-014-9371-y) contains supplementary material, which is available to authorized users.     

Data-driven models for regional coral-reef dynamics

Coral reefs have been affected by natural and anthropogenic disturbances. Coral cover has declined on many reefs, and macroalgae have increased on some. The existence of alternative stable states with high or low coral cover has been widely debated, but not clearly established. We evaluate the evidence for alternative stable states in benthic coral-reef dynamics in the Caribbean, Kenya and Great Barrier Reef (GBR), using stochastic semi-parametric models based on large numbers of time series of cover of hard corals, macroalgae and other components. Only the GBR showed a consistent short-term regional decline in coral cover. There was no evidence for regional increases in macroalgae. The equilibrium distributions of our models were close to recently observed distributions, and differed among regions. In all three regions, the equilibrium distributions were unimodal rather than bimodal, and thus did not suggest the existence of alternative stable states on a regional scale, under current conditions.