Animal waste products are an important component of nutrient cycles and result in the trophic transmission of diverse microorganisms. There is growing recognition that the feces of consumers, such as predators, may impact resource species, their prey, via physical effects and/or microbial activity. We tested the effect of feces from distinct fish trophic groups on coral health and used heat-killed fecal controls to tease apart physical versus microbial effects of contact with fecal material. Fresh grazer/detritivore fish feces caused lesions more frequently on corals, and lesions were 4.2-fold larger than those from sterilized grazer/detritivore feces; in contrast, fresh corallivore feces did not cause more frequent or larger lesions than sterilized corallivore feces. Thus, microbial activity in grazer/detritivore feces, but not corallivore feces, was harmful to corals. Characterization of bacterial diversity in feces of 10 reef fish species, ranging from obligate corallivores to grazer/detritivores, indicated that our experimental findings may be broadly generalizable to consumer guild, since feces of some obligate corallivores contained ~2-fold higher relative abundances of coral mutualist bacteria ( e.g., Endozoicomonadaceae), and lower abundances of the coral pathogen, Vibrio coralliilyticus , than feces of some grazer/detritivores. These findings recontextualize the ecological roles of consumers on coral reefs: although grazer/detritivores support coral reef health in various ways ( e.g. , promoting coral settlement and herbivory through the removal of detritus and sediments from the algal matrix), they also disperse coral pathogens. Corallivore predation can wound corals, yet their feces contain potentially beneficial coral-associated bacteria, supporting the hypothesized role of consumers, and corallivores in particular, in coral symbiont dispersal. Such consumer-mediated microbial dispersal as demonstrated here has broad implications for environmental management.
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The role of predators in coral disease dynamics
Abstract Coral disease is becoming increasingly problematic on reefs worldwide. However, most coral disease research has focused on the abiotic drivers of disease, potentially overlooking the role of species interactions in disease dynamics. Coral predators in particular can influence disease by breaking through protective tissues and exposing corals to infections, vectoring diseases among corals, or serving as reservoirs for pathogens. Numerous studies have demonstrated the relationship between corallivores and disease in certain contexts, but to date there has been no comprehensive synthesis of the relationships between corallivores and disease, which hinders our understanding of coral disease dynamics. To address this void, we identified 65 studies from 26 different ecoregions that examine this predator–prey-disease relationship. Observational studies found over 20 positive correlations between disease prevalence and corallivore abundance, with just four instances documenting a negative correlation between corallivores and disease. Studies found putative pathogens in corallivore guts and experiments demonstrated the ability of corallivores to vector pathogens. Corallivores were also frequently found infesting disease margins or targeting diseased tissues, but the ecological ramifications of this behavior remains unknown. We found that the impact of corallivores was taxon-dependent, with most invertebrates increasing disease incidence, prevalence, or progression; fish showing highly context-dependent effects; and xanthid crabs decreasing disease progression. Simulated wounding caused disease in many cases, but experimental wound debridement slowed disease progression in others, which could explain contrasting findings from different taxa. The negative effects of corallivores are likely to worsen as storms intensify, macroalgal cover increases, more nutrients are added to marine systems, and water temperatures increase. As diseases continue to impact coral reefs globally, a more complete understanding of the ecological dynamics of disease—including those involving coral predators—is of paramount importance to coral reef conservation and management.
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- Award ID(s):
- 2224354
- NSF-PAR ID:
- 10421689
- Date Published:
- Journal Name:
- Coral Reefs
- Volume:
- 41
- Issue:
- 2
- ISSN:
- 0722-4028
- Page Range / eLocation ID:
- 405 to 422
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract As coral populations decline across the Caribbean, it is becoming increasingly important to understand the forces that inhibit coral survivorship and recovery. Predation by corallivores, such as the short coral snail
Coralliophila abbreviata , are one such threat to coral health and recovery worldwide, but current understanding of the factors controlling corallivore populations, and therefore predation pressure on corals, remains limited. To examine the extent to which bottom-up forces (i.e., coral prey), top-down forces (i.e., predators), and marine protection relate toC. abbreviata distributions, we surveyedC. abbreviata abundance, percent coral cover, and the abundance of potential snail predators across six protected and six unprotected reefs in the Florida Keys. We found thatC. abbreviata abundance was lower in protected areas where predator assemblages were also more diverse, and that across all sites snail abundance generally increased with coral cover.C. abbreviata abundance had strong, negative relationships with two gastropod predators—the Caribbean spiny lobster (Panulirus argus ) and the grunt black margate (Anisotremus surinamensis ), which may be exerting top-down pressure onC. abbreviata populations. Further, we found the size ofC. abbreviata was also related to reef protection status, with largerC. abbreviata on average in protected areas, suggesting that gape-limited predators such asP. argus andA. surinamensis may alter size distributions by targeting small snails. Combined, these results provide preliminary evidence that marine protection in the Florida Keys may preserve critical trophic interactions that indirectly promote coral success via control of local populations of the common corallivorous snailC. abbreviata. -
null (Ed.)Abstract Background The microbiomes of foundation (habitat-forming) species such as corals and sponges underpin the biodiversity, productivity, and stability of ecosystems. Consumers shape communities of foundation species through trophic interactions, but the role of consumers in dispersing the microbiomes of such species is rarely examined. For example, stony corals rely on a nutritional symbiosis with single-celled endosymbiotic dinoflagellates (family Symbiodiniaceae) to construct reefs. Most corals acquire Symbiodiniaceae from the environment, but the processes that make Symbiodiniaceae available for uptake are not resolved. Here, we provide the first comprehensive, reef-scale demonstration that predation by diverse coral-eating (corallivorous) fish species promotes the dispersal of Symbiodiniaceae, based on symbiont cell densities and community compositions from the feces of four obligate corallivores, three facultative corallivores, two grazer/detritivores as well as samples of reef sediment and water. Results Obligate corallivore feces are environmental hotspots of Symbiodiniaceae cells: live symbiont cell concentrations in such feces are 5–7 orders of magnitude higher than sediment and water environmental reservoirs. Symbiodiniaceae community compositions in the feces of obligate corallivores are similar to those in two locally abundant coral genera ( Pocillopora and Porites ), but differ from Symbiodiniaceae communities in the feces of facultative corallivores and grazer/detritivores as well as sediment and water. Combining our data on live Symbiodiniaceae cell densities in feces with in situ observations of fish, we estimate that some obligate corallivorous fish species release over 100 million Symbiodiniaceae cells per 100 m 2 of reef per day. Released corallivore feces came in direct contact with coral colonies in the fore reef zone following 91% of observed egestion events, providing a potential mechanism for the transfer of live Symbiodiniaceae cells among coral colonies. Conclusions Taken together, our findings show that fish predation on corals may support the maintenance of coral cover on reefs in an unexpected way: through the dispersal of beneficial coral symbionts in corallivore feces. Few studies examine the processes that make symbionts available to foundation species, or how environmental reservoirs of such symbionts are replenished. This work sets the stage for parallel studies of consumer-mediated microbiome dispersal and assembly in other sessile, habitat-forming species.more » « less
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Dubilier, Nicole (Ed.)ABSTRACT The increase in prevalence and severity of coral disease outbreaks produced by Vibrio pathogens, and related to global warming, has seriously impacted reef-building corals throughout the oceans. The coral Oculina patagonica has been used as a model system to study coral bleaching produced by Vibrio infection. Previous data demonstrated that when two coral pathogens ( Vibrio coralliilyticus and Vibrio mediterranei ) simultaneously infected the coral O. patagonica , their pathogenicity was greater than when each bacterium was infected separately. Here, to understand the mechanisms underlying this synergistic effect, transcriptomic analyses of monocultures and cocultures as well as experimental infection experiments were performed. Our results revealed that the interaction between the two vibrios under culture conditions overexpressed virulence factor genes (e.g., those encoding siderophores, the type VI secretion system, and toxins, among others). Moreover, under these conditions, vibrios were also more likely to form biofilms or become motile through induction of lateral flagella. All these changes that occur as a physiological response to the presence of a competing species could favor the colonization of the host when they are present in a mixed population. Additionally, during coral experimental infections, we showed that exposure of corals to molecules released during V. coralliilyticus and V. mediterranei coculture induced changes in the coral microbiome that favored damage to coral tissue and increased the production of lyso-platelet activating factor. Therefore, we propose that competition sensing, defined as the physiological response to detection of harm or to the presence of a competing Vibrio species, enhances the ability of Vibrio coral pathogens to invade their host and cause tissue necrosis. IMPORTANCE Vibrio coralliilyticus and Vibrio mediterranei are important coral pathogens capable of inducing serious coral damage, which increases severely when they infect the host simultaneously. This has consequences related to the dispersion of these pathogens among different locations that could enhance deleterious effects on coral reefs. However, the mechanisms underlying this synergistic interaction are unknown. The work described here provides a new perspective on the complex interactions among these two Vibrio coral pathogens, suggesting that coral infection could be a collateral effect of interspecific competition. Major implications of this work are that (i) Vibrio virulence mechanisms are activated in the absence of the host as a response to interspecific competition and (ii) release of molecules by Vibrio coral pathogens produces changes in the coral microbiome that favor the pathogenic potential of the entire Vibrio community. Thus, our results highlight that social cues and competition sensing are crucial determinants of development of coral diseases.more » « less
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null (Ed.)Abstract A suite of processes drive variation in coral populations in space and time, yet our understanding of how variation in coral density affects coral performance is limited. Theory predicts that reductions in density can send coral populations into a predator pit, where concentrated corallivory maintains corals at low densities. In reality, how variation in coral density alters corallivory rates is poorly resolved. Here, we experimentally quantified the effects of corallivory and coral density on growth and survival of small colonies of the staghorn coral Acropora pulchra . Our findings suggest that coral density and corallivory have strong but independent effects on coral performance. In the presence of corallivores, corals suffered high but density-independent mortality. When corallivores were excluded, however, vertical extension rates of colonies increased with increasing densities. While we found no evidence for a predator pit, our results suggest that spatio-temporal variation in corallivore and coral densities can fundamentally alter population dynamics via strong effects on juvenile corals.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1007/s00338-022-02219-w
