An official website of the United States government
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.
more »
« less
Fish predation on corals promotes the dispersal of coral symbionts
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
- PAR ID:
- 10218284
- Date Published:
- Journal Name:
- Animal Microbiome
- Volume:
- 3
- Issue:
- 1
- ISSN:
- 2524-4671
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Framework‐building corals create the three‐dimensional structure of coral reefs and are subject to predation from fishes, echinoderms, and gastropods. Anthropogenic stressors can magnify the effects of such top‐down pressure on foundation species. The gastropodCoralliophilaviolacea(Kiener, 1836) depletes coral energy reserves via predation, potentially increasing coral susceptibility to land‐based pollution (i.e., sediment accumulation and nutrient pollution). We hypothesized that sedimentation would worsen coral mortality, while nutrient enrichment would mitigate the harmful effects of sediment and predation on coral mortality by increasing the densities of algal symbionts. To test these hypotheses, we conducted in situ surveys of the fringing reefs in Mo'orea, French Polynesia to explore the relationships among massivePoritesspp. cover,C. violaceadensities, and sediment accumulation on coral colonies across low and high nutrient sites. We also conducted a factorial field experiment to test the interactions among these stressors on coral tissue mortality, symbiont densities, and chlorophyll. MassivePoritescolonies at higher nutrient sites hadC. violaceadensities 13 times higher than at low nutrient sites but there was no difference in the amount of live tissue on coral colonies with or without snails among these sites. In our experiment, there were interactions between predation and nutrients as well as nutrients and sediment that impacted coral mortality. Sedimentation and predation byC. violaceaincreased coral tissue mortality independently by ~20%. Nutrient enrichment reduced this effect in corals under sedimentation or predation pressure by lowering coral tissue mortality by 18% and increasing algal symbiont densities by ~28%. Our results indicate that sediment does not magnify top‐down pressure on this coral, and that moderate nutrient enrichment may interact with predation in complex, unexpected ways to alter the responses of corals to top‐down pressure.more » « less
-
Banaszak, A (Ed.)Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from nine species were marked and sampled in 2017. Of these colonies, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes (2017) and the regional onset of stony coral tissue loss disease (2019). While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together, these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals.more » « less
-
null (Ed.)Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ 15 N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a , lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.more » « less
-
null (Ed.)Abstract Dinoflagellates in the family Symbiodiniaceae are obligate endosymbionts of diverse marine invertebrates, including corals, and impact the capacity of their hosts to respond to climate change-driven ocean warming. Understanding the conditions under which increased genetic variation in Symbiodiniaceae arises via sexual recombination can support efforts to evolve thermal tolerance in these symbionts and ultimately mitigate coral bleaching, the breakdown of the coral-Symbiodiniaceae partnership under stress. However, direct observations of meiosis in Symbiodiniaceae have not been reported, despite various lines of indirect evidence that it occurs. We present the first cytological evidence of sex in Symbiodiniaceae based on nuclear DNA content and morphology using Image Flow Cytometry, Cell Sorting and Confocal Microscopy. We show the Symbiodiniaceae species, Cladocopium latusorum , undergoes gamete conjugation, zygote formation, and meiosis within a dominant reef-building coral in situ. On average, sex was detected in 1.5% of the cells analyzed (N = 10,000–40,000 cells observed per sample in a total of 20 samples obtained from 3 Pocillopora colonies). We hypothesize that meiosis follows a two-step process described in other dinoflagellates, in which diploid zygotes form dyads during meiosis I, and triads and tetrads as final products of meiosis II. This study sets the stage for investigating environmental triggers of Symbiodiniaceae sexuality and can accelerate the assisted evolution of a key coral symbiont in order to combat reef degradation.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s42523-021-00086-4
