Dataset Information

Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome.

ABSTRACT: Perturbations in natural systems generally are the combination of multiple interactions among individual stressors. However, methods to interpret the effects of interacting stressors remain challenging and are biased to identifying synergies which are prioritized in conservation. Therefore we conducted a multiple stressor experiment (no stress, single, double, triple) on the coral Pocillopora meandrina to evaluate how its microbiome changes compositionally with increasing levels of perturbation. We found that effects of nutrient enrichment, simulated predation, and increased temperature are antagonistic, rather than synergistic or additive, for a variety of microbial community diversity measures. Importantly, high temperature and scarring alone had the greatest effect on changing microbial community composition and diversity. Using differential abundance analysis, we found that the main effects of stressors increased the abundance of opportunistic taxa, and two-way interactions among stressors acted antagonistically on this increase, while three-way interactions acted synergistically. These data suggest that: (1) multiple statistical analyses should be conducted for a complete assessment of microbial community dynamics, (2) for some statistical metrics multiple stressors do not necessarily increase the disruption of microbiomes over single stressors in this coral species, and (3) the observed stressor-induced community dysbiosis is characterized by a proliferation of opportunists rather than a depletion of a proposed coral symbiont of the genus Endozoicomonas.

SUBMITTER: Maher RL

PROVIDER: S-EPMC6497639 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome.

Maher Rebecca L RL Rice Mallory M MM McMinds Ryan R Burkepile Deron E DE Vega Thurber Rebecca R

Scientific reports 20190502 1

Perturbations in natural systems generally are the combination of multiple interactions among individual stressors. However, methods to interpret the effects of interacting stressors remain challenging and are biased to identifying synergies which are prioritized in conservation. Therefore we conducted a multiple stressor experiment (no stress, single, double, triple) on the coral Pocillopora meandrina to evaluate how its microbiome changes compositionally with increasing levels of perturbation. ...[more]

PMID: 31048787

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Project description:The potential for complex synergistic or antagonistic interactions between multiple stressors presents one of the largest uncertainties when predicting ecological change but, despite common use of the terms in the scientific literature, a consensus on their operational definition is still lacking. The identification of synergism or antagonism is generally straightforward when stressors operate in the same direction, but if individual stressor effects oppose each other, the definition of synergism is paradoxical because what is synergistic to one stressor's effect direction is antagonistic to the others. In their highly cited meta-analysis, Crain et al. (Ecology Letters, 11, 2008: 1304) assumed in situations with opposing individual effects that synergy only occurs when the cumulative effect is more negative than the additive sum of the opposing individual effects. We argue against this and propose a new systematic classification based on an additive effects model that combines the magnitude and response direction of the cumulative effect and the interaction effect. A new class of "mitigating synergism" is identified, where cumulative effects are reversed and enhanced. We applied our directional classification to the dataset compiled by Crain et al. (Ecology Letters, 11, 2008: 1304) to determine the prevalence of synergistic, antagonistic, and additive interactions. Compared to their original analysis, we report differences in the representation of interaction classes by interaction type and we document examples of mitigating synergism, highlighting the importance of incorporating individual stressor effect directions in the determination of synergisms and antagonisms. This is particularly pertinent given a general bias in ecology toward investigating and reporting adverse multiple stressor effects (double negative). We emphasize the need for reconsideration by the ecological community of the interpretation of synergism and antagonism in situations where individual stressor effects oppose each other or where cumulative effects are reversed and enhanced.

Project description:Sedimentation and overfishing are important local stressors on coral reefs that can independently result in declines in coral recruitment and shifts to algal-dominated states. However, the role of herbivory in driving recovery across environmental gradients is often unclear. Here we investigate early successional benthic communities and coral recruitment across a sediment gradient in Palau, Micronesia over a 12-month period. Total sedimentation rates measured by 'TurfPods' varied from 0.03 ± 0.1 SE mg cm-2 d-1 at offshore sites to 1.32 ± 0.2 mg cm-2 d-1 at inshore sites. To assess benthic succession, three-dimensional settlement tiles were deployed at sites with experimental cages used to exclude tile access to larger herbivorous fish. Benthic assemblages exhibited rapid transitions across the sediment gradient within three months of deployment. At low levels of sedimentation (less than 0.6 mg cm-2 d-1), herbivory resulted in communities dominated by coral recruitment inducers (short turf algae and crustose coralline algae), whereas exclusion of herbivores resulted in the overgrowth of coral inhibitors (encrusting and upright foliose macroalgae). An 'inducer threshold' was found under increasing levels of sedimentation (greater than 0.6 mg cm-2 d-1), with coral inducers having limited to no presence in communities, and herbivore access to tiles resulted in sediment-laden turf algal assemblages, while exclusion of herbivores resulted in invertebrates (sponges, ascidians) and terrestrial sediment accumulation. A 'coral recruitment threshold' was found at 0.8 mg cm-2 d-1, below which net coral recruitment was reduced by 50% in the absence of herbivores, while recruitment was minimal above the threshold. Our results highlight nonlinear trajectories of benthic succession across sediment gradients and identify strong interactions between sediment and herbivory that have cascading effects on coral recruitment. Local management strategies that aim to reduce sedimentation and turbidity and manage herbivore fisheries can have measurable effects on benthic community succession and coral recruitment, enhancing reef resilience and driving coral recovery.

Dataset Information

Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome.

Publications

Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome.

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