Predation, community asynchrony, and metacommunity stability in cyanobacterial mats

Holistically characterizing mechanisms that connect biotic context with patterns in persistence across levels of ecological organization requires integrating patterns of variability across scale. This is especially true in microbial communities, where relevant trophic interactions operate across disparate spatiotemporal scales. Here, we integrated observational, experimental, and theoretical approaches to unify local and regional ecological processes driving the dynamics of benthic cyanobacterial mats on coral reefs off the island of Bonaire, Caribbean Netherlands. Community and metacommunity dynamics of mats were tracked for 49 days alongside quantification of macropredation pressure from fishes. Viral interactions were interrogated using shotgun metagenomics and metatranscriptomics within a dying mat community to explore patterns in viral infectivity and prey population dynamics. Further, we employed a field experiment to test the hypothesis that enhanced predation would result in decreased mat persistence. Finally, we constructed a cellular automaton model to predict patterns in mat metacommunity dynamics across different scenarios of top-down and bottom-up control and dispersal. Cyanobacterial mat metacommunities were temporally stable across the study, stabilized by asynchrony in the dynamics of communities (∼54% death rate in communities across 10 death dates). A total of 11 different reef fishes were documented foraging on mats, exhibiting heterogeneity in predation pressure among communities (72.8 mean bites per mat ± 111.2 bites SD) that likely contributes to the stabilizing asynchrony of community dynamics. Predation from reef fishes, though, may interact with other factors to influence mat community dynamics, as experimentally enhanced predation decreased the instantaneous mortality rate of mat communities over natural mat communities (-0.012 vs. -0.023). Viral linkage strength increased in decaying mat area over healthy mat area (median log abundance 2.41 vs. 2.27) alongside decreases in prey population abundances. Theoretical simulations suggested that dispersal conveys a rescuing effect on mat metacommunity abundance under scenarios of strong trophic control, and dispersal is likely an important but unexplored driver of observed benthic cyanobacterial mat dynamics. We contextualize our experimental work with a collection of curated natural history observations and a unifying definition of benthic cyanobacterial mats. These data establish critical baselines and generate hypotheses relevant to the processes maintaining cyanobacterial dominance of reefs.