Predation, community asynchrony, and metacommunity stability in cyanobacterial mats

Abstract

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.

Convergent photophysiology and prokaryotic assemblage structure in epilithic cyanobacterial tufts and algal turf communities

“…Emerging evidence from examination of the nutritional ecology of nominal herbivores, specifically reef parrotfishes, suggests a fundamental preference for targeting cyanobacteria as nutritional resources by these fishes (Clements et al, 2017;Nicholson & Clements, 2020. Alongside this evidence from nutritional ecology, multiple observational studies now have confirmed the consumption of benthic cyanobacterial mats by multiple nominally herbivorous fishes on Caribbean reefs (Cissell et al, 2019;Cissell & McCoy, 2022b), including the documented preferential consumption by several of these fishes (Manning & McCoy, 2023). These various lines of evidence imply that the expansion of conspicuous benthic cyanobacterial assemblages may not inherently disrupt trophic flow through ecosystems (here, on coral reefs) owing to a lack of palatability as previously generally theorized (Ullah et al, 2018).…”

Top‐heavy trophic structure within benthic viral dark matter

“…Strong lineage‐specific patterns in intra‐mat trophic structure (Figures 4 and S16; potentially coupled to host trophic affiliation; Cissell & McCoy, 2022a; Cissell & McCoy, 2022b) may, in part, contribute to patterns of spatial genomic diversification among mat‐building populations and likely impact intra‐mat chemistry and nutrient recycling (Weitz & Wilhelm, 2012). Bacteria‐phage coevolution is known to increase both phage and bacterial divergence rates mediated via reciprocal adaptation (evolutionary conflict) and promote diversity across multiple levels of ecological organisation, affecting overall community structure (Koskella & Brockhurst, 2014).…”

Viral association with cyanobacterial mat community mortality

“…Benthic cyanobacterial mats (BCMs) are becoming increasingly dominant members of coral reef communities worldwide due to the influence of both local and global stressors (Cissell & McCoy, 2022a; de Bakker et al, 2017; Ford et al, 2018). We define coral reef BCMs as a functional grouping that broadly encompasses taxonomically and functionally rich, conspicuous benthic consortia primarily comprised of prokaryotic members of the phyla Cyanobacteria (dominating the construction and maintenance of mat structural complexity), Proteobacteria, and Bacteroidetes (Cissell & McCoy, 2021; Stuij et al, 2022).…”

“…Previous work on coral reef BCMs has focused on mat formation and growth, emphasizing the importance of bottom‐up and physical drivers in the proliferation of mat cover (Brocke et al, 2015; Kuffner & Paul, 2001). Past research on mat dynamics is also generally scale restricted and often focuses on reef sites (total benthic cover of BCMs) rather than documenting the dynamics of the individual component mat communities (but see Cissell & McCoy, 2022a). Conversely, limited attention has been given to understanding the natural senescence dynamics of mature BCM communities or elucidating the drivers and manifestations of individual mat physical trajectory and mortality.…”

“…In this equilibrium state, individual microbial mats can stably survive for years (Bolhuis et al, 2014; Doemel & Brock, 1977). In contrast, individual cyanobacterial mats on coral reefs around the Caribbean island of Bonaire were recently found to persist only on the scale of weeks (Cissell & McCoy, 2022a). These striking field observations emphasize the significant gap in our understanding of the natural history of cyanobacterial mats on coral reefs.…”