Chronic disturbance modulates symbiont (Symbiodiniaceae) beta diversity on a coral reef

Abstract

chronic disturbance can disrupt ecological interactions including the foundational symbiosis between reef-building corals and the dinoflagellate family Symbiodiniaceae. Symbiodiniaceae are photosynthetic endosymbionts necessary for coral survival, but many Symbiodiniaceae can also be found free-living in the environment. Since most coral species acquire new Symbiodiniaceae from the environment each generation, free-living Symbiodiniaceae represent important pools for coral symbiont acquisition. Yet, little is known about the diversity of, or impacts of disturbance on, freeliving Symbiodiniaceae. To determine how chronic and pulse disturbances influence Symbiodiniaceae communities, we sampled three reef habitat compartments-sediment, water, and coral (Pocillopora grandis, Montipora aequituberculata, Porites lobata)-at sites exposed to different levels of chronic anthropogenic disturbance, before, during, and after a major storm. Almost no (4%) Symbiodiniaceae amplicon sequence variants (ASVs) were found in all three compartments, and over half were found uniquely in coral. Sites experiencing chronic disturbance were typically associated with higher symbiont beta diversity (i.e., variability and turnover) across reef habitat compartments. Pulse stress, from the storm, exhibited some influence on symbiont beta diversity but the effect was inconsistent. This suggests that in this ecosystem, the effects of chronic disturbance are more prominent than temporal variability during a pulse disturbance for shaping symbiont communities. Disturbances, both natural and anthropogenic, can alter species diversity and cause stress on ecosystem structure and function. Disturbance can manifest as chronic disturbance (i.e., long-term or press disturbance) or pulse disturbance (i.e., short-term or acute disturbances events) 1,2. Both types of disturbance can alter not only alpha diversity (i.e., species diversity within a community; e.g. 3,4) but also beta diversity (i.e., differences in species composition among communities 5,6), which has emerged as a sensitive indicator of ecosystem change under stress 7,8. Beta diversity metrics can be split into two working definitions: 'turnover' is defined as compositional changes of species assemblages across a gradient, while 'variation' is defined as the amount of variability among species assemblages within each community 9. When communities are analyzed in a multivariate context, 'turnover' represents multivariate location, while 'variation' represents multivariate spread (beta dispersion). A growing body of literature has shown that for macro-organisms, disturbances often cause a decrease in beta diversity, leading to 'biotic homogenization' (i.e., communities become simplified and more similar to one another 10-13). In microorganisms , however, emerging evidence suggests that disturbance can have the opposite effect, resulting in elevated beta diversity (e.g. 14-16 ; reviewed in 17). This effect has been attributed to the ' Anna Karenina' principle, wherein stress causes an increase in ...

On a Reef Far, Far Away: Anthropogenic Impacts Following Extreme Storms Affect Sponge Health and Bacterial Communities

“…For example, the ' Anna Karenina Principle' or AKP (Zaneveld et al, 2017) predicts that dysbiotic host individuals are more dissimilar in microbial community composition than healthy host individuals. The AKP has previously been detected in corals (Zaneveld et al, 2016;Claar et al, 2020;Howe-Kerr et al, 2020) as well as reef sponges (Lesser et al, 2016). Previous work has shown the utility of using filter-feeding sponges as monitoring tools for fecalcoliform contamination in near-shore environments (Longo et al, 2010;Maldonado et al, 2010).…”

Unlocking the phylogenetic diversity, primary habitats, and abundances of free‐living Symbiodiniaceae on a coral reef

“…To examine Symbiodiniaceae community structure across free-living habitats we used a permutational multivariate analysis of variance 250 Symbiodiniaceae reads were removed from the data set) the design was unbalanced which reduces the power of PERMANOVA to separate treatment effects from dispersion around group centroids. Variable dispersion between levels of each factor were tested (vegan, betadisper), and where a factor was significant in PERMANOVA yet also had significant differences in dispersion, a bootstrapping analysis was conducted to assess the impact of design imbalance (Claar et al, 2020). We randomly subsampled each group to match the sample size of the smallest group, and re-ran the PERMANOVA.…”

“…(2020) into the matrix (similar to Claar et al. (2020), and from this a phylogenetic tree was generated (phangorn, upgma : Schliep, 2011). ASV abundances were Hellinger transformed and the weighted UniFrac distances computed in phyloseq (McMurdie & Holmes, 2013).…”

Differential Symbiodiniaceae Association With Coral and Coral-Eroding Sponge in a Bleaching Impacted Marginal Coral Reef Environment

“…The determined ITS2 ASVs were assigned a taxonomic identity using the RDP classifier (Wang et al, 2007) against reference database sequences. This study employed three different databases for taxonomic classification of ASVs: (i) Db1 (Claar et al, 2020), (ii) Db2 (Shi et al, 2021), and (iii) Db3 1 . To aid in the removal of non−Symbiodiniaceae sequences (e.g., non-target dinoflagellates), default RDP bootstrap value of 50 was used.…”

“…Response to environmental stressors varies among coral species and endosymbiont communities (van Woesik et al, 2011;Cunning et al, 2017). The local environment exerts selection pressure which eliminates the sensitive Symbiodiniaceae taxa and results in the dominance of stress-resilient species (Cunning et al, 2015;Claar et al, 2020). This differential abundance of specific thermotolerant Symbiodiniaceae taxa affects the functional characteristics of their host (LaJeunesse et al, 2010a;Carballo-Bolaños et al, 2019), eventually leading to the emergence of a particular "space winner" genotype (LaJeunesse et al, 2010a;Stat and Gates, 2011).…”