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Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral-algal competition.

ABSTRACT: Understanding the effects of natural processes on coral-algal competition is an important step in identifying the role of macroalgae in perturbed coral reef ecosystems. However, studies investigating coral-algal interactions are often conducted in response to a disturbance, and rarely incorporate seasonal variability. Here, naturally occurring coral-algal interactions were assessed in situ four times a year over 2 years across eight sites spanning diverse benthic communities. In over 6500 recorded coral-algal interactions, cyanobacteria and turf algae were found to be the most damaging regardless of season, resulting in visible damage to coral in greater than 95% of interactions. Macroalgae that primarily compete using chemical mechanisms were found to be more damaging than those that compete using physical mechanisms (e.g. abrasion), with both groups demonstrating decreased competitive ability in summer. While crustose coralline algae were the least damaging to competing coral, during summer, it became three times more competitive. Our results demonstrate that the competitive ability of macroalgae and the outcomes of coral-algal competition can fluctuate in seasonal cycles that may be related to biomass, production of chemical defences and/or physical toughness. The results of this study have important implications for understanding the trajectory and resilience of coral reef ecosystems into the future.

SUBMITTER: Brown KT

PROVIDER: S-EPMC7813255 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral-algal competition.

Brown Kristen T KT Bender-Champ Dorothea D Hoegh-Guldberg Ove O Dove Sophie S

Royal Society open science 20201223 12

Understanding the effects of natural processes on coral-algal competition is an important step in identifying the role of macroalgae in perturbed coral reef ecosystems. However, studies investigating coral-algal interactions are often conducted in response to a disturbance, and rarely incorporate seasonal variability. Here, naturally occurring coral-algal interactions were assessed <i>in situ</i> four times a year over 2 years across eight sites spanning diverse benthic communities. In over 6500 ...[more]

PMID: 33489294

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Project description:Benthic primary producers in tropical reef ecosystems can alter biogeochemical cycling and microbial processes in the surrounding seawater. In order to quantify these influences, we measured rates of photosynthesis, respiration, and dissolved organic carbon (DOC) exudate release by the dominant benthic primary producers (calcifying and non-calcifying macroalgae, turf-algae and corals) on reefs of Mo'orea French Polynesia. Subsequently, we examined planktonic and benthic microbial community response to these dissolved exudates by measuring bacterial growth rates and oxygen and DOC fluxes in dark and daylight incubation experiments. All benthic primary producers exuded significant quantities of DOC (roughly 10% of their daily fixed carbon) into the surrounding water over a diurnal cycle. The microbial community responses were dependent upon the source of the exudates and whether the inoculum of microbes included planktonic or planktonic plus benthic communities. The planktonic and benthic microbial communities in the unamended control treatments exhibited opposing influences on DO concentration where respiration dominated in treatments comprised solely of plankton and autotrophy dominated in treatments with benthic plus plankon microbial communities. Coral exudates (and associated inorganic nutrients) caused a shift towards a net autotrophic microbial metabolism by increasing the net production of oxygen by the benthic and decreasing the net consumption of oxygen by the planktonic microbial community. In contrast, the addition of algal exudates decreased the net primary production by the benthic communities and increased the net consumption of oxygen by the planktonic microbial community thereby resulting in a shift towards net heterotrophic community metabolism. When scaled up to the reef habitat, exudate-induced effects on microbial respiration did not outweigh the high oxygen production rates of benthic algae, such that reef areas dominated with benthic primary producers were always estimated to be net autotrophic. However, estimates of microbial consumption of DOC at the reef scale surpassed the DOC exudation rates suggesting net consumption of DOC at the reef-scale. In situ mesocosm experiments using custom-made benthic chambers placed over different types of benthic communities exhibited identical trends to those found in incubation experiments. Here we provide the first comprehensive dataset examining direct primary producer-induced, and indirect microbially mediated alterations of elemental cycling in both benthic and planktonic reef environments over diurnal cycles. Our results highlight the variability of the influence of different benthic primary producers on microbial metabolism in reef ecosystems and the potential implications for energy transfer to higher trophic levels during shifts from coral to algal dominance on reefs.

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Project description:Pervasive environmental stressors on coral reefs are attributed with shifting the competitive balance in favor of alternative dominants, such as macroalgae. Previous studies have demonstrated that macroalgae compete with corals via a number of mechanisms, including the production of potent primary and secondary metabolites that can influence coral-associated microbial communities. The present study investigates the effects of the Pacific brown macroalga Lobophora sp. (due to the shifting nature of the Lobophora species complex, it will be referred to here as Lobophora sp.) on coral bacterial isolates, coral larvae, and the microbiome associated with the coral Porites cylindrica. Crude aqueous and organic macroalgal extracts were found to inhibit the growth of coral-associated bacteria. Extracts and fractions were also shown to inhibit coral larval settlement and cause mortality at concentrations lower (<0.3 mg · ml-1) than calculated natural concentrations (4.4 mg · ml-1). Microbial communities associated with coral tissues exposed to aqueous (e.g., hydrophilic) crude extracts demonstrated a significant shift to Vibrio dominance and a loss of sequences related to the putative coral bacterial symbiont, Endozoicomonas sp., based on 16S rRNA amplicon sequencing. This study contributes to growing evidence that macroalgal allelochemicals, dissolved organic material, and native macroalgal microbial assemblages all play a role in shifting the microbial equilibrium of the coral holobiont away from a beneficial state, contributing to a decline in coral fitness and a shift in ecosystem structure. Diverse microbial communities associate with coral tissues and mucus, providing important protective and nutritional services, but once disturbed, the microbial equilibrium may shift from a beneficial state to one that is detrimental or pathogenic. Macroalgae (e.g., seaweeds) can physically and chemically interact with corals, causing abrasion, bleaching, and overall stress. This study contributes to a growing body of evidence suggesting that macroalgae play a critical role in shifting the coral holobiont equilibrium, which may promote the invasion of opportunistic pathogens and cause coral mortality, facilitating additional macroalgal growth and invasion in the reef. Thus, macroalgae not only contribute to a decline in coral fitness but also influence coral reef ecosystem structure.

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Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral-algal competition.

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Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral-algal competition.

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