Rewiring coral: Anthropogenic nutrients shift diverse coral–symbiont nutrient and carbon interactions toward symbiotic algal dominance

Abstract

Improving coral reef conservation requires heightened understanding of the mechanisms by which coral cope with changing environmental conditions to maintain optimal health. We used a long‐term (10 month) in situ experiment with two phylogenetically diverse scleractinians (Acropora palmata and Porites porites) to test how coral–symbiotic algal interactions changed under real‐world conditions that were a priori expected to be beneficial (fish‐mediated nutrients) and to be harmful, but non‐lethal, for coral (fish + anthropogenic nutrients). Analyzing nine response variables of nutrient stoichiometry and stable isotopes per coral fragment, we found that nutrients from fish positively affected coral growth, and moderate doses of anthropogenic nutrients had no additional effects. While growing, coral maintained homeostasis in their nutrient pools, showing tolerance to the different nutrient regimes. Nonetheless, structural equation models revealed more nuanced relationships, showing that anthropogenic nutrients reduced the diversity of coral–symbiotic algal interactions and caused nutrient and carbon flow to be dominated by the symbiont. Our findings show that nutrient and carbon pathways are fundamentally “rewired” under anthropogenic nutrient regimes in ways that could increase corals’ susceptibility to further stressors. We hypothesize that our experiment captured coral in a previously unrecognized transition state between mutualism and antagonism. These findings highlight a notable parallel between how anthropogenic nutrients promote symbiont dominance with the holobiont, and how they promote macroalgal dominance at the coral reef scale. Our findings suggest more realistic experimental conditions, including studies across gradients of anthropogenic nutrient enrichment as well as the incorporation of varied nutrient and energy pathways, may facilitate conservation efforts to mitigate coral loss.

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

“…In the Florida Keys, this pattern is compounded by a cross‐shelf gradient in water quality, characterized by decreasing turbidity and nutrient concentrations moving away from shore (Lapointe et al, 2019; Lirman & Fong, 2007). Variation in water quality parameters, such as overall nutrient load, dissolved nutrient stoichiometry and the concentration of suspended particulate matter, can dramatically alter coral physiology (Allgeier et al, 2020; Anthony & Fabricius, 2000; Koop et al, 2001) and have been shown to diminish coral resistance to bleaching and disease (DeCarlo et al, 2020; Vega Thurber et al, 2014; Wiedenmann et al, 2013). It is likely that the combined pressure of these cross‐shelf gradients in temperature and water quality conditions is responsible for the observed genetic specialization to each reef zone.…”

“…In the Florida Keys, this pattern is compounded by a cross-shelf gradient in water quality, characterized by decreasing turbidity and nutrient concentrations moving away from shore (Lapointe et al, 2019;Lirman & Fong, 2007). Variation in water quality parameters, such as overall nutrient load, dissolved nutrient stoichiometry and the concentration of suspended particulate matter, can dramatically alter coral physiology (Allgeier et al, 2020;Anthony & Fabricius, 2000;Koop et al, 2001) and have been shown…”

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

“…In the Florida Keys, this pattern is compounded by a cross-shelf gradient in water quality, characterized by decreasing turbidity and nutrient concentrations moving away from shore (Lapointe et al, 2019; Lirman & Fong, 2007). Variation in water quality parameters, such as overall nutrient load, dissolved nutrient stoichiometry, and the concentration of suspended particulate can dramatically alter coral physiology (Allgeier et al, 2020; Anthony & Fabricius, 2000; Koop et al, 2001) and has been shown to diminish coral resistance to bleaching and disease (DeCarlo et al, 2020; Vega Thurber et al, 2014; Wiedenmann et al, 2013). It is likely that the combined pressure of these cross-shelf gradients in temperature and water quality conditions is responsible for the observed genetic specialization to each reef zone.…”

Effects of Ocean Acidification on Carbon and Nitrogen Fixation in the Hermatypic Coral Galaxea fascicularis

“…This was further confirmed by the results of δ 13 C values showing no difference among different pH treatments (Figure 2C). The natural C isotope abundance has been used to understand the balance of autotrophy and heterotrophy in hermatypic corals (Wall et al, 2020), with the δ 13 C values positively relating to the photosynthate or autotrophic input (Tremblay et al, 2015;Allgeier et al, 2020). Therefore, the similar δ 13 C values among different pH treatments suggest stable PFC assimilation.…”