Unveiling the importance of heterotrophy for coral symbiosis under heat stress

Abstract

ABSTRACT Global warming endangers reef-building corals as they lose their photosynthetic symbionts, which limits their ability to feed autotrophically. Consequently, heterotrophy, the capture of zooplankton, can become crucial for the energy budget of heat-stressed corals. However, it is difficult to assess the extent of the heterotrophic contribution in corals, as well as the dynamics of nutrient exchange between the host and its symbionts. In this pioneering study, we employed a suite of isotopic markers, including 13 C- and 15 N bulk tissue isotope measurements, compound-specific isotope analysis of amino acids (CSIA-AAs), and 13 C- and 15 N-labeled food incubations, to investigate nutrient acquisition and allocation in the coral Stylophora pistillata under controlled and heat-induced bleaching conditions. Bulk isotope values and inorganic carbon assimilation remained unchanged in the bleached corals compared to the control corals, overall indicating undisturbed autotrophic activity of the symbionts under heat stress. However, CSIA-AAs showed an increased dependence on heterotrophy for amino acid synthesis in both the host and the symbionts despite reduced assimilation of 15 N-labeled food. Overall, these results suggest that although S. pistillata reduces its assimilation of heterotrophic food under heat stress, the acquisition of amino acids by the coral host and symbionts still relies on heterotrophy. This study emphasizes the importance of using multiple indicators to gain a comprehensive understanding of coral nutrition. It shows that coral dependence on heterotrophy is not only associated with a decline in autotrophic availability. Rather, it demonstrates the ability of S. pistillata to adapt its utilization of food sources to the prevailing environmental conditions. IMPORTANCE This work highlights that every isotopic marker displays a piece of different information concerning the diet of the model coral S. pistillata . By combining all markers, we observed that although S. pistillata exhibited reduced heterotrophic assimilation under heat stress, amino acid acquisition and synthesis remained dependent on heterotrophy. The findings emphasize the adaptability of corals in utilizing different food sources, which is vital for their resilience and recovery in changing environmental conditions. This research underscores the complexity of coral symbiosis and highlights the need for multiple indicators to understand dietary dynamics comprehensively.