Trophic niche partitioning through nutritional mutualism in a eutrophic environment

Mutualisms that involve the exchange of nutrients between autotrophic (photosynthetic) and heterotrophic (consumer) partners have evolved across marine taxa, including corals, nudibranchs, and giant clams. By partnering divergent metabolisms together, these relationships allow species to access uncontested resources and enter novel trophic niche space. Under nutrient-limiting conditions, access to multiple nutritional sources can enable symbiotic holobionts to outcompete sympatric aposymbiotic species. Additionally, variation in the reliance on autotrophy versus heterotrophy can lead to niche partitioning, providing the foundation for holobiont diversification. However, nutritional mutualisms also persist in nutrient-replete environments, such as along the California coast. In this study, we explored trophic niche partitioning along the autotrophy-heterotrophy spectrum in four congeneric anemone species that inhabit similar environments in the California intertidal zone: Anthopleura elegantissima, A. sola, and A. xanthogrammica, which maintain mutualisms with unicellular algae, and A. artemisia which lacks algae. We compared the trophic niches of these four species by comparing their carbon (δ13C) and nitrogen (δ15N) stable isotope values. Further, we compared nutrient sharing between symbiotic anemone hosts and associated algae with the difference between host and symbiont δ13C and δ15N values as well as the overlap of host and symbiont isotopic niches, a proxy for trophic niche, using the Host Evaluation: Reliance on Symbionts (HERS) index. Our results show that all Anthopleura anemones primarily rely on heterotrophy for nutrition, however trophic partitioning is evident along both the heterotrophic and autotrophic niche axis. Larger species (A. sola, A. xanthogrammica) had significantly higher δ15N than small species (A. artemisia, A. elegantissima), suggesting they consume higher trophic level prey. Across symbiotic species, A. elegantissima had significantly smaller differences between host and symbiont δ13C values, indicating it obtained more carbon from its symbionts, whereas A. xanthogrammica had the largest difference between host and symbiont δ13C values, indicating reduced carbon transfer. However, the HERS index showed that A. xanthogrammica exhibited significantly higher overlap between host and symbiont isotopic niches. Together, these results suggest that A. xanthogrammica is typically the most heterotrophic species yet exhibits a high amount of plasticity in the amount of nutrition it obtains from associated algae. Although all species were found to rely predominantly on heterotrophic feeding, our findings demonstrate differences in symbiotic nutrient exchange across species, supporting the hypothesis that Anthopleura anemones exhibit trophic partitioning along the autotrophy-heterotrophy spectrum and providing a potential mechanism behind their coexistence in the intertidal zone.