نبذة مختصرة : Coral reef symbioses are well-established models for studying multi-level networks of species interactions that provide nutritional benefits to partners. While the contributions of endosymbionts to cnidarian hosts have been extensively documented, relatively little is known about how exosymbionts contribute to nutrient cycling in coral reef cnidarians. We investigated exosymbiotic sources of ammonia and their contributions to physiological processes in Caribbean corkscrew sea anemones Bartholomea annulata. In laboratory experiments, anemones absorbed ammonia from seawater, which significantly enhanced the mitotic index of their endosymbiotic microalgae Symbiodinium, while anemone shrimp presence alone had no effect. Anemone shrimps excreted ammonia at much slower rates than anemones were able to absorb it, indicating that shrimp alone were not able to meet host nitrogen demand. Client fishes excreted ammonia ~10× more rapidly than did associated shrimps. On Caribbean coral reefs, anemone shrimps attract diverse client fishes through their parasite-cleaning behavior; these fishes excrete substantial ammonia near anemones while being cleaned. Exosymbiotic anemone shrimps thus may provide nutritional benefits to host anemones and microalgae indirectly, through their attraction of nitrogen-excreting fishes. This multi-level mutualistic network facilitates tight nutrient cycling among diverse species belonging to several phyla on coral reefs. While we assessed the rates and benefits of nutrient transfer under laboratory conditions, further research is needed to quantify the contributions of ammonia and other nutrients from client fishes through cleaner shrimps to host sea anemones in the field.
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