Symbiotic benefits to sea anemones from the metabolic byproducts of anemonefish
Abstract
Although anemonefishes and their giant sea anemone hosts became known to the western world in the late nineteenth century, and the first studies exploring these associations were published almost one hundred years ago, to this day the underlying benefits of this interaction to each partner are not fully understood. While benefits to the obligate anemonefishes are widely recognized, benefits to the anemone hosts have been quantified only recently. I describe here physiological benefits to the sea anemone host Entacmaea quadricolor from metabolic waste products excreted by the anemonefish Amphiprion bicinctus. This project was conducted in three main stages: Initially, basal levels of excretion versus uptake of ammonia in laboratory-cultured sea anemones (Entacmaea quadricolor) and anemonefish (Amphiprion bicinctus) were quantified under varying levels of food and light. The nutritional balance sheet indicated that nitrogenous excretion by anemonefish potentially can supply >100% of the nitrogen requirements of sea anemone hosts. Secondly, a starvation experiment was conducted in laboratory aquaria to assess variation in the fitness traits of unfed anemones that were cultured either with 1-2 anemonefish, with artificial ammonia supplements, or with neither. The results indicated that ammonia excreted by resident anemonefish was the primary factor responsible for enhanced zooxanthellae density and reduced tissue loss of sea anemones that were cultured with fish. Thirdly, a field assessment of this symbiosis was conducted on coral reefs in the northern Red Sea. Analysis of water samples taken by scuba divers from among anemones tentacles versus from the water column a few meters away indicated that anemonefish alter the ammonia availability to their hosts by generating significant local enrichment around sea anemones. Examination of zooxanthella populations in field anemones showed that individuals of E. quadricolor exhibit a highly specific association with clade C Symbiodinium at all depths on the reef. In the Red Sea, sea anemones without anemonefish are extremely rare, and the density of their zooxanthellae is contingent primarily on variation in light availability among microhabitats. In conclusion, resident anemonefish are important nutritional benefactors that provide ammonia, an essential limiting nutrient, to their benthic anemone hosts, and thus enhance their survival and fitness in nutrient-poor waters on coral reefs.