Benefits to host sea anemones from ammonia contributions of resident anemonefish

Abstract

Large ectosymbionts (especially fishes and crustaceans) may have major impacts on the physiology of host cnidarians (sea anemones and corals), but these effects have not been well quantified. Here we describe impacts on giant sea anemone hosts ( Entacmaea quadricolor) and their endosymbiotic zooxanthellae ( Symbiodinium spp.) from the excretion products of anemonefish guests ( Amphiprion bicinctus) under laboratory conditions. Starved host anemones were maintained with anemonefish, ammonia supplements (= NH 3 gas and NH 4 + ion), or neither for 2 mo. In the presence of external ammonia supplements or resident anemonefish, the zooxanthellae within host anemones increased in abundance (173% and 139% respectively), and provided the hosts with energy that minimized host body size loss. In contrast, anemones cultured with neither ammonia nor anemonefish harbored significantly lower abundances of zooxanthellae (84% of initial abundance) and decreased > 60% in body size. Although they maintained higher zooxanthella abundances, anemones cultured with either ammonia supplements or resident anemonefish exhibited significantly lower ammonia uptake rates (0.065 ± 0.005 µmol g - 1 h - 1 , and 0.052 ± 0.018 µmol g - 1 h - 1 respectively) than did control anemones (0.119 ± 0.009 µmol g - 1 h - 1 ), indicating that their zooxanthellae were more nitrogen sufficient. We conclude that, in this multi-level mutualism, ammonia supplements provide essentially the same level of physiological contribution to host anemones and zooxanthellae as do live resident fish. This nutrient supplement reduces the dependence of the zooxanthellae on host feeding, and allows them to provide abundant photosynthetically-produced energy to the host.