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Nutritional exchange in a tropical tripartite symbiosis II: direct evidence for the transfer of nutrients from host anemone and zooxanthellae to anemonefish

Abstract

The anemone–anemonefish association is the quintessential symbol of a symbiotic mutualism from the Indo-Pacific waters. Both historical field documentation and extant scientific research advocate that these interactions are fundamental at the level of nutrient exchanges and evolutionary driving forces (natural selection) to facilitate this mutualism. Through the use of 15N and 13C stable isotope tracers, complementary laboratory- and field-based experiments were implemented in the Philippines to investigate the possibility of nutrient transmission from the host anemone, Heteractis crispa and/or endosymbiotic zooxanthellae, to two species of exosymbiotic anemonefishes (Amphiprion clarkii and A. perideraion). Mass spectrometry analyses suggest that 15N and 13C concentrations were significantly higher in tissues of the anemonefishes (intestines, liver, gills, and gonads), anemone host, and zooxanthellae compared with controls. We interpret the presence of 15N and 13C in the anemonefish tissues as direct empirical evidence for the transmission of nitrogen and/or carbon from host anemone and endosymbiotic zooxanthellae to resident anemonefish. These “translocations” and resultant recycling of elements within this classical tripartite relationship highlight the fundamental role of nutrient dynamics in this synergistic symbiosis.

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Acknowledgments

We are thankful of A. Duncanson, E. Cochrane, C. Blair, and D. Dallis for laboratory and field support and H. Calumpong and the scientific staff at Silliman University Marine Laboratory for logistical and laboratory support. This study was undertaken within the waters of Dumaguete, Philippines, and complied with all relevant local, regional, and national regulations. We thank L.R. McCloskey, N. Chadwick, and an anonymous reviewer for their time and constructive comments because it ultimately crystalized the manuscript’s arguments. Financial support was provided by the Corning School of Ocean Studies and Maine Maritime Academy.

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Alan Verde, E., Cleveland, A. & Lee, R.W. Nutritional exchange in a tropical tripartite symbiosis II: direct evidence for the transfer of nutrients from host anemone and zooxanthellae to anemonefish. Mar Biol 162, 2409–2429 (2015). https://doi.org/10.1007/s00227-015-2768-8

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Keywords

  • Coral Rubble
  • Host Anemone
  • Endosymbiotic Zooxanthella
  • Anemonefish Species
  • Amphiprion Clarkii