Ratio of Energy and Nutrient Fluxes Regulates Symbiosis between Zooxanthellae and Corals

Ambient irradiance levels determine the rate of carbon influx into zooxanthellae at any given time, and thereby the energy available for the whole coral symbiotic association. Long-term photoacclimation of zooxanthellae to the time-averaged light regime at which the host coral grows results in optimization of light harvesting and utilization. Under high irradiance light harvesting is reduced, thereby avoiding photodynamic damage, whereas under low light, photon capture and quantum yield are maximized. Most of the photosynthate produced by the algae is respired. However, the capability of the zooxanthellae and the coral to retain carbon beyond that required to meet their respiratory needs depends on the availability of the commonly limiting nutrients, nitrogen and phosphorus. Therefore, the ratio of the flux of these nutrients into the colony to that of the photosynthetically driven carbon flux will regulate the growth of the zooxanthellae and ofthe animal. Nutrients acquired by predation of the coral on zooplankton are available first to the animal, whereas those absorbed by the zooxanthellae from seawater as inorganic compounds lead first to growth of the algae. to the photosynthetic production of highenergy compounds, mainly carbohydrates. These are produced in great excess of that needed to support the basic metabolic needs of the zooxanthellae. However, because these compounds have a very high C: N ratio, they cannot by themselves support multiplication of the algae. The excess photosynthate, which may reach as much as 95% of the total, is "translocated" to the host animal, a process stimulated by "host factors" that dramatically increase the excretion of assimilated carbon compounds by the algae (Muscatine 1967, Sutton and Heegh-Guldberg 1990). The translocated carbon compounds are more than enough to provide for the respiratory needs of the host (Muscatine et al. 1984), although, as is also the case for the zooxanthellae, they cannot support growth of animal tissue. These energy-rich, nitrogen-poor products of photosynthesis were termed "junk food" because of their insufficiency as food for growth (Falkowski et al. 1984). In return for fixed carbon, the zooxanthellae gain access to the high nitrogen and phosphorus metabolic waste products of their 313 I This study was supported by grant no. 89 00444 from the U.S.-Israel Binational Science Foundation. Manuscript accepted 15 August 1993. 2 Department of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel. 3 Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1346, Kaneohe, Hawaii 96744. IT HAS BEEN an accepted dogma in coral biology that the extensive spatial and long-term temporal success of coral reefs in the oligotrophic littoral of tropical seas stems from the symbiotic association between endocellular microalgae (the zooxanthellae) and the host hermatype. It is this association that allows corals and coral reef communities to thrive in spite of the low concentrations of nitrogen and phosphorus in the oligotrophic ambient waters (Muscatine and Porter 1977). It is this oligotrophy that also causes the striking paucity of phytoand zooplankton in these "blue deserts," limiting the availability of particulate food as an alternate nutrient source. In this mutualistic symbiosis the algae contribute their capability to harness sunlight