13C-based model of photosynthate translocation

INTRODUCTION Symbiotic dinoflagellates of the genus Symbiodinium, commonly called zooxanthellae, live in the tissue of many scleractinian corals and are the major contributors to the primary productivity of reefs. Dinoflagellates fix inorganic carbon into organic molecules, partly use the photosynthetic products (photosynthates) for their own respiration and growth, and translocate a large fraction of their daily photosynthate production to their coral host. The latter uses it for its own needs such as growth, respiration and reproduction (Muscatine et al., 1983; Davies, 1984; Davy and Cook, 2001). A fraction of the carbon fixed is lost from the symbiotic association as dissolved and particulate organic carbon (DOC and POC, respectively) (Crossland et al., 1980), the latter being in the form of mucus. Photosynthates are a cocktail of glycerol, glucose, amino acids and lipids (Muscatine et al., 1994; Ishikura et al., 1999; Davy and Cook, 2001; Treignier et al., 2008). Because isolated dinoflagellates release less than 5% of the fixed carbon to the surrounding seawater as DOC and POC, it has been suggested that the release of photosynthates from the symbionts is induced by the host animal via chemical stimuli known as host release factors (Muscatine, 1967; Grant et al., 1998; Davy and Cook, 2001). Numerous studies have investigated the budget of autotrophic carbon of tropical cnidarian–algal symbioses (Muscatine et al., 1984; Davies, 1991; McCloskey et al., 1994; Davy et al., 1996) and have suggested that symbionts living with shallow-water corals translocate more than 90% of their photosynthates to the animal host. This nutritional interaction is one of the key reasons for the success of corals and other symbiotic invertebrates in nutrient-poor tropical waters. As habitat depth increases, however, photosynthetic production decreases because of light limitation, and some coral species rely on zooplankton grazing to sustain their metabolism (Palardy et al., 2005; Palardy et al., 2008). Photosynthetic production is also severely decreased during bleaching events (loss of symbionts and/or photosynthetic pigments) following stressful conditions, which impact the ability of corals to survive (Hoegh-Guldberg, 1999). In order to predict the health of corals under future climate scenarios, it is crucial to accurately determine the amount of photosynthetically fixed carbon that is translocated from the symbionts to the host animal, the daily contribution of these photosynthates to the animal respiration, and the allocation of the remaining carbon to the various components of the symbiotic association. Assessing the carbon budget of corals is therefore a central question in reef studies, and calculating the amount of photosynthetically fixed carbon that is translocated from the symbionts to the host coral is a problem that still vexes ecophysiologists. Indeed, it is currently assumed that a reduction in total carbon translocated to the host coincides, in general, with a The Journal of Experimental Biology 215, 1384-1393 © 2012. Published by The Company of Biologists Ltd doi:10.1242/jeb.065201