The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host

Abstract

Bleaching (loss of symbiotic dinoflagellates) is known to significantly decrease the fitness of symbiotic marine invertebrates resulting in reduced growth, fecundity and survival. This report is the first to quantify the effects of bleaching on inorganic carbon (C i ) and ammonium flux, fixation and export of photosynthate to the host, in this case the giant clam Tridacna gigas . The 1998 bleaching event was found to decrease the zooxanthellae population 30-fold when comparing bleached to non-bleached clams. This resulted in significant increases in haemolymph C i and decreases in haemolymph pH and glucose concentration, the predominant photosynthate exported from zooxanthellae in this symbiosis. There was also a decrease in the expression levels of host carbonic anhydrase, an enzyme involved in C i transport to the zooxanthellae, and although host glutamine synthase levels were unaffected, the clams ability to assimilate ammonium was eliminated in bleached individuals, suggesting that photosynthate from the zooxanthellae is required for ammonium assimilation. In an artificial bleaching experiment haemolymph C i ( r 2 = = = = 0.97), pH ( r 2 = = = = 0.94) and glucose levels ( r 2 = = = = 0.95) were correlated to zooxanthellae numbers during both bleaching and recovery. Recovery of the zooxanthellae population, was enhanced four-fold by the addition of organic and inorganic nutrients, as were related haemolymph characteristics. These results highlight the profound physiological changes that occur in symbiotic organisms during and after a bleaching event.

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

“…The host supplies the symbiont with CO 2 and other compounds for cellular synthesis such as nitrogen and phosphorus (Trench, 1979;Allemand et al, 1998;Leggat et al, 2003;Weis et al, 2008). In turn, the symbiont supplies the host with more than 90% of its metabolic requirement, in the form of organic compounds including glucose, glycerol, fatty acids, and amino acids (Muscatine, 1990;Grant et al, 1997;Papina et al, 2003;Burriesci et al, 2012).…”

Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching

“…This, however, goes beyond these results and requires the analysis of protein concentrations, carbon translocation from symbiont to host, and tissue sections taken during the thermal treatments. The loss of tissue biomass can be explained either by host cell detachment (Gates et al 1992, Dunn et al 2002 or by a reduction in translocated carbon from the remaining symbionts (Leggat et al 2003).…”

Stress responses of zooxanthellae in juvenile Tridacna gigas (Bivalvia, Cardiidae) exposed to reduced salinity

“…However, the majority of research on climate change effects in the marine environment has focused on corals and sea anemones (Leggat et al, 2003). While similar effects may be expected in other symbiotic invertebrates, expulsion of zooxanthellae as a response to low salinity has not been reported in giant clams.…”

“…Bleaching has been reported in almost all zooxanthellate symbiotic marine invertebrates found on coral reefs such corals, sponges, sea anemones, and giant clams (Brown, 1997;Buck et al, 2002;Leggat et al, 2003). However, the majority of research on climate change effects in the marine environment has focused on corals and sea anemones (Leggat et al, 2003).…”

“…Environmental changes such as increasing temperature and high irradiance are known to cause expulsion of the zooxanthellae or bleaching (Brown, 1997;Douglas, 2003;Hoegh-Guldberg et al, 2007). The effects of bleaching are known to significantly decrease the fitness of the host-symbiont association, resulting in reduced growth, fecundity, and survival (Leggat et al, 2003). However, effects of changing climate do not limit to rising global temperatures but as well as changing weather patterns.…”