Algal symbionts increase oxidative damage and death in coral larvae at high temperatures

Abstract

Mutualisms are often viewed as reciprocal exploitations that nonetheless provide net benefits to each partner. While the benefits of symbiosis with dinoflagellates of the genus Symbiodinium (zooxanthellae) for corals are well understood, the costs of the association, particularly when under stress, remain a focus of much research. One of the primary impediments to exploring the costs of symbiosis in zooxanthellate corals is that it is impossible to examine the animal host in isolation. Evidence for a cost of symbiosis with zooxanthellae includes the fact that direct transmission of zooxanthellae between generations is rare, particularly in broadcast spawning corals. Fortuitously, the absence of zooxanthellae in oocytes of many species and the ability to readily infect larvae with zooxanthellae provide an opportunity to compare individuals with and without these symbionts. Here, we use this larval model to show that individuals with zooxanthellae have lower survival than those lacking zooxanthellae when exposed to high temperature. Higher activity of anti-oxidant defenses and higher levels of oxidative cellular damage in larvae with zooxanthellae suggest that oxidative stress originating in the symbionts is a cause of tissue damage in the host under heat stress. We hypothesize that this may be one reason for the absence of direct transmission of zooxanthellae in most broadcast spawning corals whose propagules must spend at least 1 d on the ocean surface.

Differential coral bleaching—Contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress

“…the applied heating rate in the experimental setup. Low heating rates profoundly delay the physiological response of the coral holobiont (Middlebrook et al, 2010) and the ramping rate of 1°C day -1 used in the current study is considerably slower than in previous studies of antioxidant responses under thermal stress; these applied heating rates ranging from near-instantaneous to 4°C hour -1 (Yakovleva et al, 2004;Richier et al, 2005;Higuchi et al, 2008;Yakovleva et al, 2009;Higuchi et al, 2012;Downs et al, 2013;T. Higuchi and I. Yakovleva, personal communication).…”

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

“…For adult and larval hosts alike, the presence of symbionts is generally regarded as positive for coral reef larvae development and fitness, but under thermal stress it may have the opposite effect. High temperatures cause the symbionts to become a source of reactive oxygen species (ROS), which leads to significantly higher larval mortality (Weis, 2008;Baird et al, 2009;Yakovleva et al, 2009;Schnitzler et al, 2012). Some of the effects of ROS include DNA damage and higher rates of antioxidant activity (Yakovleva et al, 2009;Nesa et al, 2012).…”

Temperature Dependence of Respiration in Larvae and Adult Colonies of the Corals Acropora tenuis and Pocillopora damicornis

“…Stress-exposure experiments with Acropora planulae inoculated with symbionts show that symbiotic planulae are more sensitive to high temperature and strong light stress than that of non-symbiotic planulae [15,16]. Acropora planulae inoculated with homologous Symbiodinium cells suffer more severe oxidative damage than that of non-symbiotic planulae [15,16]. However, it is unknown whether symbiotic coral planulae with a vertical mode of symbiont transmission are more vulnerable to oxidative damage than non-symbiotic coral planulae with a horizontal mode of symbiont transmission.…”

“…Stress-exposure experiments with Acropora planulae inoculated with symbionts show that symbiotic planulae are more sensitive to high temperature and strong light stress than that of non-symbiotic planulae [15,16]. Acropora planulae inoculated with homologous Symbiodinium cells suffer more severe oxidative damage than that of non-symbiotic planulae [15,16].…”