Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress

Abstract

Symbiotic scleractinian corals are particularly affected by climate change stress and respond by bleaching (losing their symbiotic dinoflagellate partners). Recently, the energetic status of corals is emerging as a particularly important factor that determines the corals’ vulnerability to heat stress. However, detailed studies of coral energetic that trace the flow of carbon from symbionts to host are still sparse. The present study thus investigates the impact of heat stress on the nutritional interactions between dinoflagellates and coral Stylophora pistillata maintained under auto- and heterotrophy. First, we demonstrated that the percentage of autotrophic carbon retained in the symbionts was significantly higher during heat stress than under non-stressful conditions, in both fed and unfed colonies. This higher photosynthate retention in symbionts translated into lower rates of carbon translocation, which required the coral host to use tissue energy reserves to sustain its respiratory needs. As calcification rates were positively correlated to carbon translocation, a significant decrease in skeletal growth was observed during heat stress. This study also provides evidence that heterotrophic nutrient supply enhances the re-establishment of normal nutritional exchanges between the two symbiotic partners in the coral S. pistillata, but it did not mitigate the effects of temperature stress on coral calcification.

Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses

“…Symbiont's food is also shared between symbiotic and non-symbiotic tissues, as demonstrated in jellyfish, for which 13 Clabeled compounds are translocated from photosymbiont-rich oral arm tissue to bell tissue (Freeman, Stoner, Easson, Matterson, & Baker, 2017). In corals, by coupling light and dark bottle incubations (P/R) with 13 C-bicarbonate tracers (Figure 8), it was shown that the percentage of autotrophic carbon assimilated by the symbionts (Z2 in Figure 8), translocated (Z3), and retained in the host tissue (Z5), or lost as respiration and mucus (Z6) depends on the environment and trophic state of the symbiotic association (Baker et al, , 2018Tremblay et al, 2016). Therefore, under low light (i.e., limited autotrophic acquisition) or warm conditions, coral symbionts sequester more resources for their own growth, thus parasitizing their hosts ( Figure 8, pie charts).…”

Nutrient starvation impairs the trophic plasticity of reef‐building corals under ocean warming

“…This indicates that corals under control conditions were able to regulate the loss in autotrophic capacities by maintaining or increasing heterotrophic activities. It is well known that plankton supplementation prevents damage to the photosynthetic apparatus (Borell & Bischof, ; Connolly, Lopez‐Yglesias, & Anthony, ; Ferrier‐Pagès, Sauzéat, & Balter, ; Tremblay, Gori, Maguer, Hoogenboom, & Ferrier‐Pagès, ), lowers coral bleaching susceptibility (Grottoli et al, ; Hughes & Grottoli, ) and can further enhance the re‐establishment of photosynthate transfer following heat stress (Tremblay et al, ). Hughes and Grottoli () showed that some coral species can increase rates of heterotrophic carbon acquisition in host tissues for almost a year following bleaching in order to either compensate for the autotrophic loss of energy or prevent the effect of subsequent elevated temperature.…”

Impact of diurnal temperature fluctuations on larval settlement and growth of the reef coral <i>Pocillopora damicornis</i>

“…Firstly, the paling of recruits at elevated temperatures as a result of pigment dilution will enhance their internal light fields, which could bring about a 2-to 3-fold increase in symbiont-specific productivity (Wangpraseurt et al, 2017) and in turn support skeletal growth and asexual budding. Secondly, since coral calcification is positively correlated with carbon translocation between Symbiodinium and the host (Tremblay et al, 2016), the elevated calcification and growth at 31 • C indicates more efficient nutritional exchange, sustaining the metabolic expenditure of faster development. This interpretation is further supported by the excessive deviation of Q 10 from the kinetic expectations (2-3): this signifies a strong amplifying effect through changes in fundamental biochemical systems along with the acceleration of functional enzyme activities at increased temperatures (Hochachka and Somero, 2002).…”