Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type

Abstract

Coral bleaching has been identified as one of the major contributors to coral reef decline, and the occurrence of different symbionts determined by broad genetic groupings (clades A-H) is commonly used to explain thermal responses of reef-building corals. By using Stylophora pistillata as a model, we monitored individual tagged colonies in situ over a two-year period and show that fine level genetic variability within clade C is correlated to differences in bleaching susceptibility. Based on denaturing gradient gel electrophoresis of the internal transcribed spacer region 2, visual bleaching assessments, symbiont densities, host protein, and pulse amplitude modulated fluorometry, we show that subcladal types C78 and C8/a are more thermally tolerant than C79 and C35/a, which suffered significant bleaching and postbleaching mortality. Although additional symbiont types were detected during bleaching in colonies harboring types C79 and C35/a, all colonies reverted back to their original symbionts postbleaching. Most importantly, the data propose that the differential mortality of hosts harboring thermally sensitive versus resistant symbionts rather than symbiont shuffling/switching within a single host is responsible for the observed symbiont composition changes of coral communities after bleaching. This study therefore highlights that the use of broad cladal designations may not be suitable to describe differences in bleaching susceptibility, and that differential mortality results in a loss of both symbiont and host genetic diversity and therefore represents an important mechanism in explaining how coral reef communities may respond to changing conditions.

Fig. 1.

Seawater temperatures recorded from 2002 to 2006 at Heron Island on the southern Great Barrier Reef (June 2003 to June 2004, no data available). (Inset Right) Average (maximum, minimum) summer and winter temperatures. Water temperatures did not differ significantly between the deep (15–18 m) and shallow (3–6 m), but regional bleaching was evident in 2002 and 2006 when the long-term summer average (Tmean) or maximum (Tmax) was exceeded for prolonged periods. (Inset Left) Tagged Stylophora pistillata colony in March 2005 (healthy) and March 2006 (bleached).

Fig. 2.

Bleaching susceptibility and recovery of Stylophora pistillata colonies as a function of symbiont type. (A) Left axis: Cumulative histogram of the in situ visual assessments of bleaching susceptibility of S. pistillata colonies as a factor of symbiont type. Right axis: Symbiont cell loss expressed as a percentage loss (± SE) because bleaching by comparing March 2006 (bleached) with March 2005 (normal). (B) The recovery potential of S. pistillata colonies as a factor of symbiont type based on in situ visual assessments 8 months postbleaching (November 2006). Visual assessments were divided into categories: completely healthy, bleached, 10–20% mortality, >50% mortality, or total colony mortality. Number of examined colonies is shown in parentheses below the symbiont types.

Fig. 3.

ITS2-DGGE symbiont profiles of seven individual colonies of S. pistillata at three time points: N5 (November 2005, prebleaching), M6 (March 2006, during bleaching), and N6 (November 2006, 8 months postbleaching). March 2005 profiles were identical to November 2005 and are not shown. Symbiont profiles C79 (colonies 1–3) and C35/a (colonies 4 and 5) showed additional bands belonging to symbiont types C8/a, C78, C35/a, or C1^unk during bleaching (M6), whereas C8/a and C78 profiles (colonies 6 and 7) remained stable. Representative characteristic bands that were sequenced are marked on the gel, and all sequences belong to known ITS2-DGGE types except C1^unk. The lowest C8/a band represents a previously identified pseudogene (C8/a-ps) (29) and HD indicates a heteroduplex formed during PCR. Symbiont designation is shown below each lane; + indicates a symbiont is present other than the original. *C78a was wrongly identified as C1 in ref. . Sequence C78a contains a 1bp deletion difference from C1 and occurs in conjunction with C78.

Fig. 4.

Changes in the symbiont community structure in Stylophora pistillata based on random versus repeated sampling methodologies. (A) Random assessments of postbleaching community structure do not account for symbiont-specific colony mortality and subsequently show a marked change in the relative proportions of symbionts present on the reef. (B) Repeated sampling highlights the importance of symbiont-specific differential colony mortality as a result of bleaching. The hatched lines represent the relative abundance of dead colonies within each symbiont type. Comparing mechanisms of path A versus B highlights that shifts in the symbiont community are driven by differential mortality as opposed to sustained changes in symbiont types of individual colonies.