Mass coral bleaching has increased in intensity and frequency and has severely impacted shallow tropical reefs worldwide. Although extensive investigation has been conducted on the resistance and resilience of coral reefs in the Indo-Pacific and Caribbean, the unique reefs of the South Atlantic remain largely unassessed. Here we compiled primary and literature data for reefs from three biogeographical regions: Indo-Pacific, Caribbean and South Atlantic and performed comparative analyses to investigate whether the latter may be more resistant to bleaching. Our findings show that South Atlantic corals display critical features that make them less susceptible to mass coral bleaching: (i) deeper bathymetric distribution, as species have a mean maximum depth of occurrence of 70 m; (ii) higher tolerance to turbidity, as nearly 60% of species are found in turbid conditions; (iii) higher tolerance to nutrient enrichment, as nitrate concentration in the South Atlantic is naturally elevated; (iv) higher morphological resistance, as massive growth forms are dominant and comprise two thirds of species; and (v) more flexible symbiotic associations, as 75% of corals and 60% of symbiont phylotypes are generalists. Such features were associated with occurrence of fewer bleaching episodes with coral mortality in the South Atlantic, approximately 60% less than the Indo-Pacific and 50% less than the Caribbean. In addition, no mass coral mortality episodes associated with the three global mass bleaching events have been reported for the South Atlantic, which suffered considerably less bleaching. These results show that South Atlantic reefs display several remarkable features for withstanding thermal stress. Together with a historic experience of lower heat stress, our findings may explain why climate change impacts in this region have been less intense. Given the large extension and latitudinal distribution of South Atlantic coral reefs and communities, the region may be recognized as a major refugium and likely to resist climate change impacts more effectively than Indo-Pacific and Caribbean reefs.
Symbiodinium are responsible for the majority of primary production in coral reefs and found in a mutualistic symbiosis with multiple animal phyla. However, little is known about the molecular signals involved in the establishment of this symbiosis and whether it initiates during host larval development. To address this question, we monitored the expression of a putative symbiosis-specific gene (H+-ATPase) in Symbiodinium A1 ex hospite and in association with larvae of a scleractinian coral (Mussismilia hispida), a nudibranch (Berghia stephanieae) and a giant clam (Tridacna crocea). We acquired broodstock for each host, induced spawning and cultured the larvae. Symbiodinium cells were offered and larval samples taken for each host during the first 72 h after symbiont addition. In addition, control samples including free-living Symbiodinium and broodstock tissue containing symbionts for each host were collected. RNA extraction and RT-PCR were performed and amplified products cloned and sequenced. Our results show that H+-ATPase was expressed in Symbiodinium associated with coral and giant clam larvae, but not with nudibranch larvae, which digested the symbionts. Broodstock tissue for coral and giant clam also expressed H+-ATPase, but not the nudibranch tissue sample. Our results of the expression of H+-ATPase as a marker gene suggest that symbiosis between Symbiodinium and M. hispida and T. crocea is established during host larval development. Conversely, in the case of B. stephanieae larvae, evidence does not support a mutualistic relationship. Our study supports the utilization of H+-ATPase expression as a marker for assessing Symbiodinium–invertebrate relationships with applications for the differentiation of symbiotic and non-symbiotic associations. At the same time, insights from a single marker gene approach are limited and future studies should direct the identification of additional symbiosis-specific genes, ideally from both symbiont and host.
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