Heat stress differentially impacts key calcification mechanisms in reef-building corals

Abstract

Coral reefs are increasingly threatened by climate change, mass bleaching events and ocean acidification (OA). Coral calcification, a process that is critical to build and maintain the structure of tropical coral reefs, is highly sensitive to both warming and acidifying oceans. However, in contrast to the impacts of OA on coral calcification, significant knowledge gaps remain regarding how coral biomineralization mechanisms are impacted by heat stress and bleaching. Using a combined physiological and geochemical approach, we investigated how a marine heatwave impacted coral symbiotic status (chlorophyll a, algal symbiont density), the carbonate chemistry of the coral calcifying fluid (via d 11 B and B/Ca) and skeletal trace element composition in the branching coral Acropora aspera. Importantly, we recorded in situ temperature throughout the bleaching event and recovery as well as coral symbiotic status during peak bleaching and after 7 months of recovery. We show that heat-stressed Acropora corals continued to upregulate the pH of their calcifying fluid (cf); however, dissolved inorganic carbon upregulation inside the cf was significantly disrupted by heat stress. Similarly, we observed suppression of the typical seasonality in the trace element (TE) temperature proxies Sr/Ca, Mg/Ca, Li/Ca and Li/Mg, indicating disruption of important calcification mechanisms, Rayleigh fractionation and reduced growth rates. Anomalies in TE/ Ca ratios were still observed 7 months after peak bleaching, even though algal symbiont densities and chlorophyll a concentrations were fully restored at this point. Interestingly, the biomineralization response to heat stress did not differ between thermally distinct reef habitats harbouring coral populations with different heat tolerance, nor between heat-stressed colonies with different severity of bleaching. Our findings suggest that coral biomineralization mechanisms in Acropora are highly sensitive to heat stress, showing similar patterns of biogeochemical stress response as other coral taxa. Keywords Calcification mechanisms Á Heat stress Á Coral bleaching Á Calcifying fluid Á Boron isotopes Á Trace elements Topic Editor Simon Davy

Marginal Reefs Under Stress: Physiological Limits Render Galápagos Corals Susceptible to Ocean Acidification and Thermal Stress

“…However, our results are based on relatively few data following this stress event, limiting the significance of these changes (Figure S6a in Supporting Information ); similar analyses of additional stress events would clarify these patterns and improve interpretations of calcification and skeletal geochemistry following thermal stress and bleaching. Nevertheless, these results are consistent with other recent studies demonstrating acute impacts of thermal stress on pH cf and skeletal geochemistry (Cheung et al., 2021; Clarke et al., 2017, 2019; D’Olivo & McCulloch, 2017; D’Olivo et al., 2019; M. T. McCulloch et al., 2017; Guillermic et al., 2020; Ross et al., 2017; Schoepf et al., 2021).…”

“…Similar reductions in DIC cf upregulation are observed during other warm extremes in the modern record, whereas DIC upregulation is highest during warm periods in the fossil record. Our results therefore add to the growing body of work identifying adverse effects of thermal stress and bleaching on coral CF chemistry under ocean warming (Cheung et al., 2021; Dishon et al., 2015; D’Olivo & McCulloch, 2017; D’Olivo et al., 2019; Schoepf et al., 2015, 2021). The changes in DIC upregulation identified here imply that extreme thermal stress undermines coral health via photosynthetic reductions that coincide with weak upwelling (and thus feeding capacity); together, these changes deprive the colony of the energy needed to drive the Ca‐ATPase pump and/or other active pathways (e.g., other alkalinity pumps or paracellular transport) that upregulate pH cf , leaving them more susceptible to regional changes in DIC sw and pH sw .…”

Marine heatwaves depress metabolic activity and impair cellular acid–base homeostasis in reef‐building corals regardless of bleaching susceptibility

“…Furthermore, if pH i in corals is regulated more tightly than extracellular body fluids (pH e ) during stress, as it is in other marine invertebrates (Tresguerres et al, 2020), the interactive effects of temperature stress and hypercapnia on pH i and pH e regulation may be particularly detrimental for biomineralization, which occurs in extracellular pockets of fluid located between the coral epidermis and the skeleton. Indeed, recent work has found that heat stress impairs coral regulation of calcifying fluid pH e with concurrent declines in calcification (Guillermic et al, 2021;Schoepf et al, 2021), which raises the question of whether coral pH i maintenance may be occurring at the expense of pH e during stress. Because the dynamics and mechanisms of acid-base regulation differ greatly between species and cell types (Tresguerres et al, 2017(Tresguerres et al, , 2020, it is critical that future work describes the molecular mechanisms that dictate these organismal responses to climate change stressors in order to better predict their ability to acclimatize and adapt to the ongoing climate crisis.…”

“…The potential effects of heat stress on acid–base regulation pose a particular challenge for maintaining coral calcification, as biomineralization is highly pH‐dependent (Barott et al, 2020; McCulloch et al, 2012; Venn et al, 2011, 2012). Indeed, recent studies have found that temperature stress alters the pH of the external calcifying fluid and depresses calcification (Guillermic et al, 2021; Schoepf et al, 2021), highlighting the need to better understand the physiology of coral climate change responses across biological scales.…”

Adaptive Responses of the Sea Anemone Heteractis crispa to the Interaction of Acidification and Global Warming

“…Studies of the effects of acidification on corals have commonly focused on calcification [ 15 , 16 , 17 , 18 , 19 ], growth [ 20 , 21 , 22 ], physiology [ 23 , 24 , 25 ], and phenotype [ 26 , 27 ], with only a few studies reporting that acidification is associated with coral bleaching [ 28 , 29 ]. Indeed, a large body of literature has demonstrated that global warming affects the coral community [ 30 , 31 ], and its health [ 32 , 33 , 34 ], metabolism [ 33 , 35 , 36 , 37 ], and calcification [ 38 , 39 ].…”