Coral histology reveals consistent declines in tissue integrity during a marine heatwave despite differences in...

Marine heatwaves are starting to occur several times a decade, yet we do not understand the effect this has on corals across biological scales. This study combines tissue-, organism-, and community-level analyses to investigate the effects of a marine heatwave on reef-building corals. Adjacent conspecific pairs of coral colonies of Montipora capitata and Porites compressa that showed contrasting phenotypic responses (i.e., bleached vs. not bleached) were first identified during a marine heatwave that occurred in 2015 in Kāne'ohe Bay, Hawai' i. These conspecific pairs of bleaching-resistant and bleaching-susceptible colonies were sampled for histology and photographed before, during, and after a subsequent marine heatwave that occurred in 2019. Histology samples were quantified for: (i) abundance of mesenterial filaments, (ii) tissue structural integrity, (iii) clarity of epidermis, and (iv) cellular integrity (lack of necrosis/granulation) on a 1-5 scale and averaged for an overall tissue integrity score. Tissue integrity scores revealed a significant decline in overall tissue health during the 2019 heatwave relative to the months prior to the heatwave for individuals of both species, regardless of past bleaching history in 2015 or bleaching severity during the 2019 heatwave. Coral tissue integrity scores were then compared to concurrent colony bleaching severity, which revealed that tissue integrity was significantly correlated with colony bleaching severity and suggests that the stability of the symbiosis is related to host tissue health. Colony partial mortality was also quantified as the cumulative proportion of each colony that appeared dead 2.5 years following the 2019 bleaching event, and tissue integrity during the heatwave was found to be strongly predictive of the extent of partial mortality following the heatwave for M. capitata but not P. compressa, the latter of which suffered little to no mortality. Surprisingly, bleaching severity and partial mortality were not significantly correlated for either species, suggesting that tissue integrity was a better predictor of mortality than bleaching severity in M. capitata. Despite negative effects of heat stress at the tissue- and colony-level, no significant changes in coral cover were detected, indicating resilience at the community level. However, declines in tissue integrity in response to heat stress that are not accompanied by a visible bleaching response may still have long-term consequences for fitness, and this is an important area of future investigation as heat stress is commonly associated with long-term decreases in coral fecundity and growth. Our results suggest that histology is a valuable tool for revealing the harmful effects of marine heatwaves on corals before they are visually evident as bleaching, and may thus improve the predictability of ecosystem changes following climate change-driven heat stress by providing a more comprehensive assessment of coral health.