Environmental conditions modulate constitutive and induced host immunity contributing to spatial patterns of coral disease susceptibility

Abstract Disease outbreaks have caused mass mortality and threaten the persistence of numerous vulnerable species, including reef-building corals. Spatiotemporal variations in disease prevalence suggest environmental conditions exacerbate disease susceptibility, potentially by compromising host immunity. Understanding how these variations influence disease dynamics and immunity may enable improved prediction of future disease outbreaks. We combined field observations and statistical modeling to identify the environmental drivers of stony coral tissue loss disease (SCTLD) in Florida. We then performed environmental manipulation experiments to confirm the effects of identified factors on immunity in the massive coral Montastraea cavernosa. SCTLD susceptibility was influenced most by the interaction between temperature and chlorophyll-a concentration (nutrients proxy) the month prior to disease survey, as well as the interaction between chlorophyll-a and three-month mean PAR. SCTLD prevalence was highest when temperatures were low (<30 °C) and chlorophyll-a concentration exceeded ∼6 mg m-3 and/or when PAR and chlorophyll-a concentrations were high. SCTLD severity had a negative relationship with temperature, a colony had a higher probability of dying during the SCTLD outbreak when temperatures stayed below 31.08 °C, a finding in contrast to previous coral disease studies. In the laboratory, coral fragments were exposed to temperature and nutrient manipulation, then immune challenged. Heat stress largely drove suppression of baseline immunity but increased production of some antioxidants, suggesting host stress. Fragments exposed to moderate ammonium concentration induced the strongest immune responses compared to those grown under high or no ammonium conditions. Combined with modeling results, these findings support long-standing hypotheses that coral disease susceptibility is at least, in part, modulated by environmentally induced changes in immunity. Overall, our results enhance the understanding of the impact of environmental conditions on SCTLD outbreaks and on general coral immunity. They also highlight the possibility of increased disease severity as anthropogenic pressure on marine environments increases. Competing Interest Statement The authors have declared no competing interest. Footnotes ↵$ Nicholas P. Jones and Sydney Dutton should be considered joint first author