Warming and pollutants interact to modulate octocoral immunity and shape disease outcomes

Abstract

Warming environments can alter the outcome of host-parasite relationships with important consequences for biodiversity. Warming often increases disease risk, and interactions with other environmental factors can intensify impacts by modifying the underlying mechanisms, such as host immunity. In coastal ecosystems, metal pollution is a pervasive stressor that influences disease and immunity in many organisms. Despite the crisis facing coral reefs, which stems in part from warming-associated disease outbreaks, the impacts of metal pollutants on scleractinian and octocoral disease are largely unknown. We investigated how warming oceans and copper pollution affect host immunity and disease risk for two diseases of the abundant Caribbean octocoral, the sea fan Gorgonia ventalina. Field surveys across a sediment copper concentration gradient in Puerto Rico, USA revealed that cellular immunity of sea fans increased by 12.6% at higher sediment copper concentrations, while recovery from multifocal purple spots disease (MFPS) tended to decrease. MFPS severity in the field increased at warmer sites. In a controlled laboratory experiment, sea fans were inoculated with live cultures of a labyrinthulid parasite to test the interactive effects of temperature and copper on immune activation. As in the field, higher copper induced greater immunity, but the factorial design of the experiment revealed that copper and temperature interacted to modulate the immune response to the parasite: immune cell densities increased with elevated temperature at lower copper concentrations, but not with high copper concentrations. Tissue damage was also greater in treatments with higher copper and warmer temperatures. Field and lab evidence confirm that elevated copper hinders sea fan immune defenses against damaging parasites. Temperature and copper influenced host-pathogen interactions in octocorals by modulating immunity, disease severity, and disease recovery. This is the first evidence that metal pollution affects processes influencing disease in octocorals and highlights the importance of immune mechanisms in environmentally mediated disease outbreaks. Although coral conservation efforts must include a focus on global factors, such as rapid warming, reducing copper and other pollutants that compromise coral health on a local scale may help corals fight disease in a warming ocean.

Keywords: Puerto Rico; copper pollution; coral; disease; global warming; interactions.