Award: OCE-1538151

Coral reefs worldwide have suffered catastrophic losses of calcifying (reef-building) organisms such as corals and crustose coralline algae (CCA). These calcifiers construct and cement the reef together, providing a complex three-dimensional structure for a diverse array of reef-associated species. This project examined an important, yet difficult to study, interaction between climate driven physical parameters, biological controls, and the disease ecology of a coralline fungal infection, recently identified by investigators on this project, for an understudied but critical component of reef ecosystems. Many tropical species of CCA are particularly sensitive to slight changes in temperature and pH in an experimental setting and our central hypothesis was that climate induced change will hasten the spread and severity of the coralline fungal disease (CFD). The exact mechanisms of how and why a previously healthy CCA host becomes infected by the pathogenic fungi are unclear. Thus the two major goals of the proposed research include: 1) a description of the CFD dynamics (incidence, prevalence, and mechanism of transmission across - and progression within - various coralline host species), and 2) an exploration of how climate-driven global change (i.e., rising SST and seawater acidity) will affect these dynamics using lab experiments and field observations. We used a combination of high-resolution, large-scale benthic imagery, intensive underwater surveying on SCUBA, and novel sensor technology arrayed across reef habitats on Palmyra Atoll to relate the spatial distribution of infected or resistant host CCA species, fungal colony-forming units, and environmental conditions over time in a natural setting at a reef-scale. High frequency time series of seawater pH, pCO2, salinity, and temperature data, calibrated and complemented by discrete sampling for additional carbonate parameters (total alkalinity and dissolved inorganic carbon), were related with biological data (disease prevalence, incidence, and host physiology). We noted the fate of tagged individual diseased CCA crusts over the course of one year following an outbreak of CFD associated with the 2015 El Nino event and subsequent anticipated recovery. From this work and concomitant field experiments using herbivore exclusion cages, we learned that infections are most prevalent near lagoonal outflows and persist in some locations beyond the duration of a thermal anomaly. However, coralline algae are capable of recovering from a fungal infection, particularly when grazing reef fish (e.g., parrotfish and surgeonfish) target fungal colony-forming units, or lesions (image 1); infected CCA that are not exposed to herbivores rapidly bleach and are replaced by fleshy macroalgae, algal turfs, and other invertebrates. Distribution of CFD lesions does not appear to be related to host density but may be more related to water quality. The herbivorous reef fish population at Palmyra Atoll, a wildlife refuge protected by the USFWS, represents sufficient grazing pressure (biomass and grazing rates) to prevent massive CCA die-off as a result of fungal infection, but less-protected reefs may be more vulnerable to CFD outbreaks. Our field measurements informed laboratory experiments that were performed at an organismal scale and designed to test alternative hypotheses about agents of disease progression within a calcareous host (e.g., fungal hyphal orientation) or transmission across hosts within a population. We verified that fungal lesions spread between host thalli via direct contact, but found no evidence yet to support waterborne or vector-based transmission. Histopathology yielded three new results: 1) fungal hyphae penetrate the host thallus through thinly calcified reproductive organs, particularly when exposed to warmer, more acidic seawater, 2) there is predominantly only one species of CCA suffering from CFD infections (Porolithon onkodes), and 3) it is likely that multiple types of fungi are present within a lesion (image 2). Ongoing genetics work supports our microscopy observation of multiple fungi and verifies that there is a singular CCA host species. The primary scientific and societal broader impacts of this project are advancing our ability to predict the future effects of climate change on disease outbreaks that negatively affect carbonate accretion and primary production of key taxa in coral reef ecosystems. Six primary publications were generated with this award, with another two manuscripts in preparation. This project also supported the education and training of highschool (1), undergraduate (5), and graduate (2) students and a postdoctoral scholar in an international arena. Stakeholders outside of academia were also engaged (e.g., the governor's Coral Reef Advisory Group in American Samoa and seaweed aquaculturists concerned about biosecurity of macroalgae in Maine, U.S.) and the general public was informed at a popular Cafe Scientifique. Last Modified: 03/29/2019 Submitted by: Nichole N Price