Vectors and environmental drivers of coral disease dynamics on the Great Barrier Reef

Coral diseases are causing significant levels of coral mortality at a global scale, based on the frequency of reports of disease and the rates of disease-related coral tissue loss worldwide. Of further concern is that the recent increase in the prevalence of coral diseases has been linked to environmental changes that can alter the outcome of host/pathogen interactions. Thus, coral diseases are expected to have increasing impacts on the structure and dynamics of coral populations and communities as the environment continues to change in the future. Despite the growing body of literature on the various diseases and pathogens that affect corals, the aetiology (i.e., causes of disease) and ecology (i.e., how the environment affects interactions between hosts and pathogens) and transmission of most coral diseases remain poorly understood. Understanding disease transmission mechanisms is critical to evaluate the potential impact of diseases on their host population. Diseases where pathogens cannot survive outside their hosts are unlikely to drive their host population to extinction, as the population would reach a threshold below which the pathogen cannot persist. In contrast, if the pathogen can infect multiple hosts, has reservoirs in the natural environment, and/or is transmitted by vectors, the disease prevalence can continue to increase even when host density is low, leading to diseasemediated population declines and extinctions. Ultimately, a comprehensive understanding of the ecology of pathogens, their vectors and environmental drivers, is required before outbreaks of coral disease can be understood and managed. The overarching objective of this thesis was to understand the aetiology of coral diseases and gain insights into the effects of diseases on coral populations. More specifically, I investigated the links between environmental factors and disease prevalence and progression rate on coral reefs at Lizard Island, for 1.5 years, and evaluated the role that vectors play in transmission of coral diseases. I also examined interactions among potential vectors, coral disease dynamics and the relative importance of multiple environmental stressors in order to determine if the outcomes of coral-vector-pathogen-environment interactions are positive or negative for corals. The specific aims of my PhD research were to; i) Evaluate the role of corallivorous fish in promoting or reducing progression rates of coral disease (Chapter 2); ii) Determine whether corallivores act as coral disease vectors, and understand the biological mechanism through which transmission occurs (Chapter 3); iii) Resolve coral disease contagiousness and transmission mechanisms by analysing spatio-temporal distribution patterns of naturally occurring coral diseases (Chapter 4); and iv) Understand the environmental drivers of disease dynamics, by quantifying how disease abundance and progression rates vary in response to environmental conditions (Chapter 5). Coral-feeding fishes (such as butterflyfishes) are known to feed on disease lesions, potentially affecting the rate of coral tissue loss (disease progression rate), and/or transmitting diseases among coral colonies. Although selective predation on lesions by corallivorous fish was observed, I found no evidence that removal of pathogens by fish reduced progression rates of black band disease (BBD) either in a controlled laboratory setting or in the natural environment. Variability in disease progression rates in the field was explained by inherent variation among coral colonies (24%) and among sampling days (38%) rather than by predation treatment (<0.1%). Furthermore, selective feeding on diseased tissue and subsequent predation on healthy colonies by corallivorous fish did not transmit either BBD or brown band disease (BrB) in the laboratory or in the field. In contrast, Drupella transmitted BrB to healthy corals in 40% of cases immediately following feeding on infected corals, and even in 12% of cases 12 and 24 hours following feeding. These results indicate that polyp-feeding fishes are unlikely to be vectors of coral diseases, possibly because their feeding creates small lesions that are too shallow for pathogens to invade coral tissues. Spatial and temporal distributions of disease prevalence and incidence provide insights into the cause, origin, and transmission mechanisms of diseases. For BBD and skeletal eroding band (SEB), the spatial patterns in disease incidence were often aggregated (i.e., in 78% and 66% of cases, respectively), suggesting that these two diseases are contagious. In contrast, incidences of white syndromes (WS) were randomly distributed; suggesting that this group of diseases is not contagious. The lack of a clear pattern in the distribution of BrB in analyses of quadrats over the 1.5 years suggests that multiple interacting factors culminate in BrB disease signs. Furthermore, the spatial distribution of most diseases (WS, SEB and BrB) was independent of the distribution of feeding scars created by Drupella snails and crown-of-thorns starfish. BBD, however aggregated around feeding scars in 43% of cases, suggesting that physical injury of the coral host might play a role in the transmission of BBD. My research demonstrates that progression rates of five common coral diseases (BBD, BrB, SEB, WS and atramentous necrosis) vary significantly with seasonal changes in environmental variables. Total dissolved nutrients (TDN) and seawater temperature were the most important factors affecting progression of coral diseases, with a general enhancement of progression rate at high temperature (>29°C) and high TDN (>6 μmol L⁻¹). Different environmental variables, however influenced the dynamics of the different diseases and non-linear, threshold relationships were observed. In contrast, there were no strong effects of environmental factors on the overall abundance of any of the five different coral diseases. Nevertheless, the increased rates of disease progression at increased seawater temperature and TDN suggest that declining water quality and ocean warming have the potential to exacerbate disease-related coral tissue loss. Overall, the results of my research demonstrate that both biotic (corallivorous snails and invertebrates) and abiotic (seawater temperature and water quality) factors influence the progression and transmission rate of coral diseases. Host condition and natural resistance of corals were also of great importance and played a greater role in disease dynamics than selective feeding by corallivorous fishes (Chapter 2). Corallivorous invertebrates, however create deeper feeding scars, and either directly transmitted disease to new hosts (Chapter 3) or indirectly increased the transmission rate of diseases by disrupting the coral's protective barrier (Chapter 4). Lastly, seawater temperature and total dissolved nutrients were the most important environmental factors that affect the progression rate of all coral diseases on the reef (Chapter 5). Reducing carbon dioxide emissions responsible for global warming and the increase in seawater temperature should remain the first priority of any management response. However, reducing land-based pollution, terrestrial runoff and seafloor dredging would moderate the impact of environmental stressors on coral diseases and may therefore be a powerful tool for lessening indirect human impacts (i.e. global warming) on coral reefs