Deciphering coral disease dynamics: integrating host, microbiome, and the changing environment

Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations

Tipping the balance: the impact of eelgrass wasting disease in a changing ocean

Infectious disease has the potential to cause devastating damage to valuable marine organisms and habitats. Eelgrass wasting disease (EGWD), caused by the pathogenic protist Labyrinthula zosterae (LZ), has caused mass die-offs in Zostera marina at regional and global scales. Despite this, little is known about the host-pathogen interaction or disease drivers in the Salish Sea. To determine the regional impact of EGWD, we measured summer prevalence and severity in the San Juan Islands, Padilla Bay, Hood Canal, South Puget Sound, and Willapa Bay. We used cultures and quantitative PCR to verify results, measuring LZ load in lesioned tissue from multiple sites. EGWD was present at all 16 sites surveyed, with prevalence ranging from 80% disease prevalence. Recent data suggest water temperature increases the virulence of LZ, indicating possible climate sensitivity. At our sites, water temperatures influenced both EGWD prevalence and severity, suggesting environmental conditions and climate change could impact the eelgrass-LZ relationship and lead to increased virulence. We ran a three-week controlled experiment to examine the impact of LZ infection on eelgrass shoots over time. We exposed half the eelgrass shoots to LZ infection and sampled shoots at seven time points. All exposed shoots showed signs of infection. EGWD severity and lesion number increased through time, corresponding with a measurable decrease in leaf and root growth and increased phenols. Our results show EGWD is widespread in Washington state eelgrass beds and suggests that EGWD severity is positively correlated with water temperature. Furthermore, EGWD has a detrimental effect on eelgrass health, potentially contributing to decreased density and meadow declines. While levels of EGWD in the field are variable, we identified four sites that are experiencing high prevalence. Further research is needed to understand the conditions leading to EGWD outbreaks

DOSAGE-CONTROLLED STUDIES OF EELGRASS WASTING DISEASE: PHENOLOGY OF INFECTION AND FACTORS MODERATING VIRULENCE

Supplemental file(s) description: Chapter 1 Data, Chapter 1 R Script, Chapter 2 DataCoinciding with increased anthropogenic stressors and climate change, many marine diseases are on the rise. Understanding the epidemiology of marine disease that affect ecologically, economically, and culturally important species is a priority, but also a challenge given the nature of marine systems. In the first chapter of this thesis, we conduct a dosage-controlled inoculation method to enable quantitative investigations of aspects of phenology of eelgrass wasting disease infection, namely timescales and descriptors of characteristic infection, timescales of immunodynamics of newly established EGWD lesions and growth consequences of infection to the host over time. Observations of developing lesions showed that lesions first became visible 2 days post pathogenic exposure and leaf tissue can become totally necrotic in as soon as 12 days and furthermore suggested that the outcome of infection is largely contingent on the genotype of the host. Growth of plants that have been exposed to the pathogen are significantly lower than control plants by 12 days. Immuno-response as measured by induction of phenols is significantly higher in treatment plants by 12 days into the time series, and phenolic production is positively correlated with higher disease severity by the end of the experiment at 20 days. The second chapter investigates factors affecting severity of infection, namely pathogenic isolates, pathogen dosage, temperature, and light. Severity of lesions on eelgrass varied among the 3 different isolates inoculated in laboratory trials. Disease severity increased with pathogen dosage from 104 to 106 cells ml−1. In a dosage-controlled light and temperature 2-way factorial experiment consisting of 2 light regimes (diel light cycle and complete darkness) and 2 temperatures (11 and 18°C), L. zosterae cell growth rate in vitro was higher at the warmer temperature. In a companion experiment that tested the effects of light and temperature in in vivo inoculations, disease severity was higher in dark treatments and temperature was marginally significant. Although the details of these studies are specific to infection of the eelgrass Zostera marina by the protist Labyrinthula zosterae, it provides a general modeling framework for studying the role of within-host disease dynamics in other increasing marine diseases. Our work with controlled inoculation methods evaluate EGWD host-pathogen interactions narrowing the knowledge gap of phenology of infection and factors affecting virulence of a widespread and historically devastating disease

EeLISA: Combating Global Warming Through the Rapid Analysis of Eelgrass Wasting Disease

Global warming is the greatest threat facing our planet, and is causing environmental disturbance at an unprecedented scale. We are strongly positioned to leverage the advancements of Artificial Intelligence (AI) and Machine Learning (ML) which provide humanity, for the first time in history, an analysis and decision making tool at massive scale. Strong evidence supports that global warming is contributing to marine ecosystem decline, including eelgrass habitat. Eelgrass is affected by an opportunistic marine pathogen and infections are likely exacerbated by rising ocean temperatures. The necessary disease analysis required to inform conservation priorities is incredibly laborious, and acts as a significant bottleneck for research. To this end, we developed EeLISA (Eelgrass Lesion Image Segmentation Application). EeLISA enables ecologist experts to train a segmentation module to perform this crucial analysis at human level accuracy, while minimizing their labeling time and integrating into their existing workflow. EeLISA has been deployed for over 16 months, and has facilitated the preparation of four manuscripts including a critical eelgrass study ranging from Southern California to Alaska. These studies, utilizing EeLISA, have led to scientific insight and discovery in marine disease ecology

Towards a systematics of ecodiversity: The EcoSyst framework

Background Although a standard taxonomy of organisms has existed for nearly 300 years, no consensus has yet been reached on principles for systematization of ecological diversity (i.e., the co‐ordinated variation of abiotic and biotic components of natural diversity). In a rapidly changing world, where nature is under constant pressure, standardized terms and methods for characterization of ecological diversity are urgently needed (e.g., to enhance precision and credibility of global change assessments). Aim The aim is to present the EcoSyst framework, a set of general principles and methods for systematization of natural diversity that simultaneously addresses biotic and abiotic variation, and to discuss perspectives opened by this framework. Innovation EcoSyst provides a framework for systematizing natural variation in a consistent manner across different levels of organization. At each ecodiversity level, EcoSyst principles can be used to establish: (a) an extensive attribute system with descriptive variables that cover all relevant sources of variation; (b) a hierarchical‐type system; and (c) a set of guidelines for land‐cover mapping that is consistent across spatial scales. EcoSyst type systems can be conceptualized as multidimensional models, by which a key characteristic (the response) is related to variation in one or more key sources of variation (predictors). EcoSyst type hierarchies are developed by a gradient‐based iterative procedure, by which the “ecodiversity distance” (i.e., the extent to which the key characteristic differs between adjacent candidate types) is standardized and the ecological processes behind observed patterns are explicitly taken into account. Application We present “Nature in Norway” (NiN), an implementation of the EcoSyst framework for Norway for the ecosystem and landscape levels of ecodiversity. Examples of applications to research and management are given. Conclusion The EcoSyst framework provides a theoretical platform, principles and methods that can complement and enhance initiatives towards a global‐scale systematics of ecodiversitypublishedVersio