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Shellfish fisheries and aquaculture within the Chesapeake Bay (hereafter 'the Bay') and its tributaries have been historically impacted by disease and climate events. Climate-driven shifts in temperature and salinity can alter host-parasite dynamics, influencing outbreaks. Here, we explore the relationship between temperature, salinity and parasite distribution and abundance in the eastern oysterCrassostrea virginica-Perkinsus marinussystem. We use long-term (30 yr) environmental data andP. marinussurveys in the Bay to identify (1) how climate affectsP. marinusprevalence and intensity, (2) seasonal and climate-driven infection patterns, and (3) regional environmental influences on disease. We found significant relationships betweenP. marinusinfection intensity, prevalence, increasing temperature and decreasing salinity. Our results indicated that there is an overall decreased abundance ofP. marinusprevalence and intensity throughout the Bay driven by decreases in salinity over time, most prominently from 2003-2020. However, these temporal trends in prevalence and intensity vary largely by region, with some regions still experiencing high disease burden. Examining monthly environmental parameters reinforced the dominant role of salinity in driving disease patterns. Salinity had significant relationships with prevalence and intensity year-round, with the largest effects in late spring/early summer. Monthly temperatures had fewer significant relationships to prevalence and intensity, but the largest significant effects were seen in late winter/early spring. Notably, this study is the first to document that winter salinity influences fall parasite prevalence, sometimes exerting a greater effect than temperature. Continued and expanded monitoring of marine disease is crucial to understand how the changing climate is impacting disease. 

Abstract Infectious disease plays a key role in shaping marine communities, including in seagrass meadows, which form biodiverse coastal habitats. Eelgrass (Zostera marina) is the most widespread seagrass species and is susceptible to seagrass wasting disease, caused by the protist Labyrinthula zosterae. As a foundation species, eelgrass strongly influences ecosystem structure, function and services; recent work has begun to explore the links between critical community interactions and seagrass wasting disease. Here, we highlight recent advances about how the eelgrass community regulates and responds to seagrass wasting disease, from the microbiome to herbivores and filter feeders. We further show how efforts to model seagrass wasting disease progression can build on prior efforts to predict eelgrass growth and productivity and can inform our understanding of ecosystem health, resilience and vulnerability. As climate change alters environmental conditions, potentially favouring the wasting disease pathogen, efforts to integrate community interactions with disease ecology will be critical to forecast ecosystem dynamics and to develop effective coastal management strategies. We offer guidance on addressing major knowledge gaps in the study of eelgrass wasting disease in order to deepen both ecological theory and applied practices and identify how an integrated marine-disease-community ecology can inform a broader, cross-cutting understanding of disease. 

Abstract Although invertebrate herbivores commonly impact terrestrial plant diseases by facilitating transmission of plant pathogens and increasing host susceptibility to infection via wounding, less is known about the role of herbivores in marine plant disease dynamics. Importantly, transmission via herbivores may not be required in the ocean since saline ocean waters support pathogen survival and transmission. Through laboratory experiments with eelgrass (Zostera marina), we showed that isopods (Pentidotea wosnesenskii) and snails (Lacunaspp.) created grazing scars that increased disease severity and thus indirectly facilitated transmission ofLabyrinthula zosterae(Lz), a protist that causes seagrass wasting disease. Experiments also quantified different feeding preferences among herbivores: Amphipods (Ampithoe lacertosa) selectively consumed diseased eelgrass, while isopods and snails selectively grazed asymptomatic leaves, suggesting different herbivore taxa may have contrasting impacts on disease dynamics. Our experiments show no sign that herbivores directly vector Lz from diseased to asymptomatic eelgrass. However, we isolated live Lz from isopod, amphipod, and snail feces and detected Lz with quantitative polymerase chain reaction in amphipods and snails, suggesting that herbivores eating diseased eelgrass could pass the live pathogen. Finally, field surveys demonstrated a close association between seagrass wasting disease and invertebrate grazing scars; disease prevalence was 29 ± 4.7% (95% CI) higher on eelgrass leaves with herbivore scars. Collectively, these findings show that some herbivores can increase eelgrass disease risk by facilitating the spread of an important pathogen via wounding, but not via direct transmission. Thus, herbivores may play different roles in plant disease dynamics in terrestrial versus marine ecosystems depending on the pathogen's ability to survive and transmit without a vector. 

IntroductionSeagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunisticLabyrinthulaspp., is an increasing concern with rising seawater temperature. To better understand the host-pathogen interaction, we paired whole organism physiological assays with dual transcriptomic analysis of the infected host and parasite. MethodsEelgrass (Zostera marina) shoots were placed in one of two temperature treatments, 11° C or 18° C, acclimated for 10 days, and exposed to a waterborne inoculation containing infectiousLabyrinthula zosterae(Lz) or sterile seawater. At two- and five-days post-exposure, pathogen load, visible disease signs, whole leaf phenolic content, and both host- and pathogen- transcriptomes were characterized. ResultsTwo days after exposure, more than 90% of plants had visible lesions andLzDNA was detectable in 100% percent of sampled plants in theLzexposed treatment. Concentrations of total phenolic compounds were lower after 5 days of combined exposure to warmer temperatures andLz, but were unaffected in other treatments. Concentrations of condensed tannins were not affected byLzor temperature, and did not change over time. Analysis of the eelgrass transcriptome revealed 540 differentially expressed genes in response toLzexposure, but not temperature.Lz-exposed plants had gene expression patterns consistent with increased defense responses through altered regulation of phytohormone biosynthesis, stress response, and immune function pathways. Analysis of the pathogen transcriptome revealed up-regulation of genes potentially involved in breakdown of host defense, chemotaxis, phagocytosis, and metabolism. DiscussionThe lack of a significant temperature signal was unexpected but suggests a more pronounced physiological response toLzinfection as compared to temperature. Pre-acclimation of eelgrass plants to the temperature treatments may have contributed to the limited physiological responses to temperature. Collectively, these data characterize a widespread physiological response to pathogen attack and demonstrate the value of paired transcriptomics to understand infections in a host-pathogen system.