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Abstract Salinity plays an important role in the physiology of marine organisms and their pathogens. As the climate continues to change, marine and estuarine salinities may become more extreme and irregular, potentially altering host–pathogen interactions. In this review, we explore and highlight the role of salinity on a range of pathosystems, outlining impacts to the host, pathogen and their interactions. We present fisheries and aquaculture-focused case studies, including behavioural preferences for freshwater in sea louse-infested trout and the use of freshwater as a delouser in salmon aquaculture, the effects of rainfall and drought on prevalence of a lethal parasitic infection of crustaceans, as well as low saline environments as refugia from oyster disease. We also present a case study of human health risks examining how changing coastal salinities can affect seafood-associated illnesses, and a conservation-directed case study examining the role of salinity and disease in defining the distribution of a habitat-forming species. Changing climatic conditions drive diverse salinity-altered epidemiological outcomes in these pathosystems. As salinities become more variable and less predictable, and fisheries management and marine conservation require increasing priority, future studies investigating multiple stressors, salinity included, on pathosystems will provide insights into organism and ecosystem resilience under future climate scenarios. This article is part of the theme issue ‘Managing infectious marine diseases in wild populations’. 

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. 

Abstract Disease is a key driver of community and ecosystem structure, especially when it strikes foundation species. In the widespread marine foundation species eelgrass (Zostera marina), outbreaks of wasting disease have caused large‐scale meadow collapse in the past, and the causative pathogen,Labyrinthula zosterae, is commonly found in meadows globally. Research to date has mainly focused on abiotic environmental drivers of seagrass wasting disease, but there is strong evidence from other systems that biotic interactions such as herbivory can facilitate plant diseases. How biotic interactions influence seagrass wasting disease in the field is unknown but is potentially important for understanding dynamics of this globally valuable and declining habitat. Here, we investigated links between epifaunal grazers and seagrass wasting disease using a latitudinal field study across 32 eelgrass meadows distributed from southeastern Alaska to southern California. From 2019 to 2021, we conducted annual surveys to assess eelgrass shoot density, morphology, epifauna community, and the prevalence and lesion area of wasting disease infections. We integrated field data with satellite measurements of sea surface temperature and used structural equation modeling to test the magnitude and direction of possible drivers of wasting disease. Our results show that grazing by small invertebrates was associated with a 29% increase in prevalence of wasting disease infections and that both the prevalence and lesion area of disease increased with total epifauna abundances. Furthermore, these relationships differed among taxa; disease levels increased with snail (Lacunaspp.) and idoteid isopod abundances but were not related to abundance of ampithoid amphipods. This field study across 23° of latitude suggests a prominent role for invertebrate consumers in facilitating disease outbreaks with potentially large impacts on coastal seagrass ecosystems. 

Abstract Foundational habitats such as seagrasses and coral reefs are at severe risk globally from climate warming. Infectious disease associated with warming events is both a cause of decline and an indicator of stress in both habitats. Since new approaches are needed to detect refugia and design climate-smart networks of marine protected areas, we test the hypothesis that the health of eelgrass (Zostera marina) in temperate ecosystems can serve as a proxy indicative of higher resilience and help pinpoint refugia. Eelgrass meadows worldwide are at-risk from environmental stressors, including climate warming and disease. Disease outbreaks of Labyrinthula zosterae are associated with recent, widespread declines in eelgrass meadows throughout the San Juan Islands, Washington, USA. Machine language learning, drone surveys, and molecular diagnostics reveal climate impacts on seagrass wasting disease prevalence (proportion of infected individuals) and severity (proportion infected leaf area) from San Diego, California to Alaska. Given that warmer temperatures favor many pathogens such as L. zosterae, we hypothesize that absent or low disease severity in meadows could indicate eelgrass resilience to climate and pathogenic stressors. Regional surveys showed the San Juan Islands as a hotspot for both high disease prevalence and severity, and surveys throughout the Northeast Pacific indicated higher prevalence and severity in intertidal, rather than subtidal, meadows. Further, among sites with eelgrass declines, losses were more pronounced at sites with shallower eelgrass meadows. We suggest deeper meadows with the lowest disease severity will be refuges from future warming and pathogenic stressors in the Northeast Pacific. Disease monitoring may be a useful conservation approach for marine foundation species, as low or absent disease severity can pinpoint resilient refugia that should be prioritized for future conservation efforts. Even in declining or at-risk habitats, disease surveys can help identify meadows that may contain especially resilient individuals for future restoration efforts. Our approach of using disease as a pulse-point for eelgrass resilience to multiple stressors could be applied to other habitats such as coral reefs to inform conservation and management decisions. 

Abstract Host‐associated microbes influence host health and function and can be a first line of defence against infections. While research increasingly shows that terrestrial plant microbiomes contribute to bacterial, fungal, and oomycete disease resistance, no comparable experimental work has investigated marine plant microbiomes or more diverse disease agents. We test the hypothesis that the eelgrass (Zostera marina) leaf microbiome increases resistance to seagrass wasting disease. From field eelgrass with paired diseased and asymptomatic tissue,16S rRNAgene amplicon sequencing revealed that bacterial composition and richness varied markedly between diseased and asymptomatic tissue in one of the two years. This suggests that the influence of disease on eelgrass microbial communities may vary with environmental conditions. We next experimentally reduced the eelgrass microbiome with antibiotics and bleach, then inoculated plants withLabyrinthula zosterae, the causative agent of wasting disease. We detected significantly higher disease severity in eelgrass with a native microbiome than an experimentally reduced microbiome. Our results over multiple experiments do not support a protective role of the eelgrass microbiome againstL. zosterae. Further studies of these marine host–microbe–pathogen relationships may continue to show new relationships between plant microbiomes and diseases. 

Eelgrass (Zostera marina) creates valuable, biodiverse habitats worldwide, but is at risk from combined environmental stressors and disease. We surveyed paired intertidal and subtidal meadows for seagrass wasting disease in the San Juan Islands, WA, USA in summers 2017–2019 to determine how disease varied with depth, temperature, and salinity. We expected reduced disease in deeper meadows with more stable environmental conditions compared to shallower, intertidal meadows with greater thermal and salinity variation. Leveraging a machine-learning algorithm to detect and quantify disease, we measured high disease levels and large changes in meadow densities, particularly in the warmer 2018 summer. Daily meanin situand remote-sensed temperatures captured exposure to warming, thoughin situtemperatures better identified site-specific, seasonal thermal ranges. Subtidal meadows experienced nearly 14°C cooler maximumin situtemperatures compared to intertidal meadows. Disease severity was 2.24 times greater in shallow, intertidal meadows compared to deeper, subtidal meadows over the 3-year study and 1.39 times greater during the 2018 warming. Thus, some subtidal meadows can serve as valuable refugia against environmental and pathogenic stressors. Lower eelgrass densities were also associated with increased severity, suggesting a link between disease and meadow patchiness. Temperature and salinity were also key predictors of higher disease: prevalence and maximum sea surface temperatures covaried, as did severity and salinity range, suggesting these environmental factors may differentially influence seagrass wasting disease risk and progression. Our work highlights the value of both subtidal eelgrass meadows and sites with more stable environmental conditions as refugia from multiple stressors, which should be considered as differential drivers of disease.