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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 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. 

Synopsis 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 of 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 that 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 creates critical coastal habitats worldwide and fulfills essential ecosystem functions as a foundation seagrass. Climate warming and disease threaten eelgrass, causing mass mortalities and cascading ecological impacts. Subtidal meadows are deeper than intertidal and may also provide refuge from the temperature-sensitive seagrass wasting disease. From cross-boundary surveys of 5761 eelgrass leaves from Alaska to Washington and assisted with a machine-language algorithm, we measured outbreak conditions. Across summers 2017 and 2018, disease prevalence was 16% lower for subtidal than intertidal leaves; in both tidal zones, disease risk was lower for plants in cooler conditions. Even in subtidal meadows, which are more environmentally stable and sheltered from temperature and other stressors common for intertidal eelgrass, we observed high disease levels, with half of the sites exceeding 50% prevalence. Models predicted reduced disease prevalence and severity under cooler conditions, confirming a strong interaction between disease and temperature. At both tidal zones, prevalence was lower in more dense eelgrass meadows, suggesting disease is suppressed in healthy, higher density meadows. These results underscore the value of subtidal eelgrass and meadows in cooler locations as refugia, indicate that cooling can suppress disease, and have implications for eelgrass conservation and management under future climate change scenarios. This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’. 

Seagrass meadows are essential habitats that support marine biodiversity and coastal communities while sequestering carbon, filtering water, and stabilizing coastal sediments. Warming temperatures stress seagrass meadows and can facilitate seagrass wasting disease, contributing to large-scale diebacks of seagrass meadows. Here, we demonstrate how high-resolution imagery, collected by uncrewed aerial vehicle (UAV) and validated by in situ sampling, can quantify seagrass responses to disease and thermal stress.