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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.
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Invertebrate herbivores influence seagrass wasting disease dynamics
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.
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- Award ID(s):
- 2109607
- PAR ID:
- 10608950
- Publisher / Repository:
- Ecology
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 106
- Issue:
- 1
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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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.more » « less
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Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass ( Zostera marina ) is a temperate species threatened by seagrass wasting disease (SWD), caused by the protist Labyrinthula zosterae . The pathogen is sensitive to warming ocean temperatures, prompting a need for greater understanding of the impacts on host health under climate change. Previous work demonstrates pathogen cultures grow faster under warmer laboratory conditions and documents positive correlations between warmer ocean temperatures and disease levels in nature. However, the consequences of disease outbreaks on eelgrass growth remain poorly understood. Here, we examined the effect of disease on eelgrass productivity in the field. We coupled in situ shoot marking with high-resolution imagery of eelgrass blades and used an artificial intelligence application to determine disease prevalence and severity from digital images. Comparisons of eelgrass growth and disease metrics showed that SWD impaired eelgrass growth and accumulation of non-structural carbon in the field. Blades with more severe disease had reduced growth rates, indicating that disease severity can limit plant growth. Disease severity and rhizome sugar content were also inversely related, suggesting that disease reduced belowground carbon accumulation. Finally, repeated measurements of diseased blades indicated that lesions can grow faster than healthy tissue in situ . This is the first study to demonstrate the negative impact of wasting disease on eelgrass health in a natural meadow. These results emphasize the importance of considering disease alongside other stressors to better predict the health and functioning of seagrass meadows in the Anthropocene.more » « less
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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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/ecy.4493
