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Perspectives on the wasting disease of eelgrass Zostera marina

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... Z. marina is a marine angiosperm that enhances local primary productivity, provides habitat for numerous invertebrates, fishes and birds, and contributes to nutrient cycling and sediment stabilization along coastlines throughout the Northern Hemisphere [31,32]. In the 1930s, over 90% of Z. marina was lost in the North Atlantic as a result of seagrass 'wasting disease' caused by the parasitic protist Labyrinthula zosterae [33][34][35]. Recovery from these disease-induced losses has been inconsistent, and chronic infections continue to be reported [33,[36][37][38]. Although the 1930s epizootic was centred in the North Atlantic, wasting disease infections have since been documented in seagrasses around the globe [39,40]. ...
... In the 1930s, over 90% of Z. marina was lost in the North Atlantic as a result of seagrass 'wasting disease' caused by the parasitic protist Labyrinthula zosterae [33][34][35]. Recovery from these disease-induced losses has been inconsistent, and chronic infections continue to be reported [33,[36][37][38]. Although the 1930s epizootic was centred in the North Atlantic, wasting disease infections have since been documented in seagrasses around the globe [39,40]. ...
... (ii) What is the relative explanatory power of host traits (host size, density, genetic diversity and nutrient content), abiotic factors (seawater temperature, seawater salinity, latitude) and biotic factors (epibiont biomass, grazer abundance) for the prevalence of wasting disease in eelgrass beds? Given the documented differences in the distribution and characteristics of both host and parasite between the Pacific and Atlantic Oceans [33,51], we expected that wasting disease prevalence would vary between oceans. We also hypothesized that abiotic environmental factors, such as temperature and salinity, would be the strongest predictors of wasting disease distribution within oceans, both because they are strong predictors of disease distributions in other marine organisms [52][53][54] and because they are known to affect the parasite, L. zosterae, and host, eelgrass, that constitute the seagrass wasting disease pathosystem [45,46,55]. ...
Article
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Diseases are ubiquitous in natural systems, with broad effects across populations, communities and ecosystems. However, the drivers of many diseases remain poorly understood, particularly in marine environments, inhibiting effective conservation and management measures. We examined biogeographical patterns of infection in the foundational seagrass Zostera marina by the parasitic protist Labyrinthula zosterae, the causative agent of seagrass wasting disease, across >20° of latitude in two ocean basins. We then identified and characterized relationships among wasting disease prevalence and a suite of host traits and environmental variables. Host characteristics and transmission dynamics explained most of the variance in prevalence across our survey, yet the particular host traits underlying these relationships varied between oceans, with host size and nitrogen content important in the Pacific and host size and density most important in the Atlantic. Temperature was also a key predictor of prevalence, particularly in the Pacific Ocean. The strength and shape of the relationships between prevalence and some predictors differed in our large-scale survey versus previous experimental and site-specific work. These results show that both host characteristics and environment influence host–parasite interactions, and that some such effects scale up predictably, whereas others appear to depend on regional or local context.
... Historic records show that seagrass species, in particular Z. marina, are highly susceptible to microbial pathogens. During the 1930s, a so-called 'wasting disease' decimated the eelgrass Z. marina in Europe and along the Atlantic Coast of North America with over 90% loss (Muehlstein 1989). Wasting disease resulted in black lesions on the leaf blades which potentially lead to loss of productivity, degradation of shoots and roots, eventually leading to the loss of large areas of seagrass (Den Hartog 1987). ...
Technical Report
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This project was commissioned by JNCC to generate an improved understanding of the sensitivities of seagrass habitats to pressures associated with human activities in the marine environment -to provide an evidence base to facilitate and support management advice for Marine Protected Areas; development of UK marine monitoring and assessment, and conservation advice to offshore marine industries.
... In the first half of the 20th century, worldwide, the area of eelgrass meadows has decreased, associated with climate change and anthropogenic eutrophication, which has led to a decrease in water transparency, as well as the spread of the parasitic organism Labyrinthula zosterae D. Porter et Muehlst in Muehlstein et Short, 1991 (Chromista) [52]. A reduction in the area of eelgrass vegetation was also observed in the Black Sea region [32]. ...
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The species composition and the structure of the macrophytobenthos, macrozoobenthos, and bottom sediments of Taman Bay are studied. This inlet is inhabited by seagrass Zostera marina L. which forms vast underwater meadows here. Samples were collected in 2008-2009, before the ongoing rise of salinity in the Sea of Azov. Three main biotopes with different bottom sediment composition (sands, sands with shells, and silts) were identified. They were inhabited by four main macrobenthic biocenoses (unvegetated near-shore biocenosis, mosaic macrophyte vegetation outside the surf zone, pure eelgrass's meadows belt, and the communities, dominated by the mobile macrozoobenthos species with low abundance of macrophytes occupying the central part of the bay). The main environmental factor associated with this distribution of the vegetation was the silt content (grain size <0.001 mm). The spatial structure of the macrozoobenthos correlated with the projective cover of Z. marina. Possible reasons for the revealed pattern in the distribution of communities are discussed.
... marina и Zostera noltei Hornemann, 1832) занимали все песчаные мелководья [14], а их суммарная фитомасса достигала нескольких десятков тысяч тонн [21]. В первой половине ХХ в. по всему миру площади морских лугов зостеры сократились, что связывают с изменением климата и антропогенной эвтрофикацией, повлекшими за собой уменьшение прозрачности вод, а также с распространением паразитического организма Labyrinthula zosterae D. Porter et Muehlst in Muehlstein et Short, 1991 (Chromista) [52]. Сокращение площадей зарослей зостеры наблюдалось и в Черноморском регионе [32]. ...
Preprint
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Research article. Detailed description of Taman Bay (Sea of Azov) bottom communities and analysis of environment factors correlations.
... However, Labyrinthula is also a ubiquitous symbiont that decomposes marine plants and algal wastes, one of which hosts the lawn grass [51]. Since the 1930s, the North American and European Atlantic coastal Zostera has been severely affected by consumptive disease, when it killed 90% of the North Atlantic Zostera population [52]. Muehlstein et al. [53] (1991) first identified L. zosterae (Labyrinthulomycetes) as the pathogen causing wasting diseases of Zostera, and later found that in many countries such as Australia, Mexico, and Republic of Korea (Table 1). ...
Article
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Due to climate change and human activities, seagrass is in crisis as the coverage of seagrass declines at an accelerated rate globally. In this paper, the severe challenges of seagrass ecosystem were briefly reviewed, including adverse effects of natural factors and human activities on seagrass beds. The research status of pollutants and pollution in seagrass bed ecosystem was reviewed, the future research directions in related fields were proposed as well. The eutrophication in coastal waters and discharge of pollutants such as sulfide, heavy metals, organic matter and microplastics caused by human activities are important reasons for seagrass loss. In addition, environmental stressors lead to reduced immunity and decreased resistance of seagrass to various pathogens, leading to seagrass wasting diseases. Future studies concerning the influence of novel pollutants, i.e., plastic waste on non-native algae, microorganisms and seagrasses, as well as their interrelationships, will be of vital importance. In addition, researches on seagrass wasting diseases and their pathogens should be much accounted in China, to fill in gaps in related fields and improve the response ability to emergent seagrass diseases. In conclusion, this review was proposed to arouse the concern about the seagrass bed pollution, and provide possible enlightening information for the protection and restoration of this significant ecosystem.
... Not too different from the ones described by a previous study, analysing salt marshes within the Solent region, of 12.2 Bq kg -1 supported 210 Pb on average [38] . Sites presenting low sediment deposition would show a 210 Pb inventory lower than expected, and bioturbation would be responsible for the apparent long-term accretion rate, while a higher-than-expected inventory could imply that the site is depositional, and the apparent long-term accretion rate reflects both bioturbation and accretion [3,59,69,70] . Results from this study support these assumptions, with higher sediment accretion rates found in Porchester (PMST 1), of 4.2-and 4.3-mm year -1 , than Farlington Marshes (FMST 2), of 1.6-and 1.2-mm year -1 , when calculated by both the CRS and CF:CS methods, respectively. ...
Article
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The aim of this study was to provide an evaluation of the current methods used to assess carbon sequestration (C seq) rates from intertidal Zostera spp. meadows in central Southern England. This study evaluated the use of 210 Pb dating methods to calculate sediment accretion rates from four intertidal seagrass meadows along the southern central coast of England. Results obtained were then used to determine C seq rates, following different models. The mean rate of C seq calculated in this study using the CRS model was 75.12 g m-2 year-1 , comparable to other global regions and within the estimated global range. However, results revealed that other, conservative methods, provide much lower C seq rates, highlighting the need for caution when choosing appropriate methods and reporting results related to seagrass carbon sequestration potential. Moreover, these results highlight the importance of local assessments of C seq , and the need to create robust models that include the effects of mixing, erosion, and disturbance, to better understand the possible effects of extreme climate events and anthropogenic impacts on seagrass ecosystems' carbon sequestration potential.
... Not too different from the ones described by a previous study, analysing salt marshes within the Solent region, of 12.2 Bq kg -1 supported 210 Pb on average [38] . Sites presenting low sediment deposition would show a 210 Pb inventory lower than expected, and bioturbation would be responsible for the apparent long-term accretion rate, while a higher-than-expected inventory could imply that the site is depositional, and the apparent long-term accretion rate reflects both bioturbation and accretion [3,59,69,70] . Results from this study support these assumptions, with higher sediment accretion rates found in Porchester (PMST 1), of 4.2-and 4.3-mm year -1 , than Farlington Marshes (FMST 2), of 1.6-and 1.2-mm year -1 , when calculated by both the CRS and CF:CS methods, respectively. ...
Article
Full-text available
The aim of this study was to provide an evaluation of the current methods used to assess carbon sequestration (C seq) rates from intertidal Zostera spp. meadows in central Southern England. This study evaluated the use of 210 Pb dating methods to calculate sediment accretion rates from four intertidal seagrass meadows along the southern central coast of England. Results obtained were then used to determine C seq rates, following different models. The mean rate of C seq calculated in this study using the CRS model was 75.12 g m-2 year-1 , comparable to other global regions and within the estimated global range. However, results revealed that other, conservative methods, provide much lower C seq rates, highlighting the need for caution when choosing appropriate methods and reporting results related to seagrass carbon sequestration potential. Moreover, these results highlight the importance of local assessments of C seq , and the need to create robust models that include the effects of mixing, erosion, and disturbance, to better understand the possible effects of extreme climate events and anthropogenic impacts on seagrass ecosystems' carbon sequestration potential.
... Northern European populations of the widespread seagrass Zostera marina (eelgrass) declined heavily in the 1930s, due to a major outbreak in eelgrass wasting disease (Labyrinthula zosterae; Den Hartog 1987; Short et al. 1988;Muehlstein 1989). Though many populations recovered to some extent, anthropogenic pressures in the second half of the 20th century have led to continued losses in some areas (Dunic et al. 2021;Turschwell et al. 2021). ...
Article
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Seagrass meadows, and their associated biodiverse assemblages have declined globally due to environmental and anthropogenic stressors. Restoration of these critical habitats has the potential to reverse coastal biodiversity loss. Here, we tested the role of patch size (which can affect e.g. recruitment, food availability, and/or predation) in driving faunal colonisation in an eelgrass (Zostera marina) restoration trial in Sweden. Eelgrass shoots were transplanted in plots with different configurations (continuous vs. checkerboard patterns with three patch sizes), and we followed invertebrate colonisation (biodiversity and functional diversity) during the first two growing seasons. We found rapid faunal colonisation following the transplantation of eelgrass shoots in all plots, with invertebrate densities reaching 50‐80% of the reference meadow after only one growing season (three months). After two growing seasons (15 months), the faunal density, biodiversity, and functional diversity were similar to the reference meadow, despite eelgrass density and biomass still being lower than the reference meadow. Biodiversity, functional diversity, and community structure were similar among the different planted plots, i.e. there was no indication that patch size influenced faunal colonisation. We therefore consider that smaller patches embedded within larger restoration plots can be as effective for promoting biodiversity as continuous patches, with reduced costs and fewer shoots required. We also noted high natural variability between years both in the reference meadow and planted plots, showing the dynamic nature of seagrass ecosystems, and the importance of a well‐planned monitoring scheme that considers the reference area and restored area within the same temporal scale. This article is protected by copyright. All rights reserved.
... Seagrass wasting disease historically shaped eelgrass meadows and continues to persist today. In the 1930s, SWD outbreaks decimated up to 90% of eelgrass meadows throughout the North Atlantic (Renn, 1936;Short et al., 1987;Muehlstein, 1989), reducing waterfowl, shrimp, scallop, and fish populations (Renn, 1936;Stauffer, 1937;Moffitt and Cottam, 1941;Milne and Milne, 1951) and compromising eelgrass ecosystem services (Orth et al., 2006). These and subsequent die-offs were traced to Labyrinthula zosterae (Muehlstein et al., 1988), which is now recognized as a virulent pathogen in eelgrass (Groner et al., 2014(Groner et al., , 2016Martin et al., 2016) and other seagrasses worldwide (reviewed in Sullivan et al., 2018). ...
Article
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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.
Thesis
Les herbiers marins constituent des habitats remarquables et diversifiés des eaux côtières des territoires ultramarins français. Une meilleure compréhension de leur état écologique sous l’influence des perturbations multiples auxquels ils sont soumis est nécessaire pour répondre aux enjeux des politiques publiques environnementales s’appliquant à l’échelle de ces territoires. Divers paramètres représentant la plupart des compartiments biologiques, allant de la physiologie des phanérogames marines à l’écosystème ont été testés in situ dans des conditions environnementales contrastées. Ces expérimentations ont permis d’évaluer les relations pressions-état des herbiers de différents territoires dans les trois océans et de sélectionner les descripteurs les plus pertinents selon les principaux objectifs de gestion. Sur la base des données collectées, une première version d’indicateurs intégrés combinant des indicateurs d'alerte précoce et de diagnostic (nutriments et certains métaux traces) et des paramètres de réponse à long terme (densité des plants et recouvrement) adaptés aux échelles de temps de la gestion ont été développés. Une première classification de l’état des herbiers étudiés est ainsi proposée. Ces outils intégrés devraient permettre de renforcer l’efficacité des mesures de gestion, tout en facilitant une mise en oeuvre mutualisée des différentes politiques publiques. L'évaluation de l'état de santé des herbiers marins et de leur environnement est essentielle afin de déployer des mesures de gestion et de préservation appropriées pour améliorer de manière durable l’état et la résilience de cet écosystème menacé.
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This paper provides a summary of research conducted to investigate possible causes of the decline in abundance of submerged aquatic vegetation beginning in the late 1960s. Three factors are emphasized: runoff of agricultural herbicides; erosional inputs of fine-grain sediments; nutrient enrichment and associated algal growth. The results are synthesized into an ecosystem simulation model which demonstrated relative potential contributions, where nutrients greater than sediments greater than herbicides. Other factors and mechanisms are also discussed along with resource managements options.