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Perspectives on the wasting disease of eelgrass Zostera marina

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... Les Zostères ont failli disparaître dans les années 30 suite, apparemment, à un évènement environnemental délétère qui s'est traduit par une réduction sans précédent des surfaces d'herbiers dans l'intégralité de l'aire de répartition de l'hémisphère nord (den Hartog 1987, Short et al. 1988, Muehlstein 1989, Giesen 1990, Godet et al. 2008. A présent, il semble que les herbiers n'aient pas recouvré leur état initial (avant les années 30) (Davison & Hughes 1998). ...
... Les effectifs n'ont cessé d'augmenter pour évoluer de 45 000 individus (1976) à 120 000 (2007) Bernaches hivernant sur le trait côtier Manche-Atlantique, soit à présent ≈60% de la population mondiale (Mahéo 1995, Deceuninck et al. 2005, Mahéo 2005, 2007, 2008, 2009. (Ranwell & Downing 1959, Drent & Prins 1987, Muehlstein 1989. ...
... Lors de cette période le nombre d'oiseaux était alors estimé aux alentours de 200 000 individus(Cottam et al. 1944, Salomonsen 1958, Oglivie & Matthews 1969. Cependant, dans les années 30, suite à une sévère diminution des surfaces d'herbiers causée par une épiphytie (Mycetozoan labyrunthula) de part et d'autre de l'Atlantique(Fischer-Piette et al. 1932, Duncan 1933, Short et al. 1988, Muehlstein 1989, les populations mondiales se sont effondrées atteignant des seuils critiques proches de l'extinction et accusant une réduction des effectifs entre 75 et 90%(Cottam et al. 1944, Oglivie & Matthews 1969.En Europe, la population avait augmenté de 5 000 à 15 000 individus (Cf.Fig.14)entre les années 30 et 50(Oglivie & Matthews 1969, Oglivie & St Joseph 1976. ...
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Dark-bellied Brent Goose as a biodincator of intertidal ecosystems
... While die-offs have continued, most have been localized and not on the scale of the 1930s outbreak (Short et al. 1987). L. zosterae infection is spread between individual plants by direct contact, with potential regional spreading occurring through drifting of infected plants, though little is known of L. zosterae life history post-infection (Muehlstein 1989). ...
... Like eastern oyster, eelgrass provides important nursery and foraging habitat for economically valuable species in Chesapeake Bay, such as blue crabs and numerous commercially exploited finfish (Reed and Hovel 2006). Eelgrass mortality as a result of L. zosterae infection causes reduced abundance, resulting in benthic habitat fragmentation and isolated patches which affects numerous marine and some terrestrial species (Muehlstein 1989). Altered eelgrass habitat configurations can lead to reductions in faunal abundance, diversity, and survival (Reed and Hovel 2006). ...
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Diseases are important drivers of population and ecosystem dynamics. This review synthesizes the effects of infectious diseases on the population dynamics of nine species of marine organisms in the Chesapeake Bay. Diseases generally caused increases in mortality and decreases in growth and reproduction. Effects of diseases on eastern oyster ( Crassostrea virginica ) appear to be low in the 2000s compared to effects in the 1980s–1990s. However, the effects of disease were not well monitored for most of the diseases in marine organisms of the Chesapeake Bay, and few studies considered effects on growth and reproduction. Climate change and other anthropogenic effects are expected to alter host-pathogen dynamics, with diseases of some species expected to worsen under predicted future conditions (e.g., increased temperature). Additional study of disease prevalence, drivers of disease, and effects on population dynamics could improve fisheries management and forecasting of climate change effects on marine organisms in the Chesapeake Bay.
... 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). ...
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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.
... The coasts of the Nordic countries support at least 1500-2100 km 2 of eelgrass Zostera marina ), but extensive declines in eelgrass coverage and depth limits have been recorded throughout the North Sea and southern Baltic Sea (de los Santos et al. 2019). In Denmark, the present distribution constitutes approximately only 10-20% of the historical distribution, while 60% has been lost along the Swedish Skagerrak coast, due to seagrass wasting disease in the first half of the 20th century (Muehlstein 1989), and overfishing and eutrophication in the second half. More recently, climate change including marine heat waves, poses new challenges to seagrass meadows (Smale et al. 2019). ...
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Understanding the ecological interactions that enhance the resilience of threatened ecosystems is essential in assuring their conservation and restoration. Top‐down trophic interactions can increase resilience to bottom‐up nutrient enrichment, however, as many seagrass ecosystems are threatened by both eutrophication and trophic modifications, understanding how these processes interact is important. Using a combination of approaches, we explored how bottom‐up and top‐down processes, acting individually or in conjunction, can affect eelgrass meadows and associated communities in the northern Baltic Sea. Field surveys along with fish diet and stable isotope analyses revealed that the eelgrass trophic network included two main top predatory fish species, each of which feeds on a separate group of invertebrate mesograzers (crustaceans or gastropods). Mesograzer abundance in the study area was high, and capable of mitigating the effects of increased algal biomass that resulted from experimental nutrient enrichment in the field. When crustacean mesograzers were experimentally excluded, gastropod mesograzers were able to compensate and limit the effects of nutrient enrichment on eelgrass biomass and growth. Our results suggest that top‐down processes (i.e., suppression of algae by different mesograzer groups) may ensure eelgrass resilience to nutrient enrichment in the northern Baltic Sea, and the existence of multiple trophic pathways can provide additional resilience in the face of trophic modifications. However, the future resilience of these meadows is likely threatened by additional local stressors and global environmental change. Understanding the trophic links and interactions that ensure resilience is essential for managing and conserving these important ecosystems and the services they provide.
... trossulus, that are widely distributed and often co-occur across the temperate North Atlantic, but are in decline in many areas (Short et al. 2011;Christie et al. 2020). Seagrass cover has decreased by at least 30% globally over the past 50 years (Waycott et al. 2009), and many northern European eelgrass populations were eliminated in the 1930s due to eelgrass wasting disease (Muehlstein et al. 1988;Muehlstein 1989). Eutrophication, algal blooms, and coastal development further reduced eelgrass cover (Erftemeijer & Lewis 2006;Burkholder et al. 2007), while trophic cascades caused by overfishing, climate change, and heat waves threaten survival and growth (Baden et al. 2010;Duarte et al. 2018). ...
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Marine ecosystem engineers such as seagrasses and bivalves create important coastal habitats sustaining high biodiversity and ecosystem services. Restoring these habitats is difficult due to the importance of feedback mechanisms that can require large‐scale efforts to ensure success. Incorporating facilitative interactions could increase the feasibility and success of small‐scale restoration efforts, which would limit pressure on donor sites and reduce costs and time associated with restoration. Here, we tested two methods for providing facilitation in small‐scale eelgrass (Zostera marina) restoration plots across northern Europe: (1) co‐restoration with blue mussels (Mytilus edulis, M. trossulus), and (2) the use of biodegradable establishment structures (BESEs). Eelgrass‐mussel co‐restoration showed promise in aquaria, where eelgrass growth was nearly twice as high in treatments with medium and high mussel densities than in treatments without mussels. However, this did not translate to higher shoot length or shoot densities in subsequent field experiments. Rather, hydrodynamic exposure limited both eelgrass and mussel survival, especially in the most exposed sites. The use of BESEs showed more potential in enabling small‐scale restoration success: they effectively enhanced eelgrass survival and reduced mussel loss, and showed potential for enabling mussel recruitment in one site. However, eelgrass planted in BESE plots along with mussels had a lower survival rate than eelgrass planted in BESE plots without mussels. Overall, we show that though co‐restoration did not work at small scales, facilitation by using artificial structures (BESEs) can increase early eelgrass survival and success of small‐scale eelgrass and bivalve restoration. This article is protected by copyright. All rights reserved.
... In the early 1930's, eelgrass populations across the Atlantic coasts of North America and Europe were decimated by an outbreak of 'wasting disease' (Muehlstein 1989). This disease is caused by an infectious slime mold (Labyrinthula zostera) that spreads via direct leaf-to-leaf contact and causes eelgrass shoots to develop black-brown dots and streaks, eventually leading to their mortality. ...
Technical Report
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Some eelgrass beds in Atlantic Canada have receded in recent years due to a multitude of interacting stressors including disease, species invasions, nutrient enrichment, and climate change. There have been concerns that aquaculture may also have the potential to negatively impact eelgrass, given aquaculture is primarily a coastal activity. This report was written by the Centre for Marine Applied Research (CMAR) to review the potential effects of shellfish and finfish aquaculture on eelgrass beds in Nova Scotia.
... Les Zostères ont failli disparaître dans les années 30 suite, apparemment, à un évènement environnemental délétère qui s'est traduit par une réduction sans précédent des surfaces d'herbiers dans l'intégralité de l'aire de répartition de l'hémisphère nord (den Hartog 1987, Short et al. 1988, Muehlstein 1989, Giesen 1990, Godet et al. 2008. A présent, il semble que les herbiers n'aient pas recouvré leur état initial (avant les années 30) (Davison & Hughes 1998 (Davison & Hughes 1998, Bester 2000, Borum et al. 2004, Hasegawa et al. 2007). ...
Technical Report
Full-text available
Identification and caracthirization of South Marenne-Oléron Zostera noltei bed
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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Seagrass wasting disease (SWD), an infection believed to be caused by Labyrinthula zosterae, has been linked to seagrass declines in several places around the world. However, there is uncertainty about the mechanisms of disease and the potential involvement of opportunistic colonising microorganisms. Using 16S rRNA gene amplicon sequencing, we compared the microbiome of SWD lesions in leaves of Zostera muelleri with communities in adjacent asymptomatic tissues and healthy leaves. The microbiome of healthy leaf tissues was dominated by Pseudomonas and Burkholderia, whereas the most predominant taxa within adjacent tissues were Pseudomonas and Rubidimonas. Members of the Saprospiraceae, potential macroalgal pathogens, were over-represented within SWD lesions. These pronounced changes in microbiome structure were also apparent when we examined the core microbiome of different tissue types. Although the core microbiome associated with healthy leaves included three operational taxonomic units (OTUs) classified as Burkholderia, Cryomorphaceae and the SAR11 clade, a single core OTU from the Arenicella was found within adjacent tissues. Burkholderia are diazotrophic microorganisms and may play an important role in seagrass nitrogen acquisition. In contrast, some members of the Arenicella have been implicated in necrotic disease in other benthic animals. Moreover, microbiome structure was maintained across sites within healthy tissues, but not within SWD lesions or the tissues immediately adjacent to lesions. Predicted functional profiles revealed increased photoautotrophic functions in SWD tissues relative to healthy leaves, but no increase in pathogenicity or virulence. Notably, we demonstrated the presence of L. zosterae in SWD lesions by polymerase chain reaction, but only in one of the two sampled locations, which indicates that other microbiological factors may be involved in the initiation or development of SWD-like symptoms. This study suggests that the dynamics of the seagrass microbiome should be considered within the diagnosis and management of SWD.
Article
Zostera marina L. plants have been seriously impacted by wasting disease along the Atlantic coasts of North America and Europe since the 1930s (Muehlstein 1989). Sudden declines in the population sizes of Zostera marina affect primary and secondary producers of different trophic levels in blue carbon ecosystems (Gleason et al. 2013). Muehlstein et al. (1991) first identified Labyrinthula zosterae (Labyrinthulomycetes) as the pathogen causing wasting disease in Zostera marina. However, there have been no reports of wasting disease pathogens affecting seagrass in Korea. In this study, we collected leaves of Z. marina showing symptoms of wasting disease in the southern region of South Korea (Dongdaeman, Namhae, Gyeongnam Province) during field monitoring (from April to September 2013). The pathogens of wasting disease, Labyrinthula zosterae has been isolated from the infected leaves of Z. marina and established as a culture strain (Supplementary Figure 1). Samples of Z. marina and L. zosterae were deposited at the Fisheries Seed and Breeding Research Institute (previous Seaweed Research Center, National Institute of Fisheries Science, South Korea). Microscopic examination of the infected leaf tissues revealed fusiform or spindle-shaped vegetative Labyrinthula cells (4–5 × 15–20 μm). These were similar in size and shape to those previously described for Labyrinthula species. The fusiform cells were cultured in 1% serum seawater agar medium, and they formed colonies and showed gliding motility along a network of hyaline slime filaments. To validate the pathogenicity, re-inoculation tests by L. zosterae were performed with the isolated strains in accordance with Koch’s postulates. Healthy leaves of Z. marina collected from the field were used in the re-inoculation tests and were cultured at 15°C under white fluorescent irradiation of approximately 20 μmol·photons·m-2·s-1 and a 12:12-h light:dark cycle (Supplementary Figure 1). Labyrinthula zosterae re-isolated from artificially infected leaves of Z. marina was confirmed by DNA sequence similarity analysis. Total genomic DNA from the infected leaf cells and the culture strains was extracted using the QIAamp DNA Stool Mini Kit (Qiagen, Germany). Internal transcribed spacer (ITS) sequences of nuclear ribosomal DNA were determined to identify Labyrinthula species. L. zosterae-specific primers (Lz2forward (5ʹ- CTAAGACTAAACGAGGCGAAAGCCTAC-3ʹ) and Lz2reverse (5ʹ-AGGTTTACAAAACACACTCGTCCACA-3ʹ) in Bergmann et al. (2011)) were used to confirm the infection of L. zosterae in the leaves from the field samples and the re-inoculation test samples. Next, PCR products were cloned using a pLUG-Prime® TA-cloning Vector (iNtRON Biotechnology, Korea) and commercially sequenced (SolGent, Korea). The ITS sequence of Korean L. zosterae (accession number MW357748) showed high sequence similarity (99.3–100%) with that of L. zosterae deposited in GenBank (National Center for Biotechnology Information) from BLAST searches. These findings confirm that this is the first report of L. zosterae as the causal pathogen of wasting disease in Z. marina in Korea.
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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.