RESUMEN
Populations of at least 20 asteroid species on the Northeast Pacific Coast have recently experienced an extensive outbreak of sea-star (asteroid) wasting disease (SSWD). The disease leads to behavioral changes, lesions, loss of turgor, limb autotomy, and death characterized by rapid degradation ("melting"). Here, we present evidence from experimental challenge studies and field observations that link the mass mortalities to a densovirus (Parvoviridae). Virus-sized material (i.e., <0.2 µm) from symptomatic tissues that was inoculated into asymptomatic asteroids consistently resulted in SSWD signs whereas animals receiving heat-killed (i.e., control) virus-sized inoculum remained asymptomatic. Viral metagenomic investigations revealed the sea star-associated densovirus (SSaDV) as the most likely candidate virus associated with tissues from symptomatic asteroids. Quantification of SSaDV during transmission trials indicated that progression of SSWD paralleled increased SSaDV load. In field surveys, SSaDV loads were more abundant in symptomatic than in asymptomatic asteroids. SSaDV could be detected in plankton, sediments and in nonasteroid echinoderms, providing a possible mechanism for viral spread. SSaDV was detected in museum specimens of asteroids from 1942, suggesting that it has been present on the North American Pacific Coast for at least 72 y. SSaDV is therefore the most promising candidate disease agent responsible for asteroid mass mortality.
Asunto(s)
Densovirus/fisiología , Monitoreo del Ambiente/métodos , Agua de Mar/virología , Estrellas de Mar/virología , Animales , Conservación de los Recursos Naturales/métodos , ADN Viral/genética , ADN Viral/aislamiento & purificación , Densovirus/genética , Regulación Viral de la Expresión Génica , Geografía , Sedimentos Geológicos/virología , Interacciones Huésped-Patógeno , Metagenoma/genética , América del Norte , Océano Pacífico , Filogenia , Plancton/virología , Densidad de Población , Dinámica Poblacional , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Especificidad de la Especie , Estrellas de Mar/clasificación , Estrellas de Mar/genética , Proteínas Virales/genéticaRESUMEN
Pathogen transmission pathways are fundamental to understanding the epidemiology of infectious diseases yet are challenging to estimate in nature, particularly in the ocean. Seagrass wasting disease (SWD), caused by Labyrinthula zosterae, impacts seagrass beds worldwide and is thought to be a contributing factor to declines; however, little is known about natural transmission of SWD. In this study, we used field and laboratory experiments to test SWD transmission pathways and temperature sensitivity. To test transmission modes in nature, we conducted three field experiments out-planting sentinel Zostera marina shoots within and adjacent to natural Z. marina beds (20 ± 5 and 110 ± 5 m from bed edge). Infection rates and severity did not differ among outplant locations, implicating waterborne transmission. The infectious dose of L. zosterae through waterborne exposure was assessed in a controlled laboratory experiment. The dose to 50% disease was 6 cells ml-1 and did not differ with the temperatures tested (7.5°C and 15°C). Our results show L. zosterae is transmissible through water without direct contact with infected plants. Understanding the transmission dynamics of this disease in the context of changing ocean conditions will improve Z. marina protection and restoration in critical coastal habitats worldwide.
RESUMEN
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'.
Asunto(s)
Ecosistema , Zosteraceae , Temperatura , Cambio Climático , FríoRESUMEN
Over 20 species of asteroids were devastated by a sea star wasting disease (SSWD) epizootic, linked to a densovirus, from Mexico to Alaska in 2013 and 2014. For Pisaster ochraceus from the San Juan Islands, South Puget Sound and Washington outer coast, time-series monitoring showed rapid disease spread, high mortality rates in 2014, and continuing levels of wasting in the survivors in 2015. Peak prevalence of disease at 16 sites ranged to 100%, with an overall mean of 61%. Analysis of longitudinal data showed disease risk was correlated with both size and temperature and resulted in shifts in population size structure; adult populations fell to one quarter of pre-outbreak abundances. In laboratory experiments, time between development of disease signs and death was influenced by temperature in adults but not juveniles and adult mortality was 18% higher in the 19 °C treatment compared to the lower temperature treatments. While larger ochre stars developed disease signs sooner than juveniles, diseased juveniles died more quickly than diseased adults. Unusual 2-3 °C warm temperature anomalies were coincident with the summer 2014 mortalities. We suggest these warm waters could have increased the disease progression and mortality rates of SSWD in Washington State.
Asunto(s)
Enfermedades de los Animales/patología , Estrellas de Mar , Animales , Interacciones Huésped-Patógeno , Densidad de Población , Temperatura , Factores de TiempoRESUMEN
Sea star wasting disease devastated intertidal sea star populations from Mexico to Alaska between 2013-15, but little detail is known about its impacts to subtidal species. We assessed the impacts of sea star wasting disease in the Salish Sea, a Canadian / United States transboundary marine ecosystem, and world-wide hotspot for temperate asteroid species diversity with a high degree of endemism. We analyzed roving diver survey data for the three most common subtidal sea star species collected by trained volunteer scuba divers between 2006-15 in 5 basins and on the outer coast of Washington, as well as scientific strip transect data for 11 common subtidal asteroid taxa collected by scientific divers in the San Juan Islands during the spring/summer of 2014 and 2015. Our findings highlight differential susceptibility and impact of sea star wasting disease among asteroid species populations and lack of differences between basins or on Washington's outer coast. Specifically, severe depletion of sunflower sea stars (Pycnopodia helianthoides) in the Salish Sea support reports of major declines in this species from California to Alaska, raising concern for the conservation of this ecologically important subtidal predator.
Asunto(s)
Estrellas de Mar/crecimiento & desarrollo , Síndrome Debilitante/patología , Animales , Canadá , Conservación de los Recursos Naturales , Ecosistema , Modelos Teóricos , Oportunidad Relativa , Estaciones del Año , Especificidad de la Especie , Síndrome Debilitante/veterinariaRESUMEN
Echinoderms, positioned taxonomically at the base of deuterostomes, provide an important system for the study of the evolution of the immune system. However, there is little known about the cellular components and genes associated with echinoderm immunity. The 2013-2014 sea star wasting disease outbreak is an emergent, rapidly spreading disease, which has led to large population declines of asteroids in the North American Pacific. While evidence suggests that the signs of this disease, twisting arms and lesions, may be attributed to a viral infection, the host response to infection is still poorly understood. In order to examine transcriptional responses of the sea star Pycnopodia helianthoides to sea star wasting disease, we injected a viral sized fraction (0.2 µm) homogenate prepared from symptomatic P. helianthoides into apparently healthy stars. Nine days following injection, when all stars were displaying signs of the disease, specimens were sacrificed and coelomocytes were extracted for RNA-seq analyses. A number of immune genes, including those involved in Toll signaling pathways, complement cascade, melanization response, and arachidonic acid metabolism, were differentially expressed. Furthermore, genes involved in nervous system processes and tissue remodeling were also differentially expressed, pointing to transcriptional changes underlying the signs of sea star wasting disease. The genomic resources presented here not only increase understanding of host response to sea star wasting disease, but also provide greater insight into the mechanisms underlying immune function in echinoderms.