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      Salinity stress increases the severity of ranavirus epidemics in amphibian populations

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          Abstract

          The stress-induced susceptibility hypothesis, which predicts chronic stress weakens immune defences, was proposed to explain increasing infectious disease-related mass mortality and population declines. Previous work characterized wetland salinization as a chronic stressor to larval amphibian populations. Thus, we combined field observations with experimental exposures quantifying epidemiological parameters to test the role of salinity stress in the occurrence of ranavirus-associated mass mortality events. Despite ubiquitous pathogen presence (94%), populations exposed to salt runoff had slightly more frequent ranavirus related mass mortality events, more lethal infections, and 117-times greater pathogen environmental DNA. Experimental exposure to chronic elevated salinity (0.8–1.6 g l −1 Cl ) reduced tolerance to infection, causing greater mortality at lower doses. We found a strong negative relationship between splenocyte proliferation and corticosterone in ranavirus-infected larvae at a moderate elevation of salinity, supporting glucocorticoid-medicated immunosuppression, but not at high salinity. Salinity alone reduced proliferation further at similar corticosterone levels and infection intensities. Finally, larvae raised in elevated salinity had 10 times more intense infections and shed five times as much virus with similar viral decay rates, suggesting increased transmission. Our findings illustrate how a small change in habitat quality leads to more lethal infections and potentially greater transmission efficiency, increasing the severity of ranavirus epidemics.

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          Most cited references42

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          Effects of environmental change on emerging parasitic diseases.

          Ecological disturbances exert an influence on the emergence and proliferation of malaria and zoonotic parasitic diseases, including, Leishmaniasis, cryptosporidiosis, giardiasis, trypanosomiasis, schistosomiasis, filariasis, onchocerciasis, and loiasis. Each environmental change, whether occurring as a natural phenomenon or through human intervention, changes the ecological balance and context within which disease hosts or vectors and parasites breed, develop, and transmit disease. Each species occupies a particular ecological niche and vector species sub-populations are distinct behaviourally and genetically as they adapt to man-made environments. Most zoonotic parasites display three distinct life cycles: sylvatic, zoonotic, and anthroponotic. In adapting to changed environmental conditions, including reduced non-human population and increased human population, some vectors display conversion from a primarily zoophyllic to primarily anthrophyllic orientation. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, water control systems (dams, canals, irrigation systems, reservoirs), and climate, singly, and in combination have been accompanied by global increases in morbidity and mortality from emergent parasitic disease. The replacement of forests with crop farming, ranching, and raising small animals can create supportive habitats for parasites and their host vectors. When the land use of deforested areas changes, the pattern of human settlement is altered and habitat fragmentation may provide opportunities for exchange and transmission of parasites to the heretofore uninfected humans. Construction of water control projects can lead to shifts in such vector populations as snails and mosquitoes and their parasites. Construction of roads in previously inaccessible forested areas can lead to erosion, and stagnant ponds by blocking the flow of streams when the water rises during the rainy season. The combined effects of environmentally detrimental changes in local land use and alterations in global climate disrupt the natural ecosystem and can increase the risk of transmission of parasitic diseases to the human population.
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            Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking.

            Delayed type hypersensitivity (DTH) reactions are antigen-specific, cell-mediated immune responses which, depending on the antigen involved, mediate beneficial (resistance to viruses, bacteria, fungi, and certain tumors) or harmful (allergic dermatitis, autoimmunity) aspects of immune function. We have shown that acute stress administered immediately before antigenic challenge results in a significant enhancement of a skin DTH response in rats. A stress-induced trafficking or redeployment of leukocytes to the skin may be one of the factors mediating this immunoenhancement. Here we investigate the effects of varying the duration, intensity, and chronicity of stress on the DTH response and on changes in blood leukocyte distribution and glucocorticoid levels. Acute stress administered for 2 h prior to antigenic challenge, significantly enhanced the DTH response. Increasing the duration of stress from 2 h to 5 h produced the same magnitude enhancement in cutaneous DTH. Moreover, increasing the intensity of acute stress produced a significantly larger enhancement of the DTH response which was accompanied by increasing magnitudes of leukocyte redeployment. In contrast, chronic stress suppressed the DTH response when it was administered for 3 weeks before sensitization and either discontinued upon sensitization, or continued an additional week until challenge, or extended for one week after challenge. The stress-induced redeployment of peripheral blood lymphocytes was attenuated with increasing exposure to chronic stress and correlated with attenuated glucocorticoid responsivity. These results suggest that stress-induced alterations in lymphocyte redeployment may play an important role in mediating the bi-directional effects of acute versus chronic stress on cell-mediated immunity in vivo.
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              Evidence for the role of infectious disease in species extinction and endangerment.

              Infectious disease is listed among the top five causes of global species extinctions. However, the majority of available data supporting this contention is largely anecdotal. We used the IUCN Red List of Threatened and Endangered Species and literature indexed in the ISI Web of Science to assess the role of infectious disease in global species loss. Infectious disease was listed as a contributing factor in <4% of species extinctions known to have occurred since 1500 (833 plants and animals) and as contributing to a species' status as critically endangered in <8% of cases (2,852 critically endangered plants and animals). Although infectious diseases appear to play a minor role in global species loss, our findings underscore two important limitations in the available evidence: uncertainty surrounding the threats to species survival and a temporal bias in the data. Several initiatives could help overcome these obstacles, including rigorous scientific tests to determine which infectious diseases present a significant threat at the species level, recognition of the limitations associated with the lack of baseline data for the role of infectious disease in species extinctions, combining data with theory to discern the circumstances under which infectious disease is most likely to serve as an agent of extinction, and improving surveillance programs for the detection of infectious disease. An evidence-based understanding of the role of infectious disease in species extinction and endangerment will help prioritize conservation initiatives and protect global biodiversity.
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                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B.
                The Royal Society
                0962-8452
                1471-2954
                May 13 2020
                May 06 2020
                May 13 2020
                : 287
                : 1926
                : 20200062
                Affiliations
                [1 ]School of Biological Sciences, Washington State University, PO Box 644236, Pullman, WA 99164-4236, USA
                Article
                10.1098/rspb.2020.0062
                ef134c42-8d81-4429-b6ef-59a9df796718
                © 2020

                https://royalsociety.org/-/media/journals/author/Licence-to-Publish-20062019-final.pdf

                https://royalsociety.org/journals/ethics-policies/data-sharing-mining/

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