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      Immune-mediated hookworm clearance and survival of a marine mammal decrease with warmer ocean temperatures

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          Abstract

          Increases in ocean temperature are associated with changes in the distribution of fish stocks, and the foraging regimes and maternal attendance patterns of marine mammals. However, it is not well understood how these changes affect offspring health and survival. The maternal attendance patterns and immunity of South American fur seals were assessed in a rookery where hookworm disease is the main cause of pup mortality. Pups receiving higher levels of maternal attendance had a positive energy balance and a more reactive immune system. These pups were able to expel hookworms through a specific immune mediated mechanism and survived the infection. Maternal attendance was higher in years with low sea surface temperature, therefore, the mean hookworm burden and mortality increased with sea surface temperature over a 10-year period. We provide a mechanistic explanation regarding how changes in ocean temperature and maternal care affect infectious diseases dynamics in a marine mammal.

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          Every year off the coasts of Chile, Guafo Island becomes a nursery for South American fur seals pups. Mother fur seals leave their young on the beaches, going out at sea to hunt for fish before returning to the shore to nurse. These first few months are dangerous for young seals, with many dying because of hookworms, parasites that latch to the wall of the bowels to suck blood. However, the immune system of the pups is usually able to mount a response and fight off these parasites.

          Even though the pups stay on land, their lives depend on the health of the ocean that feeds their nursing mothers. In recent years, sea temperature has been rising rapidly, which modifies winds and water currents. This can set off a chain of events that results in fewer fish being available for seals and other marine mammals to eat. Researchers know that years with warmer waters are associated with changes in the pattern of the mothers’ hunting trips, more pups’ deaths, and a weaker immune system in young fur seals. However, the mechanisms that connect these different factors are still unclear.

          To explore this, Seguel et al. followed South American fur seals colonies on Guafo Island for several years, tracking the mothers’ trips and monitoring the health of the pups by looking at their levels of blood sugar, whether they carry hookworms, and certain elements of their immune system. Results showed that in years when the sea is warmer, fur seal mothers are gone hunting for longer: they spend less time nursing their young, which then grow slower. These young seals also have lower levels of blood sugar, and so they have less energy to create the immune response necessary to clear off parasitic worms. In fact, in years with warmer seas, almost half of the pups die from hookworm infections.

          The work by Seguel et al. shows that warmer oceans directly weaken the immune defenses of certain marine mammals. If temperatures keep rising, infectious diseases may kill more of these animals. Further work is now needed to explore if strategies could be developed to help seal populations, for example by treating the pups with drugs that eliminate the parasites.

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          Most cited references43

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          Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

          Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.
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            Impact of Childhood Malnutrition on Host Defense and Infection.

            The global impact of childhood malnutrition is staggering. The synergism between malnutrition and infection contributes substantially to childhood morbidity and mortality. Anthropometric indicators of malnutrition are associated with the increased risk and severity of infections caused by many pathogens, including viruses, bacteria, protozoa, and helminths. Since childhood malnutrition commonly involves the inadequate intake of protein and calories, with superimposed micronutrient deficiencies, the causal factors involved in impaired host defense are usually not defined. This review focuses on literature related to impaired host defense and the risk of infection in primary childhood malnutrition. Particular attention is given to longitudinal and prospective cohort human studies and studies of experimental animal models that address causal, mechanistic relationships between malnutrition and host defense. Protein and micronutrient deficiencies impact the hematopoietic and lymphoid organs and compromise both innate and adaptive immune functions. Malnutrition-related changes in intestinal microbiota contribute to growth faltering and dysregulated inflammation and immune function. Although substantial progress has been made in understanding the malnutrition-infection synergism, critical gaps in our understanding remain. We highlight the need for mechanistic studies that can lead to targeted interventions to improve host defense and reduce the morbidity and mortality of infectious diseases in this vulnerable population.
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              Ocean temperatures chronicle the ongoing warming of Earth

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                Author and article information

                Contributors
                Role: Senior Editor
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                06 November 2018
                2018
                : 7
                : e38432
                Affiliations
                [1 ]deptDepartment of Pathology, College of Veterinary Medicine University of Georgia AthensUnited States
                [2 ]deptFacultad de Ciencias Biologicas Pontificia Universidad Catolica de Chile SantiagoChile
                [3 ]deptPhD Program in Conservation Medicine, Facultad de Ecología y Recursos Naturales Universidad Andrés Bello SantiagoChile
                [4 ]deptPrograma de Investigación Aplicada en Fauna Silvestre, Facultad de Ciencias Veterinarias Universidad Austral de Chile ValdiviaChile
                [5 ]deptFacultad de Ciencias Veterinarias, Instituto de Patología Animal Universidad Austral de Chile ValdiviaChile
                [6 ]deptDepartamento de Ciencias Básicas Universidad Santo Tomas OsornoChile
                [7 ]deptInstituto de Ciencias Clínicas Veterinarias Universidad Austral de Chile ValdiviaChile
                Max Planck Institute for Chemical Ecology Germany
                University of St Andrews United Kingdom
                University of St Andrews United Kingdom
                Walter Reed Army Institute of Research United States
                Author notes
                [†]

                Odum School of Ecology, University of Georgia, Georgia, United States.

                [‡]

                Facultad de Medicina Veterinaria, Universidad San Sebastián, Santiago, Chile.

                Author information
                http://orcid.org/0000-0002-0465-236X
                Article
                38432
                10.7554/eLife.38432
                6245726
                30398149
                184895c5-4546-4026-90b8-77f360e33edb
                © 2018, Seguel et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 16 May 2018
                : 26 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100001250, Morris Animal Foundation;
                Award ID: D16ZO-413
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007143, Society for Marine Mammalogy;
                Award ID: Small grants in aid
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007463, Rufford Foundation;
                Award ID: N 18815–1
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Microbiology and Infectious Disease
                Custom metadata
                In years with colder ocean temperatures, fur seal pups receive more maternal care and have a better energy balance, clearing hookworm infection earlier, which increases their chances of survival.

                Life sciences
                marine mammal,fur seal,immunology,climate change,parasites,other
                Life sciences
                marine mammal, fur seal, immunology, climate change, parasites, other

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