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Parasite prevalence increases with temperature in an avian metapopulation in northern Norway

Published online by Cambridge University Press:  12 April 2019

H. Holand Open the ORCID record for H. Holand [Opens in a new window] ,
H. Jensen ,
T. Kvalnes ,
J. Tufto ,
H. Pärn ,
B-E. Sæther  and
T. H. Ringsby
H. Holand*
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
H. Jensen
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
T. Kvalnes
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
J. Tufto
Affiliation:
Department of Mathematics, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
H. Pärn
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
B-E. Sæther
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
T. H. Ringsby
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, NO-7491 Trondheim, Norway
*
Author for correspondence: H. Holand, E-mail: Haakon.holand33@gmail.com
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Abstract

Climate and weather conditions may have substantial effects on the ecology of both parasites and hosts in natural populations. The strength and shape of the effects of weather on parasites and hosts are likely to change as global warming affects local climate. These changes may in turn alter fundamental elements of parasite–host dynamics. We explored the influence of temperature and precipitation on parasite prevalence in a metapopulation of avian hosts in northern Norway. We also investigated if annual change in parasite prevalence was related to winter climate, as described by the North Atlantic Oscillation (NAO). We found that parasite prevalence increased with temperature within-years and decreased slightly with increasing precipitation. We also found that a mild winter (positive winter NAO index) was associated with higher mean parasite prevalence the following year. Our results indicate that both local and large scale weather conditions may affect the proportion of hosts that become infected by parasites in natural populations. Understanding the effect of climate and weather on parasite–host relationships in natural populations is vital in order to predict the full consequence of global warming.

Keywords

Climatehouse sparrowNAOparasiteprecipitationprevalenceSyngamus tracheatemperature
Type
Research Article
Information
Parasitology , Volume 146 , Issue 8 , July 2019 , pp. 1030 - 1035
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Copyright
Copyright © Cambridge University Press 2019 

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References

Alcarro, J, Moreno, JM, Nováky, B, Bindi, M, Corobov, R, Devoy, RJN, Giannakopoulos, C, Martin, E, Olesen, JE and Shvidenko, A (2007) Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the intergovernmental Panel on Climate Change. Cambridge.Google Scholar
Altizer, S, Ostfeld, RS, Johnson, PTJ, Kutz, S and Harvell, CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514–519.10.1126/science.1239401Google Scholar
Anderson, RM and May, RM (1978) Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
Anderson, TR (2006) Biology of the Ubiquitous House Sparrow: From Genes to Populations. New York, NY: Oxford University Press.10.1093/acprof:oso/9780195304114.001.0001Google Scholar
Arneberg, P (2001) An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352–358.Google Scholar
Atkinson, CT, Thomas, NJ and Hunter, DB (2008) Parasitic Diseases of Wild Birds. Ames, Iowa: Wiley-Blackwell.Google Scholar
Bakke, TA (1973) Studies of the helminth fauna of Norway part 27 Syngamiasis in Norway. Norwegian Journal of Zoology 21, 299–303.Google Scholar
Barus, V (1966 a) The effect of temperature and air humidity on the development and the resistance of eggs of the nematode Syngamus trachea. Helminthologia (Bratislava) 7, 103–106.Google Scholar
Barus, V (1966 b) The longevity of the parasitic stages and the dynamics of eggs production of nematode Syngamus trachea in chicken and turkeys. Folia Parasitologica (Ceske Budejovice) 13, 274–277.Google Scholar
Barus, V (1966 c) Seasonal dynamics of the invasion extensity of the nematode Syngamus trachea in breeding turkeys Meleagris gallopavo f. domestica. Helminthologia (Bratislava) 7, 29–37.Google Scholar
Borg, AA, Pedersen, SA, Jensen, H and Westerdahl, H (2011) Variation in MHC genotypes in two populations of house sparrow (Passer domesticus) with different population histories. Ecology and Evolution 1, 145–159.10.1002/ece3.13Google Scholar
Bottari, T, Liguori, M, Trilles, JP, Giordano, D, Romeo, T, Perdichizzi, F and Rinelli, P (2013) Host-parasite relationship: occurrence and effect of Ceratothoa parallela (Otto, 1828) on Boops boops (L., 1758) in the Southern Tyrrhenian Sea. Journal of Applied Ichthyology 29, 896–900.Google Scholar
Burnham, K and Anderson, D (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. London: Springer.Google Scholar
Descamps, S (2013) Winter temperature affects the prevalence of ticks in an Arctic Seabird. PLoS One 8, e65374.Google Scholar
Dobson, AP (1990) Models for multi-species parasite–host communities. In Esch, G, Bush, AO and Aho, JM (eds), Parasite Communities: Patterns and Processes. London: Chapman & Hall, pp. 261–288.Google Scholar
Dormann, CF, Elith, J, Bacher, S, Buchmann, C, Carl, G, Carré, G, Marquéz, JRG, Gruber, B, Lafourcade, B, Leitão, PJ, Münkemüller, T, McClean, C, Osborne, PE, Reineking, B, Schröder, B, Skidmore, AK, Zurell, D and Lautenbach, S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46.Google Scholar
Harvell, CD, Mitchell, CE, Ward, JR, Altizer, S, Dobson, AP, Ostfeld, RS and Samuel, MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.Google Scholar
Harvell, D, Altizer, S, Cattadori, IM, Harrington, L and Weil, E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90, 912–920.Google Scholar
Helama, S and Holopainen, J (2012) Spring temperature variability relative to the North Atlantic Oscillation and sunspots – A correlation analysis with a Monte Carlo implementation. Palaeogeography, Palaeoclimatology, Palaeoecology 326, 128–134.Google Scholar
Hoar, BM, Ruckstuhl, K and Kutz, S (2012) Development and availability of the free-living stages of Ostertagia gruehneri, an abomasal parasite of barrenground caribou (Rangifer tarandus groenlandicus), on the Canadian tundra. Parasitology 139, 1093–1100.Google Scholar
Hoberg, EP, Polley, L, Jenkins, EJ, Kutz, SJ, Veitch, AM and Elkin, BT (2008) Integrated approaches and empirical models for investigation of parasitic diseases in northern wildlife. Emerging Infectious Diseases 14, 10–17.Google Scholar
Holand, H, Jensen, H, Tufto, J, Sæther, B-E and Ringsby, TH (2013) Temporal and spatial variation in prevalence of the parasite Syngamus trachea in a metapopulation of house sparrows (Passer domesticus). Parasitology 140, 1275–1286.Google Scholar
Holand, H, Kvalnes, T, Gamelon, M, Tufto, J, Jensen, H, Parn, H, Ringsby, TH and Sæther, B-E (2016) Spatial variation in senescence rates in a bird metapopulation. Oecologia 181, 865–871.Google Scholar
Hudson, PJ and Dobson, AP (1991) The Direct and Indirect Effects of the Caecal Nematode Trichostrongylus tenuis on Red Grouse. Oxford, UK: Oxford University Press.Google Scholar
Hurrell, JW (1995) Decadal trends in the north-Atlantic oscillation – regional temperatures and precipitation. Science 269, 676–679.Google Scholar
Jenkins, EJ, Veitch, AM, Kutz, SJ, Hoberg, EP and Polley, L (2006) Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis d. dalli). Parasitology 132, 387–401.Google Scholar
Jex, AR, Schneider, MA, Rose, HA and Cribb, TH (2007) Local climate aridity influences the distribution of thelastomatoid nematodes of the Australian giant burrowing cockroach. Parasitology 134, 1401–1408.Google Scholar
Karvonen, A, Rintamaki, P, Jokela, J and Valtonen, ET (2010) Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. International Journal for Parasitology 40, 1483–1488.Google Scholar
Kutz, SJ, Hoberg, EP, Polley, L and Jenkins, EJ (2005) Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society B-Biological Sciences 272, 2571–2576.Google Scholar
Kuzmina, SI, Bengtsson, L, Johannessen, OM, Drange, H, Bobylev, LP and Miles, MW (2005) The North Atlantic Oscillation and greenhouse-gas forcing. Geophysical Research Letters 32. doi: 10.1029/2004gl021064.Google Scholar
Lafferty, KD (2009) The ecology of climate change and infectious diseases. Ecology 90, 888–900.Google Scholar
Leathwick, DM (2013) The influence of temperature on the development and survival of the pre-infective free-living stages of nematode parasites of sheep. New Zealand Veterinary Journal 61, 32–40.Google Scholar
May, RM and Anderson, RM (1978) Regulation and stability of host-parasite population interactions. 2. Destabilizing processes. Journal of Animal Ecology 47, 249–267.Google Scholar
Miterpakova, M, Dubinsky, P, Reiterova, K and Stanko, M (2006) Climate and environmental factors influencing Echinococcus multilocularis occurrence in the Slovak Republic. Annals of Agricultural and Environmental Medicine 13, 235–242.Google Scholar
O'Connor, LJ, Walkden-Brown, SW and Kahn, LP (2006) Ecology of the free-living stages of major trichostrongylid parasites of sheep. Veterinary Parasitology 142, 1–15.Google Scholar
Paredes-Esquivel, C, del Rio, R, Monerris, M, Borras, D, Laglera, LM and Miranda, MA (2012) The influence of sheep age group on the seasonal prevalence of oestrosis in the island of Majorca. Veterinary Parasitology 186, 538–541.Google Scholar
Pärn, H, Ringsby, TH, Jensen, H and Sæther, B-E (2012) Spatial heterogeneity in the effects of climate and density-dependence on dispersal in a house sparrow metapopulation. Proceedings of the Royal Society B-Biological Sciences 279, 144–152.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ringsby, TH, Sæther, B-E, Tufto, J, Jensen, H and Solberg, EJ (2002) Asynchronous spatiotemporal demography of a house sparrow metapopulation in a correlated environment. Ecology 83, 561–569.Google Scholar
Sacks, BN, Chomel, BB and Kasten, RW (2004) Modeling the distribution and abundance of the non-native parasite, canine heartworm, in California coyotes. Oikos 105, 415–425.Google Scholar
Sherrard-Smith, E, Chadwick, EA and Cable, J (2013) Climatic variables are associated with the prevalence of biliary trematodes in otters. International Journal for Parasitology 43, 729–737.Google Scholar
Tinsley, RC, York, JE, Everard, ALE, Stott, LC, Chapple, SJ and Tinsley, MC (2011) Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on egg development. Parasitology 138, 1029–1038.Google Scholar
Westgarth-Smith, AR, Roy, DB, Scholze, M, Tucker, A and Sumpter, JP (2012) The role of the North Atlantic Oscillation in controlling UK butterfly population size and phenology. Ecological Entomology 37, 221–232.Google Scholar
Wilson, K, Bjørnstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Diseases. New York: Oxford University Press, pp. 6–44.Google Scholar
Zamora-Vilchis, I, Williams, SE and Johnson, CN (2012) Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS One 7, e39208.Google Scholar
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