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East-West Divide: temperature and land cover drive spatial variation of Toxoplasma gondii infection in Eurasian otters (Lutra lutra) from England and Wales

Published online by Cambridge University Press:  27 June 2017

WILLOW A. SMALLBONE Open the ORCID record for WILLOW A. SMALLBONE [Opens in a new window] ,
ELIZABETH A. CHADWICK Open the ORCID record for ELIZABETH A. CHADWICK [Opens in a new window] ,
JANET FRANCIS ,
EDWARD GUY ,
SARAH E. PERKINS ,
ELLIE SHERRARD-SMITH  and
JOANNE CABLE
WILLOW A. SMALLBONE
Affiliation:
School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK
ELIZABETH A. CHADWICK*
Affiliation:
School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK
JANET FRANCIS
Affiliation:
Toxoplasma Reference Unit, Public Health Wales Microbiology, Singleton Hospital, Swansea SA2 8QA, UK
EDWARD GUY
Affiliation:
Toxoplasma Reference Unit, Public Health Wales Microbiology, Singleton Hospital, Swansea SA2 8QA, UK
SARAH E. PERKINS
Affiliation:
School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK
ELLIE SHERRARD-SMITH
Affiliation:
School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK Department of Infectious Disease Epidemiology, MRC Centre for Outbreak Analysis and Modelling and NIHR Health Protection Research Unit in Modelling Methodology, Imperial College London, Norfolk Place, London, W2 1PG, UK
JOANNE CABLE
Affiliation:
School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK
*
*Corresponding author: School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK. E-mail: [email protected]
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Summary

Toxoplasma gondii, a zoonotic parasite of global importance, infects all endothermic vertebrates, with extensive health implications. The prevalence of this parasite is seldom monitored in wildlife. Here, a semi-aquatic species, the Eurasian otter (Lutra lutra) was used as a model to assess the potential effect of climate, land cover and biotic factors on T. gondii seroprevalence in British wildlife. The Sabin–Feldman cytoplasm-modifying dye test identified T. gondii antibodies in 25·5% of blood samples from otters found dead, mainly as road kill, in England and Wales, between 2004 and 2010. Otters in the east of England were more likely to be infected with T. gondii than those in western regions. Land cover and temperature are key determinants of T. gondii infection risk, with more infection in arable areas and lower infection where temperatures are higher. The probability of T. gondii infection increased with host age, reflecting cumulative exposure with time, but there was no association between T. gondii seroprevalence and cause of host death.

Keywords

landscape ecologymeteorological variationspatial distributionzoonosistoxoplasmosisotter
Type
Research Article
Information
Parasitology , Volume 144 , Issue 11 , September 2017 , pp. 1433 - 1440
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Afonso, E., Thulliez, P., Pontier, D. and Gilot-Fromont, E. (2007). Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal. Parasitology 134, 1963–1971.Google Scholar
Afonso, E., Germain, E., Poulle, M. L., Ruette, S., Devillard, S., Say, L., Villena, I., Aubert, D. and Gilot-Fromont, E. (2013). Environmental determinants of spatial and temporal variations in the transmission of Toxoplasma gondii in its definitive hosts. International Journal for Parasitology: Parasites and Wildlife 2, 278–285.Google Scholar
Blanco-Garrido, F., Prenda, J. and Narvaez, M. (2008). Eurasian otter (Lutra lutra) diet and prey selection in Mediterranean streams invaded by centrarchid fishes. Biological Invasions 10, 641–648.Google Scholar
Chadwick, E. A., Simpson, V. R., Nicholls, A. and Slater, F. M. (2011). Lead levels in Eurasian otters decline with time and reveal interactions between sources, prevailing weather, and stream chemistry. Environmental Science & Technology 45, 1911–1916.Google Scholar
Chadwick, E. A., Cable, J., Chinchen, A., Francis, J., Guy, E., Kean, E. F., Paul, S. C., Perkins, S. E., Sherrard-Smith, E., Wilkinson, C. and Forman, D. W. (2013). Seroprevalence of Toxoplasma gondii in the Eurasian otter (Lutra lutra) in England and Wales. Parasites & Vectors 6, 75.Google Scholar
Clarke, G. P., White, P. C. L. and Harris, S. (1998). Effects of roads on badger Meles meles populations in south-west England. Biological Conservation 86, 117–124.Google Scholar
Cole, R. A., Lindsay, D. S., Howe, D. K., Roderick, C. L., Dubey, J. P., Thomas, N. J. and Baeten, L. A. (2000). Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). Journal of Parasitology 86, 526–530.Google Scholar
Corbett, G. H. (1966). The Terrestrial Mammals of Western Europe. Foulis, London.Google Scholar
Couvreur, J. and Desmonts, G. (1962). Congenital and maternal toxoplasmosis. Developmental Medicine & Child Neurology 4, 519–530.Google Scholar
Dabritz, H. A., Miller, M. A., Atwill, R., Gardner, I. A., Leutenegger, C. M., Melli, A. C. and Conrad, P. A. (2007). Detection of Toxoplasma gondii-like oocysts in cat faeces and estimates of the environmental oocyst burden. Journal of the American Veterinary Medical Association 231, 1676–1684.Google Scholar
Di Guardo, G., Proietto, U., Di Francesco, C. E., Marsilio, F., Zaccaroni, A., Scaravelli, D., Mignone, W., Garibaldi, F., Kennedy, S., Forster, F., Iulini, B., Bozzetta, E. and Casalone, C. (2010). Cerebral toxoplasmosis in striped dolphins (Stenella coeruleoalba) stranded along the Ligurian Sea coast of Italy. Veterinary Pathology 47, 245–253.CrossRefGoogle ScholarPubMed
Dubey, J. P. (1998). Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Veterinary Parasitology 74, 75–77.Google Scholar
Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL.Google Scholar
Dubey, J. P., Miller, N. L. and Frenkel, M. D. (1970). The Toxoplasma gondii oocysts from cat faeces. Journal of Experimental Medicine 132, 636–662.Google Scholar
Dubey, J. P., Felix, T. A. and Kwok, O. C. H. (2010). Serological and parasitological prevalence of Toxoplasma gondii in wild birds from Colorado. Journal of Parasitology 96, 937–939.CrossRefGoogle ScholarPubMed
Dumètre, A. and Dardé, M. L. (2003). How to detect Toxoplasma gondii oocysts in environmental samples? Federation of European Microbiological Societies: Microbiology Reviews 27, 651–661.Google ScholarPubMed
Dumètre, A., Dubey, J. P., Ferguson, D. J. P., Bongrand, P., Azas, N. and Puech, P. H. (2013). Mechanics of the Toxoplasma gondii oocyst wall. Proceedings of the National Academy of Sciences 110, 11535–11540.Google Scholar
Dzbeński, T. H. and Zielińska, E. (1976). Antibody-induced formation of caps in Toxoplasma gondii . Experientia 32, 454–456.Google Scholar
Environment Agency (2009). Land use and environmental services: resource efficiency science programme Science report: SC080014/SR1 Environment Agency, Bristol, UK.Google Scholar
Fayer, R., Dubey, J. P. and Lindsay, D. S. (2004). Zoonotic protozoa: from land to sea. Trends in Parasitology 20, 531–536.Google Scholar
Flatt, A. and Shetty, N. (2013). Seroprevalence and risk factors for toxoplasmosis among antenatal women in London: a re-examination of risk in an ethnically diverse population. European Journal of Public Health 23, 648–652.Google Scholar
Flegr, J., Klose, J., Novotná, M., Berenreitterová, M. and Havlícek, J. (2009). Increased incidence of traffic accidents in Toxoplasma-infected military drivers and protective effect RhD molecule revealed by a large-scale prospective cohort study. BMC Infectious Diseases 9, 72.Google Scholar
Food Standard Agency (2012). Ad hoc group on vulnerable groups: risk profile in relation to Toxoplasma in the food chain. 14–18.Google Scholar
Forman, D., West, N., Francis, J. and Guy, E. (2009). The seroprevalence of Toxoplasma gondii in British marine mammals. Memorias Do Instituto Oswaldo Cruz 104, 296–298.Google Scholar
Frenkel, J. K. (2000). Biology of Toxoplasma gondii . In Congenital Toxoplasmosis: Scientific Background, Clinical Management and Control (ed. Ambroise-Thomas, P. and Peterse, E.), pp. 9–25. Springer-Verlag, Paris.Google Scholar
Frenkel, J. K. and Dubey, J. P. (1973). Effects of freezing on the viability of Toxoplasma oocysts. Journal of Parasitology, 59, 587–588.Google Scholar
Fuller, R. M., Smith, G. M., Sanderson, J. M., Hill, R. A. and Thomson, A. G. (2002). The UK Land Cover Map 2000: construction of a parcel-based vector map from satellite images. Cartographic Journal 39, 15–25.Google Scholar
Gilot-Fromont, E., Lélu, M., Dardé, M.-L., Richomme, C., Aubert, D., Afonso, E., Mercier, A., Gotteland, C. and Villena, I. (2012). The life cycle of Toxoplasma gondii in the natural environment. In Toxoplasmosis – Recent Advances (ed. Djurković Djaković, O.). InTech. doi: 10.5772/48233.Google Scholar
Gotteland, C., McFerrin, B. M., Zhao, X., Gilot-Fromont, E. and Lélu, M. (2014). Agricultural landscape and spatial distribution of Toxoplasma gondii in rural environment: an agent-based model. International Journal of Health Geographics 13, 1–11.CrossRefGoogle ScholarPubMed
Hari Dass, S. A. and Vyas, A. (2014). Toxoplasma gondii infection reduces predator aversion in rats through epigenetic modulation in the host medial amygdala. Molecular Ecology 23, 6114–6122.Google Scholar
Hill, D. and Dubey, J. P. (2002). Toxoplasma gondii: transmission, diagnosis and prevention. Clinical Microbiology and Infection 8, 634–640.Google Scholar
Hill, D. E., Chirukandoth, S., Dubey, J. P., Lunney, J. K. and Gamble, H. R. (2006). Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Veterinary Parasitology 141, 9–17.Google Scholar
Hollings, T., Jones, M., Mooney, N. and McCallum, H. (2013). Wildlife disease ecology in changing landscapes: mesopredator release and to Toxoplasmosis. International Journal for Parasitology: Parasites and Wildlife 2, 110–118.Google Scholar
Jones, J. L. and Dubey, J. P. (2010). Experimental parasitology waterborne toxoplasmosis – recent developments. Experimental Parasitology 124, 10–25.CrossRefGoogle ScholarPubMed
Kruuk, H. (2006). Otters: Ecology, Behaviour and Conservation. Oxford University Press, Oxford, pp. 58–77.Google Scholar
Kulldorff, M. (1997). A spatial scan statistic. Communications in Statistics – Theory and Methods 26, 1481–1496.Google Scholar
Kulldorff, M., Athas, W. F., Feurer, E. J., Miller, B. A. and Key, C. R. (1998). Evaluating cluster alarms: a space-time scan statistic and brain cancer in Los Alamos, New Mexico. American Journal of Public Health 88, 1377–1380.Google Scholar
Kuticic, V. and Wikerhauser, T. (1994). Effects of some chemical and physical factors on the viability of Toxoplasma gondii . Veterinarski Archive 64, 89–93.Google Scholar
Lehmann, T., Graham, D. H., Dahl, E., Sreekumar, C., Launer, F., Corn, J. L., Gamble, H. R. and Dubey, J. P. (2003). Transmission dynamics of Toxoplasma gondii on a pig farm. Infection, Genetics and Evolution 3, 135–141.Google Scholar
McGregor, R. L., Bender, D. J. and Fahrig, L. (2008). Do small mammals avoid roads because of the traffic? Journal of Applied Ecology 45, 117–123.Google Scholar
Miller, N. L., Frenkel, J. K. and Dubey, J. P. (1972). Oral infections with Toxoplasma cysts and oocysts in felines, other mammals, and in birds. Journal of Parasitology 58, 928–937.CrossRefGoogle ScholarPubMed
Pederson, M. G., Preben, P. B., Norgaard-Pederson, B. and Postolache, M. D. (2012). Toxoplasma gondii infection and self-directed violence in mothers. Archives of General Psychiatry 69, 1123–1130.Google Scholar
Perry, M. and Hollis, D. (2005). The development of a new set of long-term climate averages for the UK. International Journal of Climatology 25, 1023–1039.Google Scholar
Poirotte, C., Kappeler, P. M., Ngoubangoye, B., Bourgeois, S., Moussodji, M. and Charpentier, M. J. E. (2016). Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Current Biology 26, 98–99.CrossRefGoogle ScholarPubMed
R Development Core Team (2015) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.Google Scholar
Richomme, C., Afonso, E., Tolon, V., Ducrot, C., Halos, L., Alliot, A., Perret, C., Thomas, M., Boireau, P. and Gilot-Fromont, E. (2010). Seroprevalence and factors associated with Toxoplasma gondii infection in wild boar (Sus scrofa) in a Mediterranean island. Epidemiology and Infection 138, 1257–1266.Google Scholar
Rosenthal, B. M. (2009). How has agriculture influenced the geography and genetics of animal parasites? Trends in Parasitology 25, 67–70.CrossRefGoogle ScholarPubMed
Sabin, A. B. and Feldman, H. A. (1948). Dyes as microchemical indicators of a new immunity phenomenon affecting a protozoan parasite (Toxoplasma). Science 108, 660–663.Google Scholar
Sepúlveda, M. A., Mu, C., Rosenfeld, C., Jara, R., Pelican, K. M. and Hill, D. (2011). Toxoplasma gondii in feral American minks at the Maullín river, Chile. Veterinary Parasitology 175, 60–65.Google Scholar
Sevila, J., Richomme, C., Hoste, H., Candela, M. G., Gilot-Fromont, E., Rodolakis, A., Cebe, N., Picot, D., Merlot, J. and Verheyden, H. (2014). Does land use within the home range drive the exposure of roe deer (Capreolus capreolus) to two abortive pathogens in a rural agro-ecosystem? Acta Theriologica 59, 571–581.Google Scholar
Shapiro, K., Conrad, P. A., Mazet, J. A. K., Wallender, W. W., Miller, W. A. and Largier, J. L. (2010). Effect of estuarine wetland degradation on transport of Toxoplasma gondii surrogates from land to sea. Applied and Environmental Microbiology 76, 6821–6828.Google Scholar
Simon, A., Chambellant, M., Ward, B. J., Simard, M., Proulx, J. F., Levesque, B., Bigras-Poulin, M., Rousseau, A. N. and Ogden, N. H. (2011). Spatio-temporal variations and age effect on Toxoplasma gondii seroprevalence in seals from the Canadian Arctic. Parasitology 138, 1362–1368.Google Scholar
Simpson, V. R. (2000). Post mortem protocol for otters. In: Proceedings of the First Otter Toxicology Conference of the First Otter Toxicology Conference. Journal of the International Otter Survival Fund 1, 159–166.Google Scholar
Sobrino, R., Cabezón, O., Millán, J., Pabón, M., Arnal, M. C., Luco, D. F., Gortázar, C., Dubey, J. P. and Almeria, S. (2007). Seroprevalence of Toxoplasma gondii antibodies in wild carnivores from Spain. Veterinary Parasitology 148, 187–192.Google Scholar
Stoehr, A. and Kokko, H. (2006). Sex dimorphism in immunocompetence: what does life history theory predict? Behavioural Ecology 17, 751–756.Google Scholar
Sugden, K., Moffitt, T. E., Pinto, L., Poulton, R., Williams, B. S. and Caspi, A. (2016). Is Toxoplasma gondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLoS ONE 11, e0148435.CrossRefGoogle ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.CrossRefGoogle ScholarPubMed
Thomas, R., Vaughan, I. and Lello, J. (2013) Data Analysis with R Statistical Software: a Guidebook for Scientists. Eco-explore, Caerphilly, pp. 58–59.Google Scholar
Tizard, I. R., Fish, A. and Quinn, J. P. (1976). Some observations on the epidemiology of toxoplasmosis in Canada. Journal of Hygiene 77, 11–21.Google Scholar
Webster, J. P. (2007). The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophrenia Bulletin 33, 752–756.Google Scholar
Zhang, M., Yang, Z., Wang, S., Tao, L., Xu, L., Yan, R., Song, X. and Li, X. (2014). Detection of Toxoplasma gondii in shellfish and fish in parts of China. Veterinary Parasitology 200, 85–89.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.Google Scholar