Mammalian Biology

, Volume 79, Issue 3, pp 183–188 | Cite as

Effects of sewage-water contamination on the immune response of a desert bat

  • Shai PilosofEmail author
  • Carmi Korine
  • Marianne S. Moore
  • Boris R. Krasnov
Original Investigation


Environmental pollutants may negatively affect the immune system of animals. Yet, this phenomenon has not been studied thoroughly in terrestrial animals that use polluted water for drinking and/or foraging. We experimentally tested the hypothesis that exposure to sewage water would affect the activation of the immune response in the bat Pipistrellus kuhlii that drinks from bodies of open water. We selected two water sources where bats forage in the Negev desert, Israel: natural springs and a sewage-polluted man-made reservoir. We captured 13 non-reproductive female bats in the vicinity of the natural springs and offered seven of them water from the sewage-polluted source for 30 days (treatment) and the remaining six bats were offered water from the natural spring (control). Consumption of contaminated water did not alter the bactericidal ability of blood plasma or the proportions of monocytes circulating in the blood. However, our data provided evidence that the 30-day treatment can cause a decrease in the relative levels of neutrophils and an increase in the levels of lymphocytes. Our study provides a first account for the effect of sewage pollution on bat immune response which may be important in desert environments, where water sources are scarce. We suggest hypotheses for future, more focused studies.


Chiroptera Immune function Leukocyte profiles Sewage pollution Desert 


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  1. Abbott, I.M., Sleeman, D.P., Harrison, S., 2009. Bat activity affected by sewage effluent in Irish rivers. Biol. Conserv. 142, 2904–2914.CrossRefGoogle Scholar
  2. Anderson, E.P., Maldonado-Ocampo, JA, 2011. A regional perspective on the diversity and conservation of tropical Andean fishes. Conserv. Biol. 25, 30–39.CrossRefGoogle Scholar
  3. Barton, K., 2013. MuMIn: Multi-Model Inference.
  4. Beldomenico, P.M., Telfer, S., Gebert, S., Lukomski, L, Bennett, M., Begon, M., 2008. The dynamics of health in wild field vole populations: a haematological perspective. J. Anim. Ecol. 77, 984–997.CrossRefGoogle Scholar
  5. Brown, B.A., 1993. Hematology: Principles and Procedures. Lea & Febiger, Malvern, UK.Google Scholar
  6. Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York.Google Scholar
  7. Christe, P., Arlettaz, R., Vogel, P., 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol. Lett. 3, 207–212.CrossRefGoogle Scholar
  8. Christin, M.S., Gendron, A.D., Brousseau, P., Ménard, L., Marcogliese, D.J., Cyr, D., Ruby, S., Fournier, M., 2003. Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ. Toxicol. Chem. 22, 1127–1133.CrossRefGoogle Scholar
  9. Conrad, P.A., Miller, M.A., Kreuder, C., James, E.R., Mazet, J., Dabritz, H., Jessup, D.A., Gulland, F., Grigg, M.E., 2005. Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 35, 1155–1168.CrossRefGoogle Scholar
  10. Cotter, S.C., Simpson, S.J., Raubenheimer, D., Wilson, K., 2011. Macronutrient balance mediates trade-offs between immune function and life history traits. Funct. Ecol. 25, 186–198.CrossRefGoogle Scholar
  11. Cottontail, V.M., Wellinghausen, N., Kalko, E.K.V., 2009. Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panamá. Parasitology 136, 1133–1145.CrossRefGoogle Scholar
  12. Davis, A.K., Maney, D.L., Maerz, J.C., 2008. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct. Ecol. 22, 760–772.CrossRefGoogle Scholar
  13. Jones, G., Jacobs, D., Kunz, T., Willig, M., Racey, PA, 2009. Carpe noctem: the importance of bats as bioindicators. Endangered Species Res. 8, 93–115.CrossRefGoogle Scholar
  14. Kalcounis-Rueppell, M.C., Payne, V., Huff, S., Boyko, A., 2007. Effects of wastewater treatment plant effluent on bat foraging ecology in an urban stream system. Biol. Conserv. 138, 120–130.CrossRefGoogle Scholar
  15. Korine, C., Pinshow, B., 2004. Guild structure, foraging space use, and distribution in a community of insectivorous bats in the Negev Desert. J. Zool. 262, 187–196.CrossRefGoogle Scholar
  16. Kozul, C.D., Hampton, T.H., Davey, J.C., Gosse, J.A., Nomikos, A.P., Eisenhauer, P.L., Weiss, D.J., Thorpe, J.E., Ihnat, M.A., Hamilton, J.W., 2009. Chronic exposure to arsenic in the drinking water alters the expression of immune response genes in mouse lung. Environ. Health Perspect. 117, 1108–1115.CrossRefGoogle Scholar
  17. Lambris, J.D., Ricklin, D., Geisbrecht, B.V., 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6, 132–142.CrossRefGoogle Scholar
  18. Maceda-Veiga, A., Monroy, M., Viscor, G., De Sostoa, A., 2010. Changes in non-specific biomarkersinthe Mediterranean barbel (Barbus meridionalis) exposed to sewage effluents in a Mediterranean stream (Catalonia, NE Spain). Aquat. Toxicol. 100, 229–237.CrossRefGoogle Scholar
  19. Milla, S., Depiereux, S., Kestemont, P., 2011. The effects of estrogenic and androgenic endocrine disruptors on the immune system offish: a review. Ecotoxicology 20, 305–319.CrossRefGoogle Scholar
  20. Mitch, A.A., Gasner, K.C., Mitch, W.A., 2010. Fecal coliform accumulation within a river subject to seasonally-disinfected wastewater discharges. Water Res. 44, 4776–4782.CrossRefGoogle Scholar
  21. Moore, M.S., Reichard, J.D., Murtha, T.D., Zahedi, B., Fallier, R.M., Kunz, T.H., 2011. Specific alterations in complement protein activity of little brown Myotis (Myotis lucifugus) hibernating in white-nose syndrome affected sites. PloS ONE 6, e27430.CrossRefGoogle Scholar
  22. Nagelkerke, N.J.D., 1991. A note on a general definition of the coefficient of determination. Biometrika 78, 691.CrossRefGoogle Scholar
  23. Nollet, L.M.L., 2007. Handbook of Water Analysis. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
  24. O’Connor, B.H., 1984. A Color Atlas and Instruction Manual of Peripheral Blood Cell Morphology. Lippincott Williams & Wilkins, Baltimore, USA.Google Scholar
  25. O’Shea, T.J., Clark Jr., D.R., Boyle, T.P., 2001. Impacts of mine-related contaminants on bats. In: Vorie, K.C., Throgmorton, D. (Eds.), The Proceedings of Bat Conservation and Mining: A Technical Interactive Forum. Office of Surface Mining, St. Louis, MO, USA.Google Scholar
  26. Park, K.J., Cristinacce, A., 2006. Use of sewage treatment works as foraging sites by insectivorous bats. Anim. Conserv. 9, 259–268.CrossRefGoogle Scholar
  27. Pikula, J., Zukal, J., Adam, V., Bandouchova, H., Beklova, M., Hajkova, P., Horakova, J., Kizek, R., Valentikova, L., 2010. Heavy metals and metallothionein in vespertil-ionidbats foraging over aquatic habitats in the Czech Republic. Environ. Toxicol. Chem. 29, 501–506.CrossRefGoogle Scholar
  28. Pilosof, S., Dick, C.W., Korine, C., Patterson, B.D., Krasnov, B.R., 2012. Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS ONE 7, e41487.CrossRefGoogle Scholar
  29. Pinheiro, J., Bates, S.J., DebRoy, S., Sarkar, D., 2011. lme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1–101.Google Scholar
  30. R Development Core Team, 2012. R: A Language and Environment for Statistical Computing.Google Scholar
  31. Raida, M.K., Buchmann, K., 2009. Innate immune response in rainbow trout (Oncorhynchus mykiss) against primary and secondary infections with Yersinia ruckeri O1. Dev. Comp. Immunol. 33, 35–45.CrossRefGoogle Scholar
  32. Razgour, O., Korine, C., Saltz, D., 2010. Pond characteristics as determinants of species diversity and community composition in desert bats. Anim. Conserv. 13, 505–513.CrossRefGoogle Scholar
  33. Reynolds, D.S., Korine, C., 2009. Body composition analysis. In: Kunz, T.H., Parsons, M.S. (Eds.), Ecological and Behavioral Methods for the Study of Bats. The Johns Hopkins University Press, Baltimore, USA, pp. 674–691.Google Scholar
  34. Rohr, J.R., McCoy, K.A., 2010. A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environ. Health Perspect. 118, 20–32.CrossRefGoogle Scholar
  35. Schwarzenbach, R.P., Escher, B.I., Fenner, K., Hofstetter, T.B., Johnson, C.A., von Gunten, U., Wehrli, B., 2006. The challenge of micropollutants in aquatic systems. Science 313, 1072–1077.CrossRefGoogle Scholar
  36. Song, W.-C., Rosa Sarrias, M., Lambris, J.D., 2000. Complement and innate immunity. Immunopharmacology 49, 187–198.CrossRefGoogle Scholar
  37. Stockham, S.L., Scott, M.A., 2010. Fundamentals of Veterinary Clinical Pathology. Blackwell Publishing, Ames, Iowa, USA.Google Scholar
  38. Suorsa, P., Helle, H., Koivunen, V., Huhta, E., Nikula, A., Hakkarainen, H., 2004. Effects of forest patch size on physiological stress and immunocompetence in an areasensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment. Proc. R. Soc. Lond. B 271, 435–440.CrossRefGoogle Scholar
  39. Tieleman, I.B., Williams, J.B., Ricklefs, R.E., Klasing, K.C., 2005. Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. R. Soc. Lond. B 272, 1715–1720.CrossRefGoogle Scholar
  40. Voigt, C.C., Cruz-Neto, A., 2009. Energetic analysis of bats. In: Kunz, T.H., Parsons, M.S. (Eds.), Ecological and Behavioral Methods for the Study of Bats. The Johns Hopkins University Press, Baltimore, USA, pp. 623–645.Google Scholar
  41. Weiss, D.J., Wardrop, K.J., 2010. Schalm’s Veterinary Hematolog. Blackwell Publishing Ltd., Ames, Iowa, USA.Google Scholar
  42. Zipfel, P.F., Skerka, C., 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729–740.CrossRefGoogle Scholar
  43. Zipfel, P.F., Würzner, R., Skerka, C., 2007. Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol. Immunol. 44, 3850–3857.CrossRefGoogle Scholar
  44. Zocche, J.J., Dimer Leffa, D., Paganini Damiani, A., Carvalho, F., Avila Mendonca, R., lochims dos Santos, C.E., Appel Boufleur, L., Ferraz Dias, J., de Andrade, V.M., 2010. Heavy metals and DNA damage in blood cells of insectivore bats in coal mining areas of Catarinense coal basin, Brazil. Environ. Res. 110, 684–691.CrossRefGoogle Scholar
  45. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., Smith, G.M., 2009. Mixed Effects Models and Extensions in Ecology with R., 1st ed., Statistics. Springer, New York.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2014

Authors and Affiliations

  • Shai Pilosof
    • 1
    • 4
    Email author
  • Carmi Korine
    • 1
    • 2
  • Marianne S. Moore
    • 3
  • Boris R. Krasnov
    • 1
  1. 1.Albert Katz International School for Desert Studies and Mitrani Department of Desert EcologyJacob Blaustein Institutes for Desert Research, Ben-Gurion University of the NegevMidreshet Ben-GurionIsrael
  2. 2.The Dead Sea and the Arava Science CenterTamar Regional CouncilNeveh ZoharIsrael
  3. 3.Department of BiologyBucknell UniversityLewisburgUSA
  4. 4.Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the Negev, Sede Boqer CampusMidreshet Ben-GurionIsrael

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