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Prevalence of coccidia parasites (Protozoa) in red squirrels ( Sciurus vulgaris): effects of host phenotype and environmental factors

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Abstract

We investigated the relative importance of environmental factors versus host phenotype in determining parasite prevalence in Eurasian red squirrels ( Sciurus vulgaris). One hundred and forty-three fecal samples of 116 different squirrels collected in 2000 and 2001 from five study areas in the Italian Alps, were examined for intestinal protozoans. Two species of Eimeria were present with a medium to high prevalence in both years and in all areas, while two other species were rare, occurring only in some areas and not in all years. Cryptosporidium parvum had a high prevalence in the two study areas of the Western Alps, while in the three areas of the Central Alps it was recorded only once. The prevalence of Eimeria sciurorum and C. parvum fluctuated in parallel with squirrel density, suggesting a possible correlation between the presence of these protozoans and host density. A gender effect on E. sciurorum prevalence at low density could be explained by different space use patterns and social organization of males and females. C. parvum occurred more frequently in young squirrels, suggesting an acquired immunity in adults, but age-related susceptibility was not found for eimerian species. The coccidian community was more similar within than between regions, and study area and year were key parameters in predicting coccidia infection. There was no evidence of competition between coccidian species, but one positive interaction between E. sciurorum and E. andrewsi was observed. Our results suggest that the effects of geographic region, area features, and year effects probably related to fluctuations in host population density, were more important than individual phenotypic host characteristics in structuring the coccidian assemblage and determining levels of parasite prevalence in red squirrel populations.

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References

  • Anderson RM, May RM (1979) Population biology of infection disease. Part I. Nature 280:361–367

    CAS  PubMed  Google Scholar 

  • Bertolino S, Canestri Trotti G (2001) Cryptosporidium parvum in the European red squirrel Sciurus vulgaris. Proceedings of the 18th International Conference of the World Association for the Advancement of Veterinary Parasitology, Stresa, Italy. p 21

  • Bull SA, Chalmers RM, Sturdee AP, Healing TD (1998) A survey of Cryptosporidium species in Skomer bank voles ( Clethrionomys glareolus skomerensis). J Zool 244:119–122

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference. A practical information-theoretic approach. Springer, New York

  • Bush AO, Lafferty KD, Lotz JM, Shostaki AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    CAS  PubMed  Google Scholar 

  • Casemore D, Wright SE, Coop RL (1997) Crytosporidiosis—human and animal epidemiology. In: Fayer R (ed) Cryptosporidium and Crytosporidiosis. CRC, Boca Raton, Fla., pp 65–92

  • Chalmers RM, Sturdee AP, Bull SA, Miller AM (1995) Rodent reservoirs of Cryptosporidium. In: Betts WB, Casemore D, Fricker C, Smith H, Watkins J (eds) Protozoan parasites and water. Special Publication no. 168. The Royal Society of Chemistry, CUP, UK, pp 63–66

  • Current WL (1989) Cryptosporidium spp. In: Walzer PD, Genta RM (eds) Parasitic infections in the compromised host. Dekker, New York, pp 281–341

  • Duszynski DW, Couch L, Upton SJ (1999) Coccidia (Eimeriidae) of Sciuridae. In: Coccidae of the world (http://www.ksu.edu/parasitology/worldcoccidia/SCIURIDAE?)

  • Esch G, Bush AO, Ano JM (1990) Parasite communities: patterns and processes. Chapman and Hall, London

    Google Scholar 

  • Fayer R, Ungar BLP (1986) Cryptosporidium spp. and cryptosporidiosis. Microbiol Rev 50:458–483

    Google Scholar 

  • Fayer R, Morgan U, Upton SJ (2000) Epidemiology of Cryptosporidium: trasmission, detection and identification. Int J Parasitol 30:1305–1322

    CAS  PubMed  Google Scholar 

  • Fedynich AM, Pence DB, Bergan JF (1996) Helminth community structure and pattern in sympatric populations of black-bellied and fulvous whistling-ducks. Can J Zool 74:2219–2225

    Google Scholar 

  • Freeland WJ (1983) Parasites and the coexistence of animal host species. Am Nat 121:223–236

    Article  Google Scholar 

  • Fuller CA (1996) Population dynamics of two species of Eimeria (Apicomplexa: Eimeriidae) in deer mice ( Peromyscus maniculatus): biotic and abiotic factors. J Parasitol 82:220–225

    CAS  PubMed  Google Scholar 

  • Fuller CA, Duszynski DW (1997) Eimeria (Protozoa: Eimeriidae) from North American sciurids, Glaucomys sabrinus and Tamias townsendii: with a description of a new species. J Parasitol 81:187–194

    Google Scholar 

  • Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257-261

    CAS  PubMed  Google Scholar 

  • Gurnell J (1987) The natural history of squirrels. Helm, London

  • Gurnell J (1996) The effects of food availability and winter weather on the dynamics of a grey squirrel population in southern England. J Appl Ecol 33:325–338

    Google Scholar 

  • Healing TD, Nowell F (1985) Diseases of parasites of woodland rodent populations. Symp Zool Soc Lond 55:193–218

    Google Scholar 

  • Henriksen SA, Pohlenz JFL (1981) Staining of Cryptosporidia by modified Ziehl-Neelsen technique. Acta Vet Scand 22:594–596

    CAS  PubMed  Google Scholar 

  • Higgs S, Nowell F (2000) Population biology of Eimeria (Protozoa: Apicomplexa) in Apodemus sylvaticus: a capture/recapture study. Parasitology 120:355–363

    Article  PubMed  Google Scholar 

  • Hill TP, Duszynski DW (1986) Coccidia (Apicomplexa: Eimeriidae) from sciurid rodents ( Eutamias, Sciurus , Tamiasciurus spp.) from the Western United States and Northern Mexico with descriptions of two new species. J Parasitol 33:282–288

    CAS  Google Scholar 

  • Holmes JC, Price PW (1986) Communities of parasites. In: Anderson DJ, Kikkawa J (eds) Community ecology: pattern and processes. Blackwell, Oxford, pp 187–213

  • Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

  • Howard SC, Donelly CA, Chan M-S (2001) Methods for estimation of associations between multiple species parasite infections. Parasitology 122:233–251

    Article  CAS  PubMed  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.

  • Lurz PWW, Garson PJ, Wauters LA (2000) Effects of temporal and spatial variations in food supply on the space and habitat use of red squirrels ( Sciurus vulgaris L.). J Zool Lond 251:167–178

    Article  Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, London

  • May RM, Anderson RM (1979) Population biology of infection disease. Part II. Nature 280:455–461

    CAS  PubMed  Google Scholar 

  • Metha C, Patel N (1995) StatXact 3 for windows. Cytel Software, Cambridge, Mass.

  • Mijaki S, Tanikava T, Shikata J (1989) Prevalence of Cryptosporidium in Rattus rattus and R. norvegicus in Japan. Jpn J Parasitol 38:368–372

    Google Scholar 

  • Minchella DJ, Scott ME (1991) Parasitism: a cryptic determinant of animal community structure. Trees 6:250–254

    Google Scholar 

  • Mitchell-Jones AJ, Amori G, Bogdanowicz W, Kryštufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralík V, Zima J (1999) The atlas of European mammals. Academic Press, London

  • Noordeen F, Horadagoda NU, Faizal ACM, Rajapakse RPVJ, Razak MAA, Arulkanthan A (2002) Infectivity of Cryptosporidium parvum isolated from asymptomatic adult goats to mice and goat kids. Vet Parasitol 103:217–225

    Article  CAS  PubMed  Google Scholar 

  • Park T (1948) Esperimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium confusum Duval and Tribolium castaneum Herbst. Ecol Monogr 18:265–308

    Google Scholar 

  • Pellerdy L (1954) Contribution to the knowledge of coccidia of the common squirrel ( Sciurus vulgaris). Acta Vet Acad Sci Hung 4:475–480

    Google Scholar 

  • Pellerdy L (1974) Coccidia and coccidiosis. Akademiai Kiado, Budapest

  • Perryman LE (1990) Cryptosporidiosis in rodents. In: Dubey JP, Speer CA, Fayer R (eds) Cryptosporidiosis of man and animals. CRC, Boston, pp 125–131

  • Rushton SP, Lurz PWW, Gurnell J, Fuller R (2000) Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of the decline in the red squirrel in the UK? J Appl Ecol 37:997–1012

    Google Scholar 

  • SAS (1999) SAS/STAT user's guide, version 8. The GENMOD procedure SAS Institute, Cary, N.C., ch 29

  • Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74

    Google Scholar 

  • Seville RS, Stanton NL (1993) Eimerian guilds (Apicomplexa: Eimeriidae) in Richardson's ( Spermophilus richardsonii) and Wyoming ( Spermophilus elegans) ground squirrels. J Parasitol 79:973–975

    CAS  PubMed  Google Scholar 

  • Seville RS, Stanton NL, Gerow K (1996) Stable parasite guilds: coccidia in spermophiline rodents. Oikos 75:365–372

    Google Scholar 

  • Sousa WP (1994) Patterns and processes in communities of helminth parasites. Trees 9:52–57

    Google Scholar 

  • Stanton NL, Shults LM, Parker M, Seville RS (1992) Coccidian assemblages in the Wyoming ground squirrel, Spermophilus elegans elegans. J Parasitol 78:323–328

    CAS  PubMed  Google Scholar 

  • Stock TM, Holmes JC (1987) Host specificity and exchange of intestinal helminths among four species of grebes (Podicipedidae). Can J Zool 65:669–676

    Google Scholar 

  • Sturdee AP, Chalmers RM, Bull SA (1999) Detection of Cryptosporidium oocysts in wild mammals of mainland Britain. Vet Parasitol 80:273–280

    Article  CAS  PubMed  Google Scholar 

  • Sundberg J, Hill D, Ryan M (1982) Cryptosporidiosis in a gray squirrel. JAVMA 181:1420–1422

    CAS  Google Scholar 

  • Thomas DM, Seville RS, Stanton NL (1992) Oocyst production in multispecific eimerian infection in the Wyoming ground squirrel, Spermophilus elegans elegans. Acta Parasitol 37:111–114

    CAS  Google Scholar 

  • Thomas DM, Stanton NL, Seville RS (1995) An eimerian assemblage in Wyoming ground squirrel, ( Spermophilus elegans elegans): maintaining stability over winter. J Helminthol Soc Wash 62:1–5

    Google Scholar 

  • Toft CA (1986) Communities of species with parasitic life-styles. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 445–463

  • Tongereen OFR van (1995) Cluster analysis. In: Jongman RHG, Ter Braak CJF, van Tongeren OFR (eds) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge

  • Torres J, Gracenea M, Gómez MS, Arrizabalaga A, González-Moreno O (2000) The occurrence of Cryptosporidium parvum and C. muris in wild rodents and insectivores in Spain. Vet Parasitol 92:253–260

    Article  CAS  PubMed  Google Scholar 

  • Upton SJ, Current W (1985) The species of Cryptosporidium (Apicomplexa: Cryptosporidiidae) infecting mammals. J Parasitol 71:625–629

    CAS  PubMed  Google Scholar 

  • Verbeke G, Molenberghs G (1997) Linear mixed models. A SAS-oriented appoach. Springer, Berlin Heidelberg New York

  • Wauters LA, Dhondt AA (1989) Body weight, longevity and reproductive success in red squirrels ( Sciurus vulgaris). J Anim Ecol 58:637-651

    Google Scholar 

  • Wauters LA, Dhondt AA (1992) Spacing behaviour of red squirrels, Sciurus vulgaris: variation between habitats and the sexes. Anim Behav 43:297–311

    Google Scholar 

  • Wauters LA, Dhondt AA (1993) Immigration patterns and success in red squirrels. Behav Ecol Sociobiol 33:159–167

    Google Scholar 

  • Wauters LA, Dhondt AA (1995) Components of lifetime reproductive success of female Eurasian red squirrels. Oikos 72:402–410

    Google Scholar 

  • Wauters LA, Lens L (1995) Effects of food availability and density on red squirrel ( Sciurus vulgaris) reproduction. Ecology 76:2460-2469

    Google Scholar 

  • Wauters LA, Gurnell J, Preatoni D, Tosi G (2001) Effects of spatial variation in food availability on spacing behaviour and demography of Eurasian red squirrels. Ecography 24:525–538

    Google Scholar 

  • Wilber PG, Hanelt B, Van Horne B, Duszynski DW (1994) Two new species and temporal change in the prevalence of Eimerians in a free-living population of Townsend's ground squirrel ( Spermophilus townsendii) in Idaho. J Parasitol 80:251–259

    CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Miriam Gioia, Massimiliano Zaninetti, Ambrogio Molinari, Cinzia Long, Chiara Falco, Alessandro Dellanoce, for assistance with the field work, Mariarosa Formicola and Maura Corniati for assistance in the laboratory analyses. This study was financed by a grant from the Gran Paradiso National Park, Italy (DGE 25–2000) to L. A. W., S. B. and Faunaviva, by grant no. 6997–01 from the Committee for Research and Exploration of the National Geographic Society, Washington, D.C., to L. A. W., and by a grant from MURST 60% to G. C. T.

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Correspondence to Sandro Bertolino.

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Bertolino, S., Wauters, L.A., De Bruyn, L. et al. Prevalence of coccidia parasites (Protozoa) in red squirrels ( Sciurus vulgaris): effects of host phenotype and environmental factors. Oecologia 137, 286–295 (2003). https://doi.org/10.1007/s00442-003-1345-x

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