Oecologia

, Volume 137, Issue 2, pp 286–295 | Cite as

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

  • Sandro Bertolino
  • Luc A. Wauters
  • Luc De Bruyn
  • Giorgio Canestri-Trotti
Community Ecology

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.

Keywords

Alpine forests  Cryptosporidium parvum  Eimeria Parasite communities Host density 

References

  1. Anderson RM, May RM (1979) Population biology of infection disease. Part I. Nature 280:361–367PubMedGoogle Scholar
  2. 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 21Google Scholar
  3. Bull SA, Chalmers RM, Sturdee AP, Healing TD (1998) A survey of Cryptosporidium species in Skomer bank voles ( Clethrionomys glareolus skomerensis). J Zool 244:119–122CrossRefGoogle Scholar
  4. Burnham KP, Anderson DR (1998) Model selection and inference. A practical information-theoretic approach. Springer, New YorkGoogle Scholar
  5. Bush AO, Lafferty KD, Lotz JM, Shostaki AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedGoogle Scholar
  6. Casemore D, Wright SE, Coop RL (1997) Crytosporidiosis—human and animal epidemiology. In: Fayer R (ed) Cryptosporidium and Crytosporidiosis. CRC, Boca Raton, Fla., pp 65–92Google Scholar
  7. 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 63–66Google Scholar
  8. Current WL (1989) Cryptosporidium spp. In: Walzer PD, Genta RM (eds) Parasitic infections in the compromised host. Dekker, New York, pp 281–341Google Scholar
  9. Duszynski DW, Couch L, Upton SJ (1999) Coccidia (Eimeriidae) of Sciuridae. In: Coccidae of the world (http://www.ksu.edu/parasitology/worldcoccidia/SCIURIDAE?)
  10. Esch G, Bush AO, Ano JM (1990) Parasite communities: patterns and processes. Chapman and Hall, LondonGoogle Scholar
  11. Fayer R, Ungar BLP (1986) Cryptosporidium spp. and cryptosporidiosis. Microbiol Rev 50:458–483Google Scholar
  12. Fayer R, Morgan U, Upton SJ (2000) Epidemiology of Cryptosporidium: trasmission, detection and identification. Int J Parasitol 30:1305–1322PubMedGoogle Scholar
  13. 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 74:2219–2225Google Scholar
  14. Freeland WJ (1983) Parasites and the coexistence of animal host species. Am Nat 121:223–236CrossRefGoogle Scholar
  15. Fuller CA (1996) Population dynamics of two species of Eimeria (Apicomplexa: Eimeriidae) in deer mice ( Peromyscus maniculatus): biotic and abiotic factors. J Parasitol 82:220–225PubMedGoogle Scholar
  16. 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 81:187–194Google Scholar
  17. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257-261PubMedGoogle Scholar
  18. Gurnell J (1987) The natural history of squirrels. Helm, LondonGoogle Scholar
  19. 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 33:325–338Google Scholar
  20. Healing TD, Nowell F (1985) Diseases of parasites of woodland rodent populations. Symp Zool Soc Lond 55:193–218Google Scholar
  21. Henriksen SA, Pohlenz JFL (1981) Staining of Cryptosporidia by modified Ziehl-Neelsen technique. Acta Vet Scand 22:594–596PubMedGoogle Scholar
  22. Higgs S, Nowell F (2000) Population biology of Eimeria (Protozoa: Apicomplexa) in Apodemus sylvaticus: a capture/recapture study. Parasitology 120:355–363CrossRefPubMedGoogle Scholar
  23. 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 33:282–288Google Scholar
  24. Holmes JC, Price PW (1986) Communities of parasites. In: Anderson DJ, Kikkawa J (eds) Community ecology: pattern and processes. Blackwell, Oxford, pp 187–213Google Scholar
  25. Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New YorkGoogle Scholar
  26. Howard SC, Donelly CA, Chan M-S (2001) Methods for estimation of associations between multiple species parasite infections. Parasitology 122:233–251CrossRefPubMedGoogle Scholar
  27. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.Google Scholar
  28. 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 251:167–178CrossRefGoogle Scholar
  29. Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, LondonGoogle Scholar
  30. May RM, Anderson RM (1979) Population biology of infection disease. Part II. Nature 280:455–461PubMedGoogle Scholar
  31. Metha C, Patel N (1995) StatXact 3 for windows. Cytel Software, Cambridge, Mass.Google Scholar
  32. Mijaki S, Tanikava T, Shikata J (1989) Prevalence of Cryptosporidium in Rattus rattus and R. norvegicus in Japan. Jpn J Parasitol 38:368–372Google Scholar
  33. Minchella DJ, Scott ME (1991) Parasitism: a cryptic determinant of animal community structure. Trees 6:250–254Google Scholar
  34. 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, LondonGoogle Scholar
  35. 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 103:217–225CrossRefPubMedGoogle Scholar
  36. 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 18:265–308Google Scholar
  37. Pellerdy L (1954) Contribution to the knowledge of coccidia of the common squirrel ( Sciurus vulgaris). Acta Vet Acad Sci Hung 4:475–480Google Scholar
  38. Pellerdy L (1974) Coccidia and coccidiosis. Akademiai Kiado, BudapestGoogle Scholar
  39. Perryman LE (1990) Cryptosporidiosis in rodents. In: Dubey JP, Speer CA, Fayer R (eds) Cryptosporidiosis of man and animals. CRC, Boston, pp 125–131Google Scholar
  40. 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 37:997–1012Google Scholar
  41. SAS (1999) SAS/STAT user's guide, version 8. The GENMOD procedure SAS Institute, Cary, N.C., ch 29Google Scholar
  42. Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74Google Scholar
  43. Seville RS, Stanton NL (1993) Eimerian guilds (Apicomplexa: Eimeriidae) in Richardson's ( Spermophilus richardsonii) and Wyoming ( Spermophilus elegans) ground squirrels. J Parasitol 79:973–975PubMedGoogle Scholar
  44. Seville RS, Stanton NL, Gerow K (1996) Stable parasite guilds: coccidia in spermophiline rodents. Oikos 75:365–372Google Scholar
  45. Sousa WP (1994) Patterns and processes in communities of helminth parasites. Trees 9:52–57Google Scholar
  46. Stanton NL, Shults LM, Parker M, Seville RS (1992) Coccidian assemblages in the Wyoming ground squirrel, Spermophilus elegans elegans. J Parasitol 78:323–328PubMedGoogle Scholar
  47. Stock TM, Holmes JC (1987) Host specificity and exchange of intestinal helminths among four species of grebes (Podicipedidae). Can J Zool 65:669–676Google Scholar
  48. Sturdee AP, Chalmers RM, Bull SA (1999) Detection of Cryptosporidium oocysts in wild mammals of mainland Britain. Vet Parasitol 80:273–280CrossRefPubMedGoogle Scholar
  49. Sundberg J, Hill D, Ryan M (1982) Cryptosporidiosis in a gray squirrel. JAVMA 181:1420–1422Google Scholar
  50. Thomas DM, Seville RS, Stanton NL (1992) Oocyst production in multispecific eimerian infection in the Wyoming ground squirrel, Spermophilus elegans elegans. Acta Parasitol 37:111–114Google Scholar
  51. 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 62:1–5Google Scholar
  52. Toft CA (1986) Communities of species with parasitic life-styles. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 445–463Google Scholar
  53. 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, CambridgeGoogle Scholar
  54. 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 92:253–260CrossRefPubMedGoogle Scholar
  55. Upton SJ, Current W (1985) The species of Cryptosporidium (Apicomplexa: Cryptosporidiidae) infecting mammals. J Parasitol 71:625–629PubMedGoogle Scholar
  56. Verbeke G, Molenberghs G (1997) Linear mixed models. A SAS-oriented appoach. Springer, Berlin Heidelberg New YorkGoogle Scholar
  57. Wauters LA, Dhondt AA (1989) Body weight, longevity and reproductive success in red squirrels ( Sciurus vulgaris). J Anim Ecol 58:637-651Google Scholar
  58. Wauters LA, Dhondt AA (1992) Spacing behaviour of red squirrels, Sciurus vulgaris: variation between habitats and the sexes. Anim Behav 43:297–311Google Scholar
  59. Wauters LA, Dhondt AA (1993) Immigration patterns and success in red squirrels. Behav Ecol Sociobiol 33:159–167Google Scholar
  60. Wauters LA, Dhondt AA (1995) Components of lifetime reproductive success of female Eurasian red squirrels. Oikos 72:402–410Google Scholar
  61. Wauters LA, Lens L (1995) Effects of food availability and density on red squirrel ( Sciurus vulgaris) reproduction. Ecology 76:2460-2469Google Scholar
  62. 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 24:525–538Google Scholar
  63. 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 80:251–259PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Sandro Bertolino
    • 1
  • Luc A. Wauters
    • 2
  • Luc De Bruyn
    • 3
    • 4
  • Giorgio Canestri-Trotti
    • 5
  1. 1.Laboratory of Entomology and Zoology, DIVAPRAUniversity of TurinGrugliasco (TO)Italy
  2. 2.Department of Structural and Functional BiologyUniversity of InsubriaVarese (VA)Italy
  3. 3.Department of BiologyUniversity of AntwerpAntwerpBelgium
  4. 4.Institute of Nature ConservationBrusselsBelgium
  5. 5.Animal Biology DepartmentTorinoItaly

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