Experimental and Applied Acarology

, Volume 54, Issue 2, pp 151–164 | Cite as

Comparative population dynamics of a generalist (Ixodes ricinus) and specialist tick (I. hexagonus) species from European hedgehogs

  • M. Pfäffle
  • T. Petney
  • J. Skuballa
  • H. Taraschewski


Although the population dynamics of the tick Ixodes ricinus are relatively well studied, those of other Western European tick species are largely unknown. Moreover, there is very little information related to the interactions between I. ricinus and other ticks. Such knowledge, however, is of special interest in respect to the epidemiology of tick-borne pathogens such as Borrelia spp. We compared the dynamics of the generalist I. ricinus with the nest-dwelling hedgehog specialist, I. hexagonus. Both species were collected from hedgehogs from a naturally infested experimental population between 2006 and 2008. Ticks were collected once a month from March to October from each hedgehog counted and the life history stage and species determined. All hedgehogs harboured both tick species. Nymphs, females and males of I. ricinus showed clear bimodal seasonal distributions with peaks in spring and autumn, while larvae peaked only in summer. The density of I. hexagonus life stages was low during the whole investigation period and seasonal fluctuations of population density were much weaker compared to I. ricinus. Nymphs and larvae showed comparatively little change in population size and no consistent period of peak density. Females showed a single peak in summer and males were found only occasionally on hedgehogs. We suggest density-dependent mechanisms regulating the population density of the specialist I. hexagonus but not of the generalist I. ricinus.


European hedgehog Ixodes ricinus Ixodes hexagonus Population dynamics Generalist Specialist 



The study was funded by grants from the LBBW-Bank Baden Württemberg, the Krieger Foundation and the Landesgraduiertenförderung Baden-Württemberg. The authors would like to thank Mrs. Elisabeth Swoboda and Mrs. Sigrun Goroncy for providing us with the hedgehogs from our experimental hedgehog population and Heiko Fischer and Miriam Maurer for collecting and determining the ticks in 2006 and 2007. Special thanks to Prof. Stephen Wikel for giving advices concerning acquired resistance and differences in the sialome of tick species.


  1. Andrews RH, Petney TN, Bull CM (1982) Niche changes between parasite populations: an example from ticks on reptiles. Oecologia 55:70–80. doi: 10.1007/BF00386721 CrossRefGoogle Scholar
  2. Arthur DR (1963) British ticks. Butterworths, LondonGoogle Scholar
  3. Aubert MFA (1975) Contribution a l’ètude du parasitisme du renard (Vulpes vulpes) par les Ixodidae (Acarina) dans le nord-est de la France. Interprétation de la dynamique saisonnière des parasites en relation avec la biologie de l’hôte. Acarologia 17:452–479Google Scholar
  4. Bergers PJM, Nieuwenhuizen W (1999) Viability of hedgehog populations in Central Netherlands. Lutra 42:65–75Google Scholar
  5. Bull CM, Burzacott D, Sharrad RD (1989) No competition for resources between two tick species at their parapatric boundary. Oecologia 79:558–562. doi: 10.1007/BF00378675 CrossRefGoogle Scholar
  6. Chilton NB, Bull CM, Andres RH (1992) Niche segregation in reptile ticks: attachment sites and reproductive success of females. Oecologia 90:255–259. doi: 10.1007/BF00317183 Google Scholar
  7. Chmelar J, Anderson JM, Mu J, Jochim RC, Valenzuela JG, Kopecky J (2008) Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 9:233. doi: 10.1186/1471-2164-9-233 PubMedCrossRefGoogle Scholar
  8. Christian A (2002) Zeckenbefall am Baummarder in Mecklenburg. Abh Ber Naturkundemus Görlitz 74:15–20Google Scholar
  9. Dizij A, Kurtenbach K (1995) Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to Ixodes ricinus L., the main European vector of Borrelia burgdorferi. Parasit Immunol 17:177–183. doi: 10.1111/j.1365-3024.1995.tb00887.x CrossRefGoogle Scholar
  10. Dobbelaere DAE, Shapiro SZ, Buscher G (1987) Acquired resistance to Rhipicephalus appendiculatus (Acari: Ixodidae): identification of an antigen eliciting resistance in rabbits. J Med Entomol 24:147–154PubMedGoogle Scholar
  11. Estrada-Peña A (2001) Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in Northern Spain. J Med Entomol 38:361–370. doi: 10.1603/0022-2585-38.3.361 PubMedCrossRefGoogle Scholar
  12. Estrada-Peña A (2002) Understanding the relationships between landscape connectivity and abundance of Ixodes ricinus ticks. Exp Appl Acarol 28:239–248. doi: 10.1023/A:1025362903620 PubMedCrossRefGoogle Scholar
  13. Fingerle V, Schulte-Spechtel UC, Ruzic-Sabljic E, Leonhard S, Hofmann H, Weber K, Pfister K, Strle F, Wilske B (2008) Epidemiological aspects and molecular characterization of Borrelia burgdorferi s.l. from southern Germany with special respect to the new species Borrelia spielmanii sp. nov. Int J Med Microbiol 298:279–290. doi: 10.1016/j.ijmm.2007.05.002
  14. Fischer H (2007) Der Europäische Igel (Erinaceus europaeus) als Wirt der Schildzecken Ixodes (Ixodes) ricinus und Ixodes (Pholeoixodes) hexagonus, Thesis, University of KarlsruheGoogle Scholar
  15. Földvári G, Márialigeti SolymosiN, Lukács Z, Majoros G, Kósa JP, Farkas R (2007) Hard ticks infesting dogs in Hungary and their infection with Babesia and Borrelia species. Parasitol Res 101:S25–S34. doi: 10.1007/s00436-007-0608-6 CrossRefGoogle Scholar
  16. Gern L (2005) The biology of Ixodes ricinus. Ther Umsch 62:707–712PubMedCrossRefGoogle Scholar
  17. Gern L, Humair P-F (2002) Ecology of Borrelia burgdorferi sensu lato in Europe. In: Kahl O, Gray JS, Lane RS, Stanek G (eds) Lyme borreliosis: biology, epidemiology and control. CABI Publishing, Oxford, pp 149–174CrossRefGoogle Scholar
  18. Gern L, Toutoungi LN, Chang MH, Aeschlimann A (1991) Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory. Med Vet Entomol 5:431–435. doi: 10.1111/j.1365-2915.1991.tb00571.x PubMedCrossRefGoogle Scholar
  19. Gern L, Rouvinez E, Toutoungi LN, Godfroid E (1997) Transmission cycles of Borrelia burgdorferi sensu lato involving Ixodes ricinus and/or I. hexagonus ticks in the European hedgehog, Erinacues europaeus, in suburban and urban areas in Switzerland. Fol Parasitol 44:309–314Google Scholar
  20. Gray JS (1985) A carbone dioxide trap for prolonged sampling of Ixodes ricinus L. populations. Exp Appl Acarol 1:35–44. doi: 10.1007/BF01262198 PubMedCrossRefGoogle Scholar
  21. Gray JS (1998) The ecology of ticks transmitting Lyme borreliosis. Exp Appl Acarol 22:249–258. doi: 10.1023/A:1006070416135 CrossRefGoogle Scholar
  22. Gray JS, Kahl O, Janetzki-Mittman C, Stein J, Guy E (1994) Acquisition of Borrelia burgdorferi by Ixodes ricinus ticks fed on the European hedgehog, Erinaceus europaeus L. Exp Appl Acarol 18:485–491. doi: 10.1007/BF00051470 PubMedCrossRefGoogle Scholar
  23. Hesse GH, Völker K (1983) Ein Beitrag zur deutschen Haemaphysalis-Fauna (Ixodoidea, Ixodidae): Haemaphysalis punctata in Nordrhein-Westfalen. Parasitol Res 69:393. doi: 10.1007/BF00927881 Google Scholar
  24. Hoeck HN (1987) Hedgehog mortality during hibernation. J Zool 213:755–757. doi: 10.1111/j.1469-7998.1987.tb03743.x CrossRefGoogle Scholar
  25. Jouda F, Perret J-L, Gern L (2004a) Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. J Med Entomol 41:162–169PubMedCrossRefGoogle Scholar
  26. Jouda F, Perret J-L, Gern L (2004b) Density of questing Ixodes ricinus nymphs and adults infected by Borrelia burgdorferi sensu lato in Switzerland: spatio-temporal pattern at a regional scale. Vector Borne Zoonotic Dis 4:23–32. doi: 10.1089/153036604773082960 PubMedCrossRefGoogle Scholar
  27. Korenberg EI (2000) Seasonal population dynamics of Ixodes ticks and tick-borne encephalitis virus. Exp Appl Acarol 24:665–681. doi: 10.1023/A:1010798518261 PubMedCrossRefGoogle Scholar
  28. L’Hostis M, Bureaud A, Gorenflot A (1996) Female Ixodes ricinus (Acari: Ixodidae) in cattle of western France: infestation level and seasonality. Vet Res 27:589–597PubMedGoogle Scholar
  29. Leonhard S (2005) Untersuchungen zur Häufigkeit von Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum und Babesia spp in Ixodes ricinus aus Bayern und Baden-Württemberg. Dissertation, Ludwig-Maximilians-University MunichGoogle Scholar
  30. Liebisch A, Walter G (1986) Untersuchungen von Zecken bei Haus- und Wildtieren in Deutschland: Zum Vorkommen und zur Biologie der Igelzecke (Ixodes hexagonus) und der Fuchszecke (Ixodes canisuga). Deut Tierarztl Woch 93:447–450Google Scholar
  31. MacLeod J (1936) Ixodes ricinus in relation to its physical environment. Parasitology 28:295–319. doi: 10.1017/S0031182000022502 CrossRefGoogle Scholar
  32. Maurer M (2008) Der Einfluss von Schildzecken (Ixodes ricinus und Ixodes hexagonus) auf die Fitness des Europäischen Igels Erinaceus europaeus, Diploma thesis, University of KarlsruheGoogle Scholar
  33. Nilsson A (1988) Seasonal occurrence of Ixodes ricinus (Acari) in vegetation and on small mammals in southern Sweden. Holarctic Ecol 11:161–165. doi: 10.1111/j.1600-0587.1988.tb00795.x Google Scholar
  34. Pfäffle M (2010) Influence of parasites on fitness parameters of the European hedgehog, PhD thesis, Karlsruhe Institute of TechnologyGoogle Scholar
  35. Pfäffle M, Petney T, Elgas M, Skuballa J, Taraschewski H (2009) Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). Parasitology 136:443–452. doi: 10.1017/S0031182009005514 PubMedCrossRefGoogle Scholar
  36. Pichot J, Gilot B, Almire N, Polette K, Degeilh B (1997) Ixodes populations (Ixodes ricinus Linné, 1758, Ixodes hexagonus leach, 1815) in the city of Lyon (France) and its outskirts: preliminary results. Parasite 4:167–171Google Scholar
  37. Randolph SE (1994) Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti. Parasitology 108:413–419. doi: 10.1017/S0031182009991065 PubMedCrossRefGoogle Scholar
  38. Randolph SE (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129:37–65. doi: 10.1017/S0031182004004925 CrossRefGoogle Scholar
  39. Randolph SE, Green RM, Hoodless AN, Peacey MF (2002) An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 32:979–989. doi: 10.1016/S0020-7519(02)00030-9
  40. Reeve N (1994) Hedgehogs. Cambridge University Press, CambridgeGoogle Scholar
  41. Rosa R, Pugliese A, Norman R, Hudson PJ (2003) Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. J Theor Biol 224:359–376. doi: 10.1016/S0022-5193(03)00173-5 Google Scholar
  42. Shapiro SZ, Voigt WP, Ellis JA (1989) Acquired resistance to ixodid ticks induced by tick cement antigen. Exp Appl Acarol 7:33–41. doi: 10.1007/BF01200451 PubMedCrossRefGoogle Scholar
  43. Skuballa J, Oehme R, Hartelt K, Petney T, Bücher T, Kimmig P, Taraschewski H (2007). European hedgehogs as hosts for Borrelia spp., Germany. Emerg Infect Dis 13:952–953. doi: 10.3201/eid1306.070224 Google Scholar
  44. Skuballa J, Petney TN, Pfäffle M, Taraschewski H (2010) Molecular detection of Anaplasma phagocytophilum in the European hedgehog (Erinaceus europaeus) and its ticks. Vector Borne Zoon Dis. doi: 10.1007/s00436-009-1681-9
  45. Süss J, Schrader C (2004) Durch Zecken übertragene humanpathogene und bisher als apathogen geltende Mikroorganismen in Europa. Teil 1: Zecken und Viren. Bundesgesundheitsbl—Gesundheitsforsch—Gesundheitsschutz 47:392–404. doi: 10.1007/s00103-003-0766-3
  46. Süss J, Fingerle V, Hunfeld KP, Schrader C, Wilske B (2004) Durch Zecken übertragene humanpathogene und bisher als apathogen geltende Mikroorganismen in Europa. Teil 2: Bakterien, Parasiten und Mischinfektionen. Bundesgesundheitsbl—Gesundheitsforsch—Gesundheitsschutz 47:470–486. doi: 10.1007/s00103-004-0837-0
  47. Szell Z, Sreter-Lancz Z, Marialigeti K, Sreter T (2006) Temporal distribution of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna in Hungary. Vet Parasitol 141:377–379. doi: 10.1016/j.vetpar.2006.06.008 PubMedCrossRefGoogle Scholar
  48. Tälleklint L, Jaenson GT (1997) Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden. Exp Appl Acarol 21:755–771. doi: 10.1023/A:1018473122070 PubMedCrossRefGoogle Scholar
  49. Taraschewski H (2006) Host and parasites as aliens. J Helminthol 80:99–192. doi: 10.1079/JOH2006364 PubMedCrossRefGoogle Scholar
  50. Tomaschewski LH (2009) Der Einfluss von Ektoparasiten auf die Nestwahl von Igeln (Erinaceus europaeus), Thesis, Karlsruhe Institute of TechnologyGoogle Scholar
  51. Tonnesen MH, Penzhorn BL, Bryson NR, Stoltsz WH, Masibigiri T (2004) Displacement of Boophilus decoloratus by Boophilus microplus in the Soutpansberg region, Limpopo Province, South Africa. Exp Appl Acarol 32:199–208. doi: 10.1023/B:APPA.0000021789.44411.b5 PubMedCrossRefGoogle Scholar
  52. Toutoungi NL, Gern L (1993) Ability of transovarially and subsequent transstadially infected Ixodes hexagonus ticks to maintain and transmit Borrelia burgdorferi in the laboratory. Exp Appl Acarol 17:581–586. doi: 10.1007/BF00053487 PubMedCrossRefGoogle Scholar
  53. Tripet F, Richner H (1999) Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology 80:1267–1277Google Scholar
  54. Tyre AJ, Bull CM, Tenhumberg B, Chilton N (2003) Indirect evidence of density-dependent population regulation in Aponomma hydrosauri (Acari: Ixodidae), an ectoparasite of reptiles. Aust Ecol 28:196–203. doi: 10.1046/j.1442-9993.2003.01270.x CrossRefGoogle Scholar
  55. Walter G, Kock D, Liebisch A (1986) Beitrag zur Zecken-Fauna der Bundesrepublik Deutschland (Arachnida: Acarina: Ixodidae). Senckenb Biol 67:199–206Google Scholar
  56. Wikel SK (1996) Host immunity to ticks. Ann Rev Entomol 41:1–22CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • M. Pfäffle
    • 1
  • T. Petney
    • 1
  • J. Skuballa
    • 1
  • H. Taraschewski
    • 1
  1. 1.Department of Ecology and ParasitologyKIT, Karlsruhe Institute of Technology, Zoological InstituteKarlsruheGermany

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