Skip to main content
Log in

The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The palaeacanthocephalan Plagiorhynchus cylindraceus is a common intestinal parasite of passerine birds, which can also occur parenterally or in the intestinal tract of mammals, often as an invading species in many countries worldwide. In this survey, introduced hedgehogs (Erinaceus europaeus, n = 183) killed in New Zealand during a biocontrol campaign and conspecifics (n = 174) that had died in hedgehog rehabilitation centers in Germany and Britain were examined for this parasite. In New Zealand, P. cylindraceus is recorded for the first time here, in the vicinity of Auckland. In Europe, prevalences ranged from 4.2% up to 47.6%, while in New Zealand, only 1.6% (Auckland 7.9%). Most of the worms occurred inside the peritoneal cavity where they had partly degenerated. Since hedgehogs are seldom preyed upon in continental Europe but often become traffic victims, we hypothesize that the worms inside them, whether extra- or intraperitoneally, contribute to the abundance and persistence of the parasite by being ingested by scavenging birds. Accordingly, we consider P. cylindraceus as a “modern parasite” taking advantage of two aspects of global change: anthropogenic promoted transmission (road kills) and the transcontinental spread of infected intermediate and/or final hosts caused by humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Amin O (1985) Classification. In: Nickol BB, Crompton DWT (eds) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 27–72

    Google Scholar 

  • Amin OM, Canaris AG, Kinsella JM (1999) A taxonomic reconsideration of the genus Plagiorhynchus s. lat. (Acanthocephala: Plagiorhynchidae), with descriptions of South African Plagiorhynchus (Prosthorynchus) cylindraceus from shorebirds and P. (P.) malayensis, and a key to the species of the subgenus Prosthorynchus. J Helm Soc Wash 66:123–132

    Google Scholar 

  • Bezzel E, Obst J, Wickl KH (1976) Zur Ernährung und Nahrungswahl des Uhus (Bubo bubo). J Ornithol 117:210–238. doi:10.1007/BF01643587

    Article  Google Scholar 

  • Coady NR, Nickol BB (2000) Assessment of parenteral Plagiorhynchus cylindraceus (Acanthocephala) infections in shrews. Comp Parasitol 67:32–39

    Google Scholar 

  • Connors VA, Nickol BB (1991) Effects of Plagiorhynchus cylindraceus (Acanthocephala) on the energy metabolism of adult starlings, Sturnus vulgaris. Parasitology 103:395–402

    Article  PubMed  Google Scholar 

  • Dimelow EJ (1963) Observations on the feeding hedgehog (Erinaceus europaeus L.). Proc Zool Soc Lond 141:291–309

    Google Scholar 

  • Dimitrova ZM (2009) Occurrence of cystacanths of Plagiorhynchus cylindraceus (Acanthocephala) in the terrestrial isopods Trachelipus squamuliger and Armadillidium vulgare (Oniscidea) in Bulgaria. Acta Parasitol 54:53–56. doi:10.2478/s11686-009-0003-9

    Article  Google Scholar 

  • Dimitrova ZM, Georgiev BB, Genov T (1999) New data on acanthocephalans of the genus Plagiorhynchus Lühe, 1911 (Palaeacanthocephala, Polymorphida, Plagiorhynchidae) from birds in Bulgaria. Helminthologia 36:261–267

    Google Scholar 

  • Edelenyi B, Szabo I (1963) Parasitische Würmer in einheimischen Säugetieren. Ann Hist-Nat Mus Natl Hung 55:275–283

    Google Scholar 

  • Ferrer D, Molina R, Castellà J, Kinsella JM (2004) Parasitic helminths in the digestive tract of six species of owls (Strigiformes) in Spain. Vet J 167:181–185. doi:10.1016/S1090-0233(03)00103-5

    Article  PubMed  Google Scholar 

  • Golvan YJ (1994) Nomenclature of the Acanthocephala. Res Rev Parasitol 54:135–205

    Google Scholar 

  • Holsbeek L, Rodts J, Muyldermans S (1999) Hedgehog and other animal traffic victims in Belgium: results of a countrywide survey. Lutra 42:111–119

    Google Scholar 

  • Huijser MP, Bergers P (2000) The effect of roads and traffic on hedgehog (Erinaceus europaeus) populations. Biol Conserv 95:111–116. doi:10.1016/S0006-3207(00)00006-9

    Article  Google Scholar 

  • Jay M, Morad M, Bell A (2003) Biosecurity: a policy dilemma for New Zealand. Land Use Policy 20:121–129. doi:10.1016/S0264-8377(03)00008-5

    Article  Google Scholar 

  • Jones M (1928) An acanthocephalid, Plagiorhynchus formosus, from the chicken and robin. J Agric Res 36:773–775

    Google Scholar 

  • Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge

    Google Scholar 

  • Keymer IF, Gibson EA, Reynolds DJ (1991) Zoonoses and other findings in hedgehogs (Erinaceus europaeus): a survey of mortality and review of the literature. Vet Rec 128:245–249

    CAS  PubMed  Google Scholar 

  • Levri EP, Coppola BP (2004) First report of the acanthocephalan Plagiorhynchus cylindraceus in the terrestrial isopod Porcellio scaber. Comp Parasitol 71:90–91. doi:10.1654/4085

    Article  Google Scholar 

  • Martinez JA, Zuberogoitia I (2001) The response of the Eagle Owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease. J Ornithol 142:204–211. doi:10.1007/BF01651788

    Article  Google Scholar 

  • Moore J (1983) Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64:1000–1015

    Article  Google Scholar 

  • Moore J, Bell DH (1983) Pathology (?) of Plagiorhynchus cylindraceus in the starling, Sturnus vulgaris. J Parasitol 69:387–390

    Article  CAS  PubMed  Google Scholar 

  • Nickol BB (2003) Is postcyclic transmission under estimated as an epizootiological factor for acanthocephalans? Helminthologia 40:93–95

    Google Scholar 

  • Nickol BB, Dappen GE (1982) Armadillidium vulgare (Isopoda) as an intermediate host of Plagiorhynchus cylindraceus (Acanthocephala) and isopod response to infection. J Parasitol 68:570–575

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Reeve N (1994) Hedgehogs. T & AD Poyser (Natural History), London

    Google Scholar 

  • Richards DT, Harris S, Lewis JW (1995) Epidemiological studies on intestinal helminth parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Vet Parasitol 59:39–51. doi:10.1016/0304-4017(94)00736-V

    Article  CAS  PubMed  Google Scholar 

  • Schicht-Tinbergen M (1989) Der Igel. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Schmidt GD, Kuntz RE (1966) New and little-known plagiorhynchid Acanthocephala from Taiwan and the Pescadores Islands. J Parasitol 52:520–527

    Article  CAS  PubMed  Google Scholar 

  • Schmidt GD, Olsen O (1964) Life cycle and development of Prosthorhynchus formosus (van Cleave, 1918) Travassos, 1926, an acanthocephalan parasite of birds. J Parasitol 50:721–730

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Smales LR (1988) Plagiorhynchus (Prosthorhynchus) cylindraceus (Goeze, 1782) Schmidt and Kuntz, 1966, from the Australian bandicoots Perameles gunnii Gray, 1838, and Isodoon obesulus (Shaw 1797). J Parasitol 74:1062–1064

    Article  CAS  PubMed  Google Scholar 

  • Smales LR (2002) Plagiorhynchidae Meyer, 1931 (Acanthocephala) from Australasian birds and mammals, with descriptions of Plagiorhynchus (Plagiorhynchus) menurae (Johnston, 1912) and P. (P.) allisonae n. sp. Syst Parasitol 51:207–216. doi:10.1023/A:1014590530850

    Article  PubMed  Google Scholar 

  • Smales LR (2003) An annotated checklist of the Australian Acanthocephala from mammalian and bird hosts. Rec S Aust Mus 36:59–82

    Google Scholar 

  • Stevenson MA, Benard H, Bolger P, Morris RS (2005) Spatial epidemiology of the Asian honey bee mite (Varroa destructor) in the North Island of New Zealand. Prev Vet Med 71:241–252. doi:10.1016/j.prevetmed.2005.07.007

    Article  CAS  PubMed  Google Scholar 

  • Taraschewski H (2000) Host-parasite interactions in Acanthocephala: a morphological approach. Adv Parasitol 46:1–179

    Article  CAS  PubMed  Google Scholar 

  • Taraschewski H (2005) Acanthocephala (thorny or spiny-headed worms). In: Rhode K (ed) Marine parasitology. CSIRO Publishing, Collingwood Victoria, pp 116–121

    Google Scholar 

  • Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–129. doi:10.1079/JOH2006364

    Article  CAS  PubMed  Google Scholar 

  • Ward DF, Harris RJ, Stanley MC (2005) Human-mediated range expansion of Argentine ants Linepithema humile (Hymenoptera: Formicidae) in New Zealand. Sociobiology 45:1–7

    Google Scholar 

  • Zhang ZQ (2000) Notes on Varroa destructor (Acari: Varroidae) parasitic on honeybees in New Zealand. Syst Appl Acarol Spec Publ 5:9–15

    CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank all people running hedgehog care centers in Germany and the UK, especially Heiko and Sigrun Goroncy (“Komittee für Igelschutz Hamburg”), Elisabeth Swoboda (“Igelkrankenhaus Stocksberg”), Manfred Kolb (“NaBu Berlin”), Dora Lambert (“Igelkreis Berlin”), Ulrike Pachzelt (“Igelinsel Mühlheim”), Dru Burdon (“Jersey Hedgehog Preservation Group”), Jill Carey (“Wildlife Rescue & Care Centre”), Iris Davidson, Dr. Wieland Beck (“Tierrettung München”), and all the others for their help in obtaining hedgehogs for dissection. Dr. Thomas Bücher provided support in dissecting hedgehogs in Karlsruhe.

We thank Mark Mitchell (Biosecurity, Auckland Regional Council) and Daniel Tompkins for sampling hedgehogs in New Zealand, as well as, Chris Jones and Dave Leathwick who provided two of us (JS, MP) with the opportunity to work at their facilities. Funding was provided by grants from the Landesgraduiertenförderung BW, the DAAD (German Academic Exchange Service), Krieger Foundation, and LBBW Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Horst Taraschewski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Skuballa, J., Taraschewski, H., Petney, T.N. et al. The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand. Parasitol Res 106, 431–437 (2010). https://doi.org/10.1007/s00436-009-1681-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-009-1681-9

Keywords

Navigation