Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-20T11:59:40.989Z Has data issue: false hasContentIssue false
  • English
  • Français

Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus)

Published online by Cambridge University Press:  16 February 2009

M. PFÄFFLE ,
T. PETNEY ,
M. ELGAS ,
J. SKUBALLA  and
H. TARASCHEWSKI
M. PFÄFFLE*
Affiliation:
University of Karlsruhe, Zoological Institute I, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
T. PETNEY
Affiliation:
University of Karlsruhe, Zoological Institute I, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
M. ELGAS
Affiliation:
ZLMT, Institute for Medical Laboratory Diagnostics, Städt. Klinikum Karlsruhe, Moltkestrasse 90, 76133 Karlsruhe, Germany
J. SKUBALLA
Affiliation:
University of Karlsruhe, Zoological Institute I, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
H. TARASCHEWSKI
Affiliation:
University of Karlsruhe, Zoological Institute I, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany
*
*Corresponding author: University of Karlsruhe, Zoological Institute I, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131 Karlsruhe, Germany. Tel: +49 721 6087657. Fax: +49 721 6087655. E-mail: miripfaeffle@web.de
Get access Rights & Permissions [Opens in a new window]

Summary

Although there is an increasing understanding of the role of parasites in their host dynamics, accurate, quantitative estimates of parasite caused morbidity in wild animals are rare. Here, we examine the possible impact of 2 tick species (Ixodes ricinus, I. hexagonus) on the condition of the European hedgehog (Erinaceus europaeus). For this, we tested for correlations between blood parameters of 36 adult hedgehogs from an experimental population enclosed in a natural habitat and their tick infestation over a period of 8 months (March–October 2007). We found correlations between the tick infestation and the concentration of red blood cells, haemoglobin, haematocrit, MCH, MCHC, thrombocytes, lymphocytes and neutrophils. These results indicate that ticks can induce anaemia in the hedgehog. The peripheral blood characteristics and the erythrocyte indices characterize this anaemia as haemorrhagic and regenerative. During the course of our study the hedgehogs of our population showed below normal mortality but morbidity was found to be high resulting from the blood loss caused by the feeding activity of the ticks.

Keywords

Erinaceus europaeusEuropean hedgehogIxodeshaematologyregenerative anaemiablood sampling
Type
Research Article
Information
Parasitology , Volume 136 , Issue 4 , April 2009 , pp. 443 - 452
Copyright
Copyright © 2009 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arthur, D. R. (1963). British Ticks. Butterworths, London, UK.Google Scholar
Aubert, M. F. A. (1975). Contribution a l'étude 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, 452–479.Google Scholar
Balashov, YU. S. (1968). Bloodsucking ticks (Ixodoidea)-vectors of diseases of man and animals. Miscellaneous Publications of the Entiomological Society of America 8, 161–376.Google Scholar
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008). Poor condition and infection: a viscious circle in natural populations. Proceedings of the Royal Society of London, B 275, 1753–1759. doi: 10.1098/rspb.2008.0147.Google Scholar
Bowessidjaou, J., Brossard, M. and Aeschlimann, A. (1977). Effects and duration of resistance acquired by rabbits on feeding and egg laying in Ixodes ricinus L. Experientia 33, 528–530. doi: 10.1007/BF01922254.CrossRefGoogle ScholarPubMed
Bowman, A. S., Coons, L. B., Needham, G. R. and Sauer, J. R. (1997). Tick saliva: recent advances and implications for vector competence. Medical and Veterinary Entomology 11, 277–285. doi: 10.1111/j.1365-2915.1997.tb00407.x.CrossRefGoogle ScholarPubMed
Brossard, M. (1982). Rabbits infested with adult Ixodes ricinus L.: effects of mepyramine on acquired resistance. Experientia 38, 702–703. doi: 10.1007/BF01964106.CrossRefGoogle ScholarPubMed
Canfield, P. J. (1998). Comparative cell morphology in the peripheral blood film from exotic and native animals. Australian Veterinary Journal 76, 793–800.CrossRefGoogle ScholarPubMed
Council of Europe (1979). Convention on the conservation of European wildlife and natural habitats. Council of Europe, Strasbourg.Google Scholar
Dobson, A. P., Hudson, P. J. and Lyles, A. M. (1992). Macroparasite: worms and others. In Natural Enemies: the Population Biology of Predators, Parasites and Diseases (ed. Crawley, M. J.), pp. 329–348. Blackwell Scientific Publication, Oxford, UK.CrossRefGoogle Scholar
Dunlap, D. and Mathies, T. (1993). Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 4, 1045–1048.CrossRefGoogle Scholar
Eliassen, E. (1961). Changes of blood volume in the pre-hibernating and deep-hibernating hedgehog. Nature, London 192, 1047–1049. doi: 10.1038/1921047a0.CrossRefGoogle Scholar
Fernandez, F. R. and Grindem, C. B. (2000). Reticulocyte response. In Schalm's Veterinary Hematology (ed. Feldman, B. F., Zinkl, J. G. and Jain, N. C.),pp. 110–116. Lipincott, Philadelphia, PA, USA.Google Scholar
Fischer, H. (2007). Der Europäische Igel (Erinaceus europaeus) als Wirt der Schildzecken Ixodes (Ixodes) ricinus und Ixodes (Pholeoixodes) hexagonus. Thesis, University of Karlsruhe, Karlsruhe, Germany.Google Scholar
Gemmell, R. T., Cepon, G., Green, P. E. and Stewart, N. P. (1991). Some effects of tick infestations on juvenile northern brown bandicoot (Isoodon macrourus). Journal of Wildlife Diseases 27, 269–275.CrossRefGoogle ScholarPubMed
Gern, L., Rouvinez, E., Toutoungi, L. N. and Godfroid, E. (1997). Transmission cycles of Borrelia burgdorferi sensu lato involving Ixodes ricinus and/or I. hexagonus ticks and the European hedgehog, Erinaceus europaeus, in suburban and urban areas in Switzerland. Folia Parasitologica 44, 309–314.Google ScholarPubMed
Hadjuk, P., Copland, M. D. and Schultz, D. A. (1992). Effects of capture on hematological values and plasma cortisol levels of free-range Koalas (Phascolarctos cinereus). Journal of Wildlife Diseases 28, 502–506.Google Scholar
Hannier, S., Liversidge, J., Sternberg, J. M. and Bowman, A. S. (2004). Characterization of the B-cell inhibitory protein factor in Ixodes ricinus tick saliva: a potential role in enhanced Borrelia burgdorferi transmission. Immunology 113, 401–408. doi: 10.1111/j.1365-2567.2004.01975.x.CrossRefGoogle Scholar
Heath, G. B. S. (1951). The sheep tick, Ixodes ricinus L. eradication by dipping sheep. Parasitology 41, 109–223.CrossRefGoogle ScholarPubMed
Heldmaier, G., Ortmann, S. and Elvert, R. (2004). Natural hypometabolism during hibernation and daily torpor in mammals. Respiratory Physiology & Neurobiology 141, 317–329. doi: 10.1016/j.resp.2004.03.014.CrossRefGoogle ScholarPubMed
Hoeck, H. N. (1987). Hedgehog mortality during hibernation. Journal of Zoology 213, 755–757.CrossRefGoogle Scholar
Huijser, M. P. and Bergers, P. J. M. (2000). The effect of roads on traffic hedgehog (Erinaceus europaeus) populations. Biological Conservation 95, 111–116. doi: 10.1016/S0006-3207(00)00006-9.CrossRefGoogle Scholar
Irvine, R. J. (2006). Parasites and the dynamic of wild mammal populations. Animal Science 82, 775–781.CrossRefGoogle Scholar
Jellison, W. L. and Kohls, G. M. (1938). Tick-host anemia: a secondary anemia induced by Dermacentor andersoni Stiles. The Journal of Parasitology 24, 143–154.CrossRefGoogle Scholar
Jonsson, N. N., Mayer, D. G., Matschoss, A. L., Green, P. E. and Ansell, J. (1998). Production effects of cattle tick (Boophilus microplus) infestation of high yielding dairy cows. Veterinary Parasitology 78, 65–77. doi: 10.1016/S0304-4017(98)00118-6.CrossRefGoogle ScholarPubMed
Koch, H. G. and Sauer, J. R. (1984). Quantity of blood ingested by four species of hard ticks (Acari: Ixodidae) fed on domestic dogs. Annals of the Entomological Society of America 77, 142–146.CrossRefGoogle Scholar
Koch, H. G., Sauer, J. R. and Hair, J. A. (1974). Concentration of the ingested meal in four species of hard ticks. Annals of the Entomological Society of America 67, 861–866.CrossRefGoogle Scholar
Lack, D. (1954). The Natural Regulation of Animal Numbers. Methuen, London, UK.Google Scholar
Lawrie, C. H., Randolph, S. E. and Nuttall, P. A. (1999). Ixodes ticks: serum species sensitivity of anticomplement activity. Experimental Parasitology 93, 207–214. doi: 10.1006/expr.1999.4456.CrossRefGoogle ScholarPubMed
Leboulle, G., Crippa, M., Decrem, Y., Mejri, N., Brossard, M., Bollen, A. and Godfroid, E. (2002). Characterization of a novel salivary immunosuppressive protein from Ixodes ricinus ticks. The Journal of Biological Chemistry 277, 10083–10089. doi: 10.1074/jbc.M111391200.CrossRefGoogle ScholarPubMed
Lees, A. D. (1952). The role of cuticle growth in the feeding process of ticks. Proceedings of the Zoological Society, London 121, 759–772.CrossRefGoogle Scholar
Lewis, J. C. M., Norcott, M. R., Frost, L. M. and Cusdin, P. (2002). Normal haematological values of European hedgehogs (Erinaceus europaeus) from an English rehabilitation centre. Veterinary Record 151, 567–569.CrossRefGoogle ScholarPubMed
Lienhardt, G. (1979). Beobachtungen zum Verhalten des Igels (Erinaceus europaeus) und seine Überlebensmöglichkeiten im heutigen Biotop. Zoologische Beiträge 25, 447–484.Google Scholar
Liebisch, A. and 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). Deutsche Tierärztliche Wochenschrift 93, 447–450.Google ScholarPubMed
Liebisch, A. and Liebisch, G. (2003). Biologie und Ökologie der Zecken. In Zeckenborreliose Lyme-Krankheit bei Mensch und Tier (ed. Horst, H.),pp. 32–48. Spitta-Verlag, Balingen, Germany.Google Scholar
Martyn, K. P. (1988). Provisional atlas of the ticks (Ixodoidea) of the British Isles. Natural Environment Research Council, Dorchester, UK.Google Scholar
Mejri, N., Rutti, B. and Brossard, M. (2002). Immunosuppressive effects of Ixodes ricinus tick saliva or salivary gland extracts on innate and acquired immune response of BALB/c mice. Parasitological Research 88, 192–197. doi: 10.1007/s00436-001-0515-1.CrossRefGoogle ScholarPubMed
Orlowski, G. and Nowak, L. (2004). Road mortality of hedgehogs Erinaceus spp. in farmland in lower Silesia (south-western Poland). Polish Journal of Ecology 52, 377–382.Google Scholar
Rechav, Y. (1987). Resistance of Braham and Hereford cattle to African ticks with reference to serum gamma globulin levels and blood composition. Experimental and Applied Acarology 3, 219–232.CrossRefGoogle Scholar
Reeve, N. (1994). Hedgehogs. Poyser Ltd, London, UK.Google Scholar
Riley, P. Y. and Chomel, B. B. (2005). Hedgehog Zoonoses. Emerging Infectious Diseases 11, 1–5.CrossRefGoogle ScholarPubMed
Santhosh-Kumar, C. R., Yohannan, M. D., Higgy, K. E. and al-Mashhadani, S. A. (1991). Thrombocytosis in adults: analysis of 777 patients. Journal of Internal Medicine 229, 493–495.CrossRefGoogle ScholarPubMed
Sauer, J. R., McSwain, J. L., Bowman, A. S. and Essenberg, R. C. (1995). Tick salivary gland physiology. Annual Reviews in Entomology 40, 245–267. doi: 10.1146/annurev.en.40.010195.0013333.CrossRefGoogle ScholarPubMed
Saupe, E. (1988). Die Parasitosen des Igels und ihre Behandlung. Der praktische Tierarzt 12, 49–54.Google Scholar
Skuballa, J., Oehme, R., Hartelt, K., Petney, T., Bücher, T., Kimmig, P. and Taraschewski, H. (2007). European hedgehogs as hosts for Borrelia spp., Germany. Emerging Infectious Diseases 13, 952–953.CrossRefGoogle ScholarPubMed
Spencer, A. J. and Canfield, P. J. (1993). Haematological characterisation of heavy tick infestation in Koalas (Phascolarctos cinereus). Comparative Haematology International 3, 225–229. doi: 10.1007/BF02341970.CrossRefGoogle Scholar
Taraschewski, H. (2006). Parasiten und Wirte als Bestandteile von Ökosystemen. In Allgemeine Parasitologie (ed. Hiepe, T., Lucius, R. and Gottstein, B.), pp. 276–325. Parey, Berlin, Germany.Google Scholar
Thomas, L. (2007). Labor und Diagnose, 7th Edn.TH-Books Verlagsgesellschaft GmbH, Frankfurt/Main, Germany.Google Scholar
Timme, A. (1980). Krankheits- und Todesursachen beim Igel (Erinaceus europaeus L.) Sektionsfälle 1975–1979. Der praktische Tierarzt 61, 744–746.Google Scholar
Tompkins, D. M., Dobson, A. P., Arneberg, P., Begon, M. E., Cattadori, I. M., Greenman, J. V., Heesterbeek, J. A. P., Hudson, P. J., Newborn, D., Pugliese, A., Rizzoli, A. P., Rosà, R., Rosso, F. and Wilson, K. (2006). Parasites and host population dynamics. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 45–62. Oxford University Press, Oxford, UK.Google Scholar
Toutoungi, L. N., Gern, L. and Aeschlimann, A. (1995). Biology of Ixodes (Pholeoixodes) hexagonus under laboratory conditions. Part II. Effect of mating on feeding an fecundity of females. Experimental & Applied Acarology 19, 233–245. doi: 10.1007/BF00130826.CrossRefGoogle ScholarPubMed
Tyler, R. D. and Cowell, R. L. (1996). Classification and diagnosis of anaemia. Comparative Haematology International 6, 1–16. doi: 10.1007/BF00368096.CrossRefGoogle Scholar
Von Wick, E.-M. (2006). http://www.pro-igel.de/merkblaetter/publpdfs/tierarzt.pdf. (09.04.2008).Google Scholar
Wenzel, U. D., Sachse, M. and Arnold, P. (1977). Ein Beitrag zum Blutbild vom Igel (Erinaceus europaeus Linné 1758). Zoologischer Garten 47, 273–279.Google Scholar
Wikel, S. K. and Alarcon-Chaidez, F. J. (2001). Progress toward molecular characterization of ectoparasite modulation of host immunity. Veterinary Parasitology 101, 275–287. doi: 10.1016/S0304-4017(01)00556-8.CrossRefGoogle ScholarPubMed