Experimental & Applied Acarology

, Volume 40, Issue 3–4, pp 279–290 | Cite as

Hyalomma aegyptium as dominant tick in tortoises of the genus Testudo in Balkan countries, with notes on its host preferences

  • Pavel Široký
  • Klára J. Petrželková
  • Martin Kamler
  • Andrei D. Mihalca
  • David Modrý
Article

Abstract

Collection of 1327 ticks sampled throughout Greece, Bulgaria, Romania and Croatia, from 211 tortoises belonging to three species, Testudo marginata Schoepff, T. graeca Linnaeus, and T. hermanni Gmelin, revealed the presence of four species of ixodid ticks, namely Hyalomma aegyptium (Linnaeus), Haemaphysalis sulcata Canestrini and Fanzago, H. inermis Birula and Rhipicephalus sanguineus (Latreille). Study confirmed the strong dominance of all life stages of H. aegyptium among ticks parasitizing west Palaearctic tortoises of genus Testudo Linnaeus. Furthermore, a considerable portion of ticks collected from tortoises in southwestern Bulgaria represent larvae and nymphs of H. sulcata. At the same area we collected as exception one larva and one nymph of H. inermis from a single specimen of T. hermanni. Our findings of four adults of R. sanguineus is the first record of this species from reptilian host. According to our results achieved on localities with syntopic occurrence of two tortoise species, T. marginata and T. graeca represent in the Balkans the principal hosts of H. aegyptium, whereas T. hermanni serves only as an alternative host in the areas close to range of either T. marginata or T. graeca.

Keywords

Hyalomma aegyptium host preferences Haemaphysalis sulcata Haemaphysalis inermis Rhipicephalus sanguineus Balkan Testudo spp 

Abbreviations

GR

Greece

BG

Bulgaria

RO

Romania

CR

Croatia

Notes

Acknowledgements

The study was partially supported by the grants No. 524/03/H133 and No. 524/03/D104 of the Grant Agency of the Czech Republic. We are grateful to all members of the Bulgaria 2002 expedition for help in the field. Thanks to Vesna Cafuta and Tomi Trilar (Slovenian Museum of Natural History) for the loan of comparative material, to Gerrit Uilenberg and Philippe Parola for information on Corsican finding of H. aegyptium and to Eva Jánová for consultation of used statistic methods. We thank also to two anonymous reviewers for their improve the early version of manuscript.

References

  1. Apanaskevich DA (2003) K diagnostike vida Hyalomma (Hyalomma) aegyptium (Acari, Ixodidae) (To diagnostics of Hyalomma [Hyalomma] aegyptium [Acari: Ixodidae]). Parazitologija 37:47–59Google Scholar
  2. Apanaskevich DA (2004) Parazito-Khozjainnye svjazi vidov roda Hyalomma Koch, 1844 (Acari, Ixodidae) i ikh svjaz smikroevoljucionnym processom (Host-parasite relationships of the genus Hyalomma Koch, 1844 (Acari, Ixodidae) and their connection with microevolutionary process). Parazitologija 38:515–523Google Scholar
  3. Barnard SM, Durden LA (2000) A Veterinary Guide to the Parasites of Reptiles. Vol. 2, Arhropods (Excluding Mites). Krieger Publishing Company, Malabar, FloridaGoogle Scholar
  4. Brotóns NJ, Estrada-Peña A (2004) Survival of tick colonies on captive imported reptiles in Spain. In: Abstracts of the 7th International Symposium on pathology and medicine of reptiles and amphibians, Berlin, 16–18 April 2004Google Scholar
  5. Buresh I, Drensky P (1932) Prinosa kama izuchvane na karlezhite Ixodidae (Arachnoidea) va Balgaria (Additional data to knowledge on ticks [Ixodidae] of Bulgaria). Izv Balg Entomol 7:116–124Google Scholar
  6. Burridge MJ (2001) Ticks (Acari: Ixodidae) spread by the international trade in reptiles and their potential roles in dissemination of diseases. Bull Entomol Res 91:3–23PubMedGoogle Scholar
  7. Burridge MJ, Simmons LA (2003) Exotic ticks introduced into the United States on imported reptiles from 1962 to 2001 and their potential roles in international dissemination of diseases. Vet Parasitol 113:289–320PubMedCrossRefGoogle Scholar
  8. Černý V (1959) Ein Beitrag zur Zeckenfauna Bulgariens. Práce Brněnské Základny Československé Akademie Věd 31:361–364Google Scholar
  9. Drensky P (1955) Sastav i razprostranenie na karlezhite (Ixodoidea) v Balgaria (Species composition and distribution of ticks [Ixodoidea] in Bulgaria). Izv Zool Inst 4:109–168Google Scholar
  10. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washington, D.CGoogle Scholar
  11. Estrada-Peña A, Bouattour A, Camicas J-L, Walker AR (2004) Ticks of Domestic Animals in the Mediterranean Region. A Guide to Identification of Species. International Consortium on ticks and tick-borne diseases, University of Zaragoza, SpainGoogle Scholar
  12. Feldman-Muehsam B (1948) On larvae and nymphs of some species of Palestinian Hyalomma. Parasitology 39(1–2):138–147CrossRefPubMedGoogle Scholar
  13. Fritz U, Cheylan M (2001) Testudo Linnaeus, 1758—Eigentliche Landschildkröten. In: Fritz U (ed) Handbuch der Reptilien und Amphibien Europas. Band 3/IIIA Schildkröten (Testudines) I (Bataguridae, Testudinidae, Emydidae). AULA-Verlag GmbH, Wiebelsheim, Germany, p 113–124Google Scholar
  14. Fritz U, Široký P, Kami H, Wink M (2005) Environmentally caused dwarfism or a valid species – Is Testudo weissingeri Bour, 1996 a distinct evolutionary lineage? New evidence from mitochondrial and nuclear genomic markers. Mol Phylogenet Evol 37:389–401PubMedCrossRefGoogle Scholar
  15. Hailey A (2000) Assessing body mass condition in the tortoise Testudo hermanni. Herp J 10:57–61Google Scholar
  16. Hailey A, Wright J, Steer E (1988) Population ecology and conservation of tortoises: the effects of disturbance. Herp J 1:294–301Google Scholar
  17. Haitlinger R (1993) Acari (Arachnida) and Anoplura (Insecta) collected on small mammals, reptiles and insects in Greece and Cyprus. Biologia Gallo-hellenica 20:83–88Google Scholar
  18. Hoogstraal H (1956) African Ixodoidea. I. Ticks of the Sudan. Washington, D.CGoogle Scholar
  19. Hoogstraal H, Kaiser MN (1960) Some host relationships of the tortoise tick, Hyalomma (Hyalommasta) aegyptium (L.) (Ixodoidea, Ixodidae) in Turkey. Ann Entomol Soc Amer 53:457–458 Google Scholar
  20. Hoogstraal H, Wassef HY, Büttiker W (1981) Ticks (Acarina) of Saudi Arabia, fam. Argasidae, Ixodidae. Fauna of Saudi Arabia 3:25–110Google Scholar
  21. Horak IG, Camicas J-L, Keirans JE (2002) The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. Exp Appl Acarol 28:27–54PubMedCrossRefGoogle Scholar
  22. Iverson JB (1992) A revised checklist with distribution maps of the turtles of the world. Privately printed, Richmond, IndianaGoogle Scholar
  23. Kaiser MN, Hoogstraal H (1963) The Hyalomma ticks (Ixodoidea, Ixodidae) of Afghanistan. J Parasitol 49:130–139CrossRefGoogle Scholar
  24. Kolonin GV (1983) Mirovoe rasprostranenie iksodovykh kleshchey. Rody Hyalomma, Aponomma, Amblyomma (World distribution of ixodid ticks. Genera Hyalomma, Aponomma, Amblyomma). Nauka, Moskva, SSSRGoogle Scholar
  25. Lác J, Cyprich D, Kiefer M (1972) Zeckenartige (Ixodidae) als Parasiten von Eidechsen unter den ökologischen Bedingungen der Slowakei. Zool Listy 21:133–144Google Scholar
  26. Leontyeva O, Kolonin G (2002) Hyalomma aegyptium (Acari: Ixodida: Ixodidae) as the parasite of Testudo graeca at the western Caucasus. Chelonii 3:332–336Google Scholar
  27. Loveridge A, Williams EE (1957) Revision of the African tortoises and turtles of the suborder Cryptodira. Bull Mus Comp Zool 115:163–557Google Scholar
  28. Matsumoto K, Parola P, Brouqui P, Raoult D (2004) Rickettsia aeschlimannii in Hyalomma ticks from Corsica. Eur J Clin Microbiol Infect Dis 23:732–734PubMedCrossRefGoogle Scholar
  29. Nosek J, Sixl W (1972) Central-European ticks (Ixodoidea). Mitt Abt Zool Landesmus Joanneum 1:61–92Google Scholar
  30. Petney TN, Al-Yaman F (1985) Attachment sites of the tortoise tick Hyalomma aegyptium in relation to tick density and physical condition of the host. J Parasitol 71:287–289CrossRefGoogle Scholar
  31. Pietzsch M, Quest R, Hillyard PD, Medlock JM, Leach S (2006) Importation of exotic ticks into the United Kingdom via the international trade in reptiles. Exp Appl Acarol 38:59–65PubMedCrossRefGoogle Scholar
  32. Pomerancev BI (1950) Iksodovye kleshchi (Ixodidae) (Ixodid ticks [Ixodidae]). Fauna SSSR, Tom. 4, Vyp. 2. Paukoobraznye. Izdatelstvo Akademii Nauk SSSR, Moskva, LeningradGoogle Scholar
  33. Randolph SE, Chemini C, Furlanello C, Genchi C, Hails RS, Hudson PJ, Jones LD, Medley G, Norman RA, Rizzoli AP, Smith G, Woolhouse MEJ (2002) The ecology of tick-borne infections in wildlife reservoirs. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The Ecology of Wildlife Diseases. Oxford University Press, 119–138Google Scholar
  34. Rees DJ, Dioli M, Kirkendall LR (2003) Molecules and morphology: evidence for cryptic hybridization in African Hyalomma (Acari: Ixodidae). Mol Phylogenet Evol 27:131–142PubMedCrossRefGoogle Scholar
  35. Řeháček J, Grešíková M, Nosek J (1961) Study of the relation of the green lizard (Lacerta viridis Laur.) to natural foci of tick-borne encephalitis. J Hyg Epidemiol Microbiol Immunol 5:366–372PubMedGoogle Scholar
  36. Robbins RG, Karesh WB, Calle PP, Leontyeva OA, Pereshkolnik SL, Rosenberg S (1998) First records of Hyalomma aegyptium (Acari: Ixodida: Ixodidae) from the Russian spur-thighed tortoise, Testudo graeca nikolskii, with an analysis of tick population dynamics. J Parasitol 84:1303–1305PubMedCrossRefGoogle Scholar
  37. Sankoh AJ, Huque MF, Dubey SD (1997) Some comments on frequently used multiple endpoint adjustments methods in clinical trials. Statistics in Medicine 16:2529–2542PubMedCrossRefGoogle Scholar
  38. Sonenshine DE (1993) Biology of Ticks, Volume 2. Oxford University Press, New York, OxfordGoogle Scholar
  39. Sweatman GK (1968) Temperature and humidity effects on the oviposition of Hyalomma aegyptium ticks of different engorgement weights. J Med Entomol 5:429–439PubMedGoogle Scholar
  40. Willemsen RE, Hailey A (2002) Body mass condition in Greek tortoises: Regional and interspecific variation. Herp J 12:105–114Google Scholar
  41. Zlatanova VD (1991) Iksodovi karlezhi (Parasitiformes, Ixodidae) na suchozemnite kostenurki (Reptilia, Testudinidae) v Balgaria (Ixodid ticks [Parasitiformes, Ixodidae] of tortoises [Reptilia, Testudinidae] in Bulgaria). Acta Zool Bulg 41:77–79Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Pavel Široký
    • 1
  • Klára J. Petrželková
    • 2
  • Martin Kamler
    • 3
  • Andrei D. Mihalca
    • 4
  • David Modrý
    • 3
    • 5
  1. 1.Department of Biology and Wildlife DiseasesUniversity of Veterinary and Pharmaceutical SciencesBrnoCzech Republic
  2. 2.Department of Mammal Ecology, Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  3. 3.Department of ParasitologyUniversity of Veterinary and Pharmaceutical SciencesBrnoCzech Republic
  4. 4.Department of Parasitology and Parasitic DiseasesFaculty of Veterinary MedicineCluj-NapocaRomania
  5. 5.Institute of Parasitology, Biology CenterAcademy of Sciences of the Czech RepublicČeské BudějoviceCzech Republic

Personalised recommendations