Ticks of the genus Hyalomma have been implicated in the transmission of the bunyavirus, Crimean-Congo hemorrhagic fever virus (CCHFV) and are natural competent vectors of this virus (Hoogstraal 1979). CCHFV is currently endemic in some areas of sub-Saharan Africa, south-eastern Europe and Asia (WHO 2011). Recently, CCHFV has been isolated from Hyalomma lusitanicum ticks in Spain (Estrada-Peña et al. 2012). The long duration of host attachment enables immature Hyalomma spp. ticks to be carried across borders by migrating birds during the spring and autumn migration (Hoogstraal et al. 1961, Molin et al. 2011). Recently, Molin et al. (2011) recorded 367 Hyalomma spp. ticks on 7,453 spring migrants along the central and eastern Mediterranean flyways.

Many migrant birds that breed in northwest Europe overwinter in sub-Saharan Africa and therefore have the potential to introduce CCHFV-infected Hyalomma spp. ticks at breeding sites or en route during migration. Ticks of the genus Hyalomma have been recorded on spring migrants trapped in the UK and Germany, but the origin of these ticks is unknown (Martyn 1988, Jameson et al. 2012, Rumer et al. 2011). Many migrants breeding in northwest Europe fly across the Strait of Gibraltar from Africa in the spring. This study aimed to trap migrants on their northward journey through southern Spain and determine the number infested with ticks.

Birds were captured in mist nets at eight different locations throughout the provinces of Cadiz and Malaga, southern Spain, between 23 April and 15 May 2011. The last two weeks of April and the first two weeks of May are the most important for migrant birds introducing Hyalomma spp. ticks into central Spain (A. de la Torre, personal communication). The locations were existing bird ringing sites regularly used by the local bird ringing group and represented different habitat types including grassland, woodland, riverine, and coastal habitats. Birds were captured between 06:00–13:00 and 16:00–18:00. Each captured bird was identified to species and the ears, eyes, beak, gape, nape, and abdomen of each bird were checked for ticks (as in Molin et al. 2011). Any tick observed was removed with tweezers and placed immediately into tick fixative consisting of 70% ethanol, 20% distilled water, and 10% glycerol. Ticks were stored separately according to the individual birds from which they were removed. The ticks were aged and identified to genus morphologically using Estrada-Peña et al. (2004). Identification of immature ticks is difficult (Molin et al. 2011), and molecular identification methods were not available. Immature Hyalomma spp. ticks were morphologically identified to species using Apanaskevich and Horak (2008) and were then tested for CCHFV using the RT-PCR developed by Atkinson et al. (2012) using a SuperScript III (SSIII) Platinum One-step qRT-PCR kit (Invitrogen).

Birds were categorized as migrant or resident (Table 1) on the basis of species, or wing length in the case of Sylvia atricapilla Linnaeus. In southern Spain, some populations of S. atricapilla are migratory and some are resident. The individual birds can be distinguished by wing length, as those with wing lengths between 66–72 mm are residents and those between 72–80 mm are migrants (R. Banham, personal communication).

Table 1.  Bird species trapped during springtime migration that were infested with ticks. An additional 289 birds of 40 different species were also caught but none were found to be infested with ticks.
SpeciesFamilyResident (R) or Migrant (M) speciesNo. birdsNo. ticksNo. birds infestedMean infestation rate (No. ticks /infested bird)Mean no. larvae /infested birdMean no. nymphs /infested birdGenus of ticks
Carduelis chloris FringillidaeR84261321.080.85 Ixodes
Erithacus rubecula MuscicapidaeR911110 Ixodes
Hippolais opaca AcrocephalidaeM821202 Hyalomma
Luscinia megarhynchos MuscicapidaeM502210.50.5 Ixodes
Parus major ParidaeR106320.671.33 Ixodes
Serinus serinus FringillidaeR4711101 Ixodes
Sylvia atricapilla SylviidaeM1111101 Ixodes
Turdus merula TurdidaeR234795.222.562.56 Ixodes

A total of 531 birds was caught in mist nets and checked for ticks. A total of 86 ticks was collected from 31 individual birds (5.83% of birds caught), with an average tick load of 2.77 ticks per infested bird (Table 1). The majority of the ticks found (n=84) were larvae and nymphs of Ixodes spp. (Table 1). Of the birds caught, 202 were migrants and one of these, a single Hippolais opaca Cabanis carried two nymphal Hyalomma spp. ticks, giving a Hyalomma spp. infestation rate of 0.5% for migrants. A Fisher's exact test was applied to determine if this percentage was significantly different from the number of Hyalomma spp. ticks found on migrant birds (Molin et al. 2011) migrating along the central and eastern Mediterranean flyways. The result of the Fisher's exact test was p= 0.0660. After morphological analysis, the two Hyalomma spp. nymphs were identified as H. marginatum (identification provided by A. Bouattour, Institut Pasteur, Tunis) but molecular confirmation of this was not possible. The total number of ticks found on migrant bird species was five, compared to 81 found on resident bird species and all ticks found were immatures (43 nymphs, 41 larvae) with the exception of two ticks that it was not possible to age due to damage during removal. The result of the RT-PCR test on the two Hyalomma spp. nymphs showed them to be negative for CCHFV.

Eighty-six ticks were found on 531 birds at sites in the provinces of Cadiz and Malaga, Spain, between late April and mid-May, 2011. The majority of ticks (97.7%) were Ixodes spp. collected from resident birds with just two Hyalomma spp. ticks found on a migrant H. opaca. Molin et al. (2011) found that Hyalomma spp. made up 95.6% of all the ticks that they collected from migrant birds in Antikythera, Greece, and Capri, Italy, with only seven Ixodes spp. ticks reported. This study focused on the movement of ticks on birds along the East Atlantic flyway in the western Mediterranean and in this respect complements the study of Molin et al. (2011) on ticks on migrants along the central and eastern Mediterranean flyways. In Greece and Italy, immature ticks (predominantly Hyalomma spp.) were recovered from some 20 species of birds including Erithacus rubecula Linnaeus, Ficedula hypoleuca Pallas, Sylvia borin Boddaert, Hippolais pallida Ehrenberg, and Luscinia megarhynchos Brehm (Molin et al. 2011).

In this study, more resident birds (n=329) were trapped than migrants (n=202). The total number of all birds trapped, especially migrants, was lower than expected due to adverse local weather conditions and therefore comparison with Molin et al. (2011) has to be made with caution, due to their much larger sample size.

Birds of the species Turdus merula Linnaeus were the most infested, followed by Carduelis chloris Linnaeus. Hasle et al. (2009b) found that most of the ticks they collected were from ground-feeding birds, with particular reference to the family Turdidae. It is possible that ticks are more likely to infest ground-feeding birds as the birds will come into contact with questing ticks among vegetation in the case of Ixodes spp. and on the ground itself in the case of Hyalomma spp. In total, 51 of the 86 ticks collected were from bird species that nest on or close to the ground. However, there is variation in nesting and feeding strategies within bird species and therefore it is not possible to determine whether these factors had an impact on tick infestation rates in this study.

H. opaca is a migrant species in Spain and spends the winter in sub-Saharan Africa. It breeds and over-winters in dry habitats with medium height trees and shrubs, including gardens and orchards. Due to its preference for dry habitats, it is not surprising that it is parasitized by the xerophilic Hyalomma spp. tick. The two Hyalomma spp. nymphs removed from the H. opaca in this study were morphologically identified as H. marginatum. If this identification was correct, then the origin of the ticks could have been Spain or North Africa (Apanaskevich and Horak 2008). If the ticks were not H. marginatum, then they would almost certainly have been H. rufipes picked up in Africa. A large number of H. rufipes have been found on African wintering migrants (Hoogstraal et al. 1961, Hoogstraal et al. 1964). If the two Hyalomma spp. nymphs recovered from the H. opaca were confirmed to be H. marginatum by molecular identification, their origin would remain uncertain. The nymphs were engorged, suggesting they had been attached to the bird for some time, but it is not known when the H. opaca arrived in Spain. Irrespective of their origin, the ticks tested negative for CCHFV. Both H. marginatum and H. rufipes are vectors of CCHFV and recently CCHFV has been identified in Hyalomma lusitanicum ticks in the region of Extremadura, Spain (Estrada-Peña et al. 2012). H. lusitanicum do not commonly parasitize birds (Apanaskevich et al. 2008), and at present CCHFV has not been found in any other tick species in Spain. This suggests that ticks picked up by passage migrants in Spain would currently pose no risk of entry of CCHFV into northwest Europe. Research on the prevalence of CCHFV in other Hyalomma spp. ticks in Spain is required to fully assess the risk.

The percentage of migrant birds infested with Hyalomma spp. was low in this study carried out along the East Atlantic flyway, at 0.5% (with 95% binomial confidence interval of 0.01%–2.73%). The percentage of migrants carrying Hyalomma spp. along the central and eastern Mediterranean flyways, the other migration routes into Europe from Africa, was found to be five-fold higher at 2.59% (193/7,453 migrants with a 95% binomial confidence interval of 2.24%–2.98%) (Molin et al. 2011). This difference was found to be significant to 10% (p=0.0660), such that there is some evidence to suggest that the number of immature Hyalomma spp. ticks introduced per migrant bird is lower on migrants coming into western Europe through the East Atlantic flyway compared to those entering central and eastern Europe. More sampling along the East Atlantic flyway is required to draw conclusions.

A study conducted at four bird observatories on the south coast of Norway (an area that falls within the East Atlantic flyway) found low infestation rates of Hyalomma spp. ticks (Hasle et al. 2009a). Of 9,768 passerine birds captured, seven nymphal Hyalomma rufipes were found on seven individual migrants, giving an infestation rate of 0.07%. A recent study on the south coast of England found a Hyalomma spp. infestation rate of 0.93%, with 57% of all Hyalomma spp. ticks found on Oenanthe oenanthe Linnaeus (Jameson et al. 2012). These studies add support to our finding of low infestation rates of Hyalomma spp. on migrants using the East Atlantic flyway. Further research is required at different locations along the East Atlantic flyway to clarify where Hyalomma spp. ticks are being picked up by migratory birds that breed in northwest Europe and whether these ticks are infected with CCHFV. This would help to evaluate the risk, if any, that this migration pathway poses to northwest Europe in terms of an incursion event of CCHFV.


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  2. Acknowledgments

We thank Katy Heath, Dr. Richard Banham, and Grupo Ornitológico del Estrecho for their help with bird ringing and tick collection, and Dr. Ali Bouattour of the Institut Pasteur, Tunis for his help with tick identification. This study was funded as part of a Ph.D. studentship at the Animal Health and Veterinary Laboratories Agency and the Health Protection Agency.


  1. Top of page
  2. Acknowledgments
  • Apanaskevich, D.A. and I. Horak. 2008. The genus Hyalomma Koch, 1844: v. Re-evaluation of the taxonomic rank of taxa comprising the h. Euhyalomma marginatum Koch complex of species (acari: ixodidae) with redescription of all parasitic stages and notes on biology. Int. J. Acarol. 34: 1342.
  • Apanaskevich, D.A., M.M. Santos-Silva, and I. Horak. 2008. The genus Hyalomma Koch, 1844.IV. Redesciption of all parasitic stages of H. (Euhyalomma) lusitanicum Kock, 1844 and the adults of H. (E.) franchinii Tonelli Rondelli, 1932 (Acari: Ixodidae) with a first description of its immature stages. Folia Parasitol. 55: 6174.
  • Atkinson, B., J. Chamberlain, C.H. Logue, N. Cook, C. Bruce, S.D. Dowall, and R. Hewson. 2012. Development of a real-time RT-PCR assay for the detection of Crimean-Congo hemorrhagic fever virus. Vector-Borne Zoonot. Dis. 12.
  • Estrada-Peña, A., A. Bouattour, J.L. Camicas, and A.R. Walker. 2004. Ticks of Domestic Animals in the Mediterranean region: A Guide to Identification of Species. Netherlands , University of Zaragoza.
  • Estrada-Peña, A., A.M. Palomar, P. Santibáñez, N. Sánchez, M.A. Habela, A. Portillo, L. Romero, and J.A. Oteo. 2012. Crimean-Congo hemorrhagic fever virus in ticks, southwestern Europe, 2012. Emerg. Infect. Dis. 18: 179180.
  • Hasle, G., G. Bjune, E. Edvardsen, C. Jakobsen, B. Linnehol, J.E. Røer, R. Mehl, K.H. Røed, J. Pedersen, and H.P. Leinaas. 2009a. Transport of ticks by migratory passerine birds to Norway. J. Parasitol. 95: 13421351.
  • Hasle, G., I. Horak, G. Grieve, H.P. Leinaas, and F. Clarke. 2009b. Ticks collected from birds in the northern provinces of South Africa, 2004–2006. Onderstepoort J. Vet. Res. 76: 167175.
  • Hoogstraal, H. 1979. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe and Africa. J. Med. Entomol. 15: 307417.
  • Hoogstraal, H., M.N. Kaiser, M.A. Traylor, S. Gaber, and E. Guindy. 1961. Ticks (Ixodoidas) on birds migrating from Africa to Europe and Asia. Bull. Wld. Hlth. Org. 24: 197212.
  • Hoogstraal, H., M.A. Traylor, S. Gaber, G. Malakatis, E. Guindy, and I. Helmy. 1964. Ticks (Ixodidae) on migrating birds in Egypt, spring and fall 1962. Bull. Wld. Hlth. Org. 30: 355367.
  • Jameson, L.J., P.J. Morgan, J.M. Medlock, G. Watola, and A.G.C. Vaux. 2012. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks Tick-borne Dis. 3: 9599.
  • Martyn, K.P. 1988. Provisional Atlas of the ticks (Ixodoidea) of the British Isles, Cumbria , Institute of Terrestrial Ecology.
  • Molin, Y. L., M. Lindeborg, F. Nyström, M. Madder, E. Hjelm, B. Olsen, T.G.T. Jaenson, and C. Ehrenborg. 2011. Migratory birds, ticks, and Bartonella. Infect. Ecol. Epidemiol. 1: 10.3402iee.v1i0.5997.
  • Rumer, L., E. Graser, T. Hillebrand, T. Talaska, H. Dautel, O. Mediannikov, P. Roy-Chowdhury, O. Sheshukova, O.D. Mantke, and M. Niedrig. 2011. Rickettsia aeschlimannii in Hyalomma marginatum Ticks, Germany. Emerg. Infect. Dis. 17: 325326.
  • WHO. 2011. Crimean Congo Haemorrhagic Fever [Online]. [Accessed 26.08.2011 2011].