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Hyalomma ticks on northward migrating birds in southern Spain: Implications for the risk of entry of Crimean-Congo haemorrhagic fever virus to Great Britain

2016; Wiley; Volume: 41; Issue: 1 Linguagem: Inglês

10.1111/jvec.12204

1948-7134

Marion England, Paul Phipps, Jolyon M. Medlock, Peter M. Atkinson, Barry Atkinson, Roger Hewson, P. Gale,

Vector-Borne Animal Diseases

Journal of Vector EcologyVolume 41, Issue 1 p. 128-134 Original ArticlesFree Access Hyalomma ticks on northward migrating birds in southern Spain: Implications for the risk of entry of Crimean-Congo haemorrhagic fever virus to Great Britain Marion E. England, Marion E. England marion.england@pirbright.ac.uk Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this authorPaul Phipps, Paul Phipps paul.gale@apha.gsi.gov.uk Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this authorJolyon M. Medlock, Jolyon M. Medlock Medical Entomology Group, MRA, Emergency Response Department, Public Health England, Porton Down, Salisbury, SP4 0JG United KingdomSearch for more papers by this authorPeter M. Atkinson, Peter M. Atkinson Geography and Environment, University of Southampton, University Road, Southampton, SO17 1BJ United Kingdom Faculty of Science and Technology, Engineering Building, Lancaster University, Lancaster LA1 4YR United Kingdom Faculty of Geosciences, University of Utrecht, Heidelberglaan 2, 3584 CS Utrecht The Netherlands School of Geography, Archaeology and Palaeoecology, Queen's University Belfast, BT7 1NN Northern Ireland, United KingdomSearch for more papers by this authorBarry Atkinson, Barry Atkinson Public Health England, Virology and Pathogenesis Group, Porton Down, Salisbury, Wiltshire, SP4 0JG United KingdomSearch for more papers by this authorRoger Hewson, Roger Hewson Public Health England, Virology and Pathogenesis Group, Porton Down, Salisbury, Wiltshire, SP4 0JG United KingdomSearch for more papers by this authorPaul Gale, Paul Gale Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this author Marion E. England, Marion E. England marion.england@pirbright.ac.uk Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this authorPaul Phipps, Paul Phipps paul.gale@apha.gsi.gov.uk Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this authorJolyon M. Medlock, Jolyon M. Medlock Medical Entomology Group, MRA, Emergency Response Department, Public Health England, Porton Down, Salisbury, SP4 0JG United KingdomSearch for more papers by this authorPeter M. Atkinson, Peter M. Atkinson Geography and Environment, University of Southampton, University Road, Southampton, SO17 1BJ United Kingdom Faculty of Science and Technology, Engineering Building, Lancaster University, Lancaster LA1 4YR United Kingdom Faculty of Geosciences, University of Utrecht, Heidelberglaan 2, 3584 CS Utrecht The Netherlands School of Geography, Archaeology and Palaeoecology, Queen's University Belfast, BT7 1NN Northern Ireland, United KingdomSearch for more papers by this authorBarry Atkinson, Barry Atkinson Public Health England, Virology and Pathogenesis Group, Porton Down, Salisbury, Wiltshire, SP4 0JG United KingdomSearch for more papers by this authorRoger Hewson, Roger Hewson Public Health England, Virology and Pathogenesis Group, Porton Down, Salisbury, Wiltshire, SP4 0JG United KingdomSearch for more papers by this authorPaul Gale, Paul Gale Animal and Plant Health Agency, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB United KingdomSearch for more papers by this author First published: 27 May 2016 https://doi.org/10.1111/jvec.12204Citations: 18AboutSectionsPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat ABSTRACT Crimean-Congo haemorrhagic fever virus (CCHFV) is a zoonotic virus transmitted by Hyalomma ticks, the immature stages of which may be carried by migratory birds. In this study, a total of 12 Hyalomma ticks were recovered from five of 228 migratory birds trapped in Spring, 2012 in southern Spain along the East Atlantic flyway. All collected ticks tested negative for CCHFV. While most birds had zero Hyalomma ticks, two individuals had four and five ticks each and the statistical distribution of Hyalomma tick counts per bird is over-dispersed compared to the Poisson distribution, demonstrating the need for intensive sampling studies to avoid underestimating the total number of ticks. Rates of tick exchange on migratory birds during their northwards migration will affect the probability that a Hyalomma tick entering Great Britain is positive for CCHFV. Drawing on published data, evidence is presented that the latitude of a European country affects the probability of entry of Hyalomma ticks on wild birds. Further data on Hyalomma infestation rates and tick exchange rates are required along the East Atlantic flyway to further our understanding of the origin of Hyalomma ticks (i.e., Africa or southern Europe) and hence the probability of entry of CCHFV into GB. INTRODUCTION Each spring, birds of a range of species migrate from wintering grounds in sub-Saharan Africa to Great Britain (GB). Many cross the Mediterranean Sea at the Strait of Gibraltar on the East Atlantic flyway. Birds, together with small mammals, are the vertebrate hosts for immature Hyalomma spp. ticks, including Hyalomma marginatum Koch and Hyalomma rufipes Koch (Hoogstraal 1972). Hyalomma spp. ticks have been implicated in the transmission of Crimean-Congo haemorrhagic fever virus (CCHFV) and are considered competent vectors (Whitehouse 2004). CCHFV is widespread in Asia and sub-Saharan Africa and is also endemic in some areas of southeastern Europe and the Balkans (Vorou 2009). Recently, CCHFV was isolated from Hyalomma lusitanicum Koch ticks in Spain (Estrada-Peña et al. 2012). Immature H. marginatum and H. rufipes ticks have a long duration of attachment to the host, owing to their two-host life history (up to 26 days (Hoogstraal 1979)), enabling them and their associated pathogens to be carried long distances by migrating birds (Hoogstraal et al. 1961, Molin et al. 2011, Jameson et al. 2012). There is the possibility that CCHFV could enter GB in Hyalomma spp. ticks transported on migratory birds. Indeed, immature Hyalomma spp. ticks have been recorded on spring migrants trapped in GB (Martyn 1988, Jameson et al. 2012), although to date no CCHFV-positive ticks have been found despite testing (Jameson et al. 2012). Palomar et al. (2012) reported CCHFV in four out of six pools of H. marginatum collected from migratory birds in Morocco. Lindeborg et al. (2012) detected CCHFV in three Hyalomma spp. nymphs from one spring migrant in Greece. To quantify the risk of introduction of CCHFV-infected ticks into GB through migratory birds (Gale et al. 2012), information is needed on (1) The total number of Hyalomma spp. ticks entering GB on migratory birds per year, (2) The proportion of those Hyalomma spp. ticks originating from CCHFV-endemic regions, and (3) The prevalence of CCHFV in Hyalomma spp. ticks in endemic regions. To estimate the total number of ticks entering on migratory birds per year, account should be taken of the statistical distribution of the number of ticks per individual bird. Sampling from a skewed distribution (i.e., one that is over-dispersed relative to the Poisson distribution) will tend to underestimate the arithmetic mean number of ticks per bird because the "rare but all important" individual birds with high tick numbers are likely to be missed by all but the most extensive sampling programs. In a skewed distribution, most birds have zero ticks while a few have high counts. The implications of underestimating the arithmetic mean through sampling from skewed distributions have been discussed previously for pathogens in drinking water (Gale and Stanfield 2000, Gale et al. 2002) and apply similarly to estimating the mean tick count per bird. The probability that a Hyalomma spp. tick is infected with CCHFV will vary depending on its country of origin (see Gale et al. 2012). While it is not possible to determine from which country or region in sub-Saharan Africa a tick on a bird originated, it is appropriate to attempt to assess the proportion of Hyalomma spp. ticks originating from Africa where CCHFV is endemic in certain countries (Ergönül and Whitehouse 2007), relative to the proportion of ticks from southern European countries where CCHFV is not currently considered to be endemic. Southern Spain may act as a stopover site for migrating birds from Africa heading north into northern Europe and GB. In this respect, the rate at which Hyalomma spp. ticks drop off the birds during migration through Spain is an important factor. Furthermore, there is the possibility that Hyalomma spp. ticks from Africa may drop off in southern Spain, to be replaced by ticks indigenous to southern Europe. Thus, the rate at which Hyalomma spp. ticks contact migratory birds in southern Europe during stopovers is important. The duration and location of the stopover in southern Europe may be key factors affecting "tick exchange," i.e., where African ticks are replaced by European ticks. Thus, data on the tick infestation rates on migratory birds in southern Spain may permit greater understanding of tick exchange and the origin of ticks arriving in GB and northern Europe. The Hyalomma spp. infestation rate is defined as the percentage of migratory birds that carry Hyalomma spp. ticks. A previous study in April-May, 2011 found the Hyalomma spp. infestation rate of migratory birds in southern Spain to be 0.5% (Foley-Fisher et al. 2012). This paper reports the results of a second study conducted at the same trapping sites in southern Spain in April-May, 2012 to measure the numbers of Hyalomma spp. ticks on migratory birds along the East Atlantic flyway. In addition, these data are collated with data from other published studies to investigate how the faunal composition of ticks on birds varies with latitude. This may promote our understanding of tick exchange as the birds move northwards. MATERIALS AND METHODS Birds were trapped in mist nets between 22 April and 16 May 2012 at seven sites in the provinces of Malaga and Cadiz, southern Spain. The site locations were selected from existing bird ringing sites used by the local ringing group and represent various habitat types such as montane, coastal, riverine, and heathland. Birds were caught between 06:00-14:00 and between 16:00-18:00, and each bird captured was identified to species and aged. Birds were classified as either residents or migrants using the method described in Foley-Fisher et al. (2012). Only long-range migrants who winter in southern Europe or Africa were included in the analysis. For the purposes of this study, short-range migrants were classified as resident birds. Birds were then checked for ticks in the ears, eyes, beak, gape, nape, and abdomen and these were removed and stored as described previously (Foley-Fisher et al. 2012). The ticks were aged and identified morphologically to genus (and species in the case of Hyalomma spp. ticks) using the method of Estrada-Peña et al. (2004) and A. Bouattour (personal communication). Each Hyalomma spp. tick collected was homogenized using PreCellys 24 with RNA extraction performed using the Qiagen RNeasy Mini kit. Extractions were tested for CCHFV using the real-time RT-PCR method developed by Atkinson et al. (2012). The Hyalomma spp. infestation rate for migratory birds was compared to that obtained previously for the East Atlantic flyway in the 2011 study and to data for the Central and Eastern Mediterranean flyway (Wallmenius et al. 2014). Tick infestation rates at different latitudes during the spring migration were then investigated by collating data from previous studies carried out along the East Atlantic flyway and Central and Eastern Mediterranean flyway. To test whether the tick counts per bird are Poisson distributed, the dispersion statistic was calculated as ns2/sample mean where n is the number of birds sampled and s2 is the sample variance (as described by Gale et al. 2002). The dispersion statistic is then compared with the tabulated value of c2 with (n–1) degrees of freedom. The hypothesis that counts are Poisson distributed is rejected if the dispersion statistic exceeds the upper 5% point of c2 in the statistical tables. RESULTS Ticks recovered from birds in southern Spain in April-May, 2012 A total of 564 birds was caught in mist nets and checked for ticks. A total of 65 ticks was collected from 26 individual birds representing 4.6% of birds caught (Table 1). Of the 564 birds caught, 228 were migrants, of which five birds were infested with a total of 11 H. marginatum nymphs and one H. marginatum larva, giving a Hyalomma spp. infestation rate for migratory birds of 2.2% (with 95% binomial confidence interval of 0.7% – 5.0%). When this 2.2% Hyalomma spp. infestation rate for migratory birds was compared to that of 0.5% (95% binomial confidence interval of 0.01% – 2.7%) found in the 2011 study (Foley-Fisher et al. 2012) using Fisher's exact test, the difference was not significant statistically (p = 0.22). All 12 H. marginatum ticks collected from birds in this study tested negative for CCHFV. Table 1. Birds trapped that were infested with ticks in southern Spain during springtime migration, 2012. An additional 329 birds of 42 different species were also caught, but none were found to be infested with ticks. Species Family Resident (R) or Migrant (M) species No. of birds No. of ticks No. of birds infested Mean no. of ticks /infested bird Mean no. of larvae /infested bird Mean no. of nymphs /infested bird Mean no. of adults /infested bird Genus of ticks Acrocephalus schoenobaenus Acrocephalidae M 8 5 1 5 0 5 0 Hyalomma Carduelis carduelis Fringillidae R 22 1 1 1 0 1 0 Ixodes Chloris chloris Fringillidae R 36 31 10 3.1 0.2 2.9 0 Ixodes Fringilla coelebs Fringillidae R 10 1 1 1 0 1 0 Ixodes Iduna opaca Acrocephalidae M 8 1 1 1 0 1 0 Hyalomma Luscinia megarhynchos Muscicapidae M 43 1 1 1 1 0 0 Ixodes Parus major Paridae R 7 1 1 1 0 1 0 Ixodes Phylloscopus trochilus Phylloscopidae M 10 1 1 1 1 0 0 Hyalomma Serinus serinus Fringillidae R 48 3 3 1 0 1 0 Ixodes Sylvia communis Sylviidae M 12 5 2 2.5 0 2.5 0 Hyalomma Turdus merula Turdidae R 31 15 4 3.75 0.5 3 0.25 Ixodes Comparison of tick infestation rates on birds within the Mediterranean The data collected in this study were combined with those collected in the 2011 study to give a mean Hyalomma spp. infestation rate for migratory birds of 1.4% for southern Spain. Wallmenius et al. (2014) did not specify the Hyalomma spp. infestation rate of migratory birds along the Central and Eastern Mediterranean flyway, but it has been estimated at 2.4% based on the data provided that 90% of collected ticks were identified as Hyalomma spp‥ The difference between the Hyalomma spp. infestation rate (2.4%) for the Central and Eastern Mediterranean flyway (Wallmenius et al. 2014) and the Hyalomma spp. infestation rate of the data for the East Atlantic flyway (1.4% from this study and Foley-Fisher et al. (2012) combined), was found to be statistically not significant using a c2 test with Yates' correction (p = 0.23). Statistical distribution of tick counts per bird The means, variances, and maxima are compared for tick counts per bird for Hyalomma and Ixodes spp. ticks in Table 2. Just one bird had one Ixodes spp. tick and no conclusions can be made on the statistical distribution of counts of Ixodes spp. ticks per bird. In contrast, five birds were infested with Hyalomma spp. ticks with one, one, one, four, and five ticks per bird. The dispersion statistic of 828 with 227 d.f. for the Hyalomma spp. counts has a remote probability of occurring if the counts were Poisson distributed, and it is concluded that the Hyalomma spp. tick counts are over-dispersed compared to the Poisson distribution. Table 2. Statistics for recorded tick counts per bird for Hyalomma and Ixodes spp. ticks. Tick genus Number of birds sampled (n) Number of birds with at least one tick Maximum tick count recorded on an individual bird Mean number of ticks per bird () Variance (s2) Dispersion statistic (p*) Hyalomma 228 5 5 0.0526 0.1911 828 (0.00) Ixodes 228 1 1 0.0044 0.0044 228 (0.47) *Right-tailed probability of the c2 distribution with (n – 1) degrees of freedom. DISCUSSION The four bird species found to be carrying H. marginatum ticks in this study (A. schoenobaenus, I. opaca, P. trochilus, and S. communis) are migrants to Spain having wintered in sub-Saharan Africa. In general, these species prefer dry, open scrub and grassland habitats in their wintering areas (Hagemeijer and Blair 1997), although P. trochilus utilizes a wide range of other habitats (reviewed in Salewski and Jones (2006)), which concurs with the habitat preferences of Hyalomma spp. ticks. Hyalomma spp. ticks were not found on resident birds, despite Hyalomma spp. ticks being distributed widely in Spain (M. England, unpublished observations and A. Estrada-Pena, personal communication). Indeed, most of the Hyalomma spp. ticks removed from migratory birds in this study were semi- or fully-engorged nymphs, suggesting that the ticks had been present on the bird for one to two weeks. Although there is no information on the length of the stopover and how long each migrant had been in Spain prior to its being trapped, this would be consistent with most of the ticks originating from Africa. The difference in migratory bird infestation rates between years (i.e., 2011 and 2012) in southern Spain was not significant statistically. However, there are several factors that could influence the population size of Hyalomma spp. ticks in Africa, such as flooding, drought, predators, availability of hosts, and overwintering conditions, which could give rise to differences between years in the Hyalomma spp. infestation rate of migratory birds. Similarly, such factors could result in differences in tick infestation rates on birds in different regions of the Mediterranean during spring, although again the differences are not statistically significant. The statistical distribution of the number of Hyalomma spp. ticks per bird is over-dispersed compared to the Poisson distribution. The mean number of Hyalomma spp. ticks per bird is 0.53 (Table 2). If the Hyalomma spp. tick counts were Poisson distributed (mean = 0.53), then it would be expected that approximately 12 of the 228 birds would be infested, each with a single tick. The observed results show that only five of the 228 birds were infested. The percentage of birds being infested with four or more Hyalomma spp. ticks, if they were Poisson distributed (mean = 0.53), would be negligible at <0.00001%. The observed results, however, revealed two birds (i.e., almost 1%) having four and five ticks each. The consequence of over-dispersion is that more birds have zero ticks, but the few that are infested carry higher numbers than if counts were randomly distributed according to the Poisson distribution. This skewed distribution has sampling implications for detecting Hyalomma spp. ticks on birds. Thus, to avoid underestimating the arithmetic mean infestation rate, large numbers of birds need to be sampled to increase the chance of detecting the rare individuals carrying a high number of ticks. Estrada-Peña and de la Fuente (2014) also reported that the statistical distribution for the number of ticks per host animal is skewed and fitted a negative binomial distribution. The origin of this skewed distribution is not clear but could reflect heterogeneous distributions of ticks on the ground such that some birds are more heavily infested. The presence of CCHFV-infected Hyalomma spp. ticks on migratory birds in Morocco (Palomar et al. 2012), along with the finding of Hyalomma spp. ticks on migratory birds travelling northward in Spain, have implications for the risk of CCHFV entry into GB. Jameson et al. (2012) confirmed that Hyalomma spp. ticks enter GB on migratory birds, although it is not known if these were picked up in southern Europe or sub-Saharan Africa. It is also not known for how long these ticks are able to survive in the UK following detachment from migratory birds. The statistically significant decrease in the Hyalomma spp. tick infestation rate between the study sites in Morocco (Palomar et al. 2012) and southern Spain (Foley-Fisher et al. 2012) during simultaneous trapping in 2011 (3.85% and 0.5%, respectively; p = 0.01) suggests Hyalomma spp. ticks may detach prior to leaving Africa, or soon after arriving in Europe. Due to the long period of attachment (two to three weeks), ticks on migratory birds in southern Europe may have originated from sub-Saharan Africa, while those on birds entering northern Europe may be more likely to have originated from North Africa or southern Spain. However, the speed and duration of bird migration varies between individuals and species, with P. trochilus covering the distance between Finland and South Africa in 47 days (Hedenström and Pettersson 1987). It is, therefore, less likely, although still possible, for Hyalomma spp. ticks of more southerly origins to be carried far into northern Europe. Published data on infestation rates of migratory birds by Hyalomma spp. ticks and by Ixodes spp. Ticks at varying latitudes are collated in Table 3 and plotted in Figure 1. The Hyalomma spp. infestation rate decreases with increasing latitude while that for Ixodes spp. increases, suggesting a "tick exchange" with Hyalomma spp. ticks detaching from birds and Ixodes spp. ticks being acquired by birds as they migrate north. This reflects the geographical distribution of these tick genera, with Hyalomma spp. being more abundant in Africa and southern Europe and Ixodes spp. being the predominant genus in northern Europe. For Ixodes spp., the increase in infestation rate reverses at around 58°N which may be due to a lower abundance of ticks in the far north of Europe, where colder climates limit development rates. Indeed, there is a northern limit for Ixodes spp. in Fennoscandia (Medlock et al. 2013). It may be that Hyalomma spp. ticks on birds in southern and central Europe originate from Africa, while those on birds in northern Europe are more likely to originate from populations of Hyalomma spp. ticks in southern Europe, in particular from southern Spain. However, the African tick species, H. rufipes, has been found on migratory birds in southern Norway (Hasle et al. 2009), demonstrating that ticks can be carried from Africa to northern Europe. It is important for CCHFV risk assessment to consider what drives tick detachment during or following migration or, indeed, whether this is an entirely random process. Hyalomma spp. ticks use visual cues to hunt hosts and, therefore, may detach from birds on the ground rather than in flight. Figure 1Open in figure viewerPowerPoint Infestation rates of migratory birds with Hyalomma spp. ticks and Ixodes spp. ticks with changing latitude. Data from this study, combined with those of Foley-Fisher et al. (2012), are shown in red. For some studies, the infestation rates represent an average across more than one trapping site and so the points are represented at the average latitude for each study. Table 3. Evidence for tick exchange as birds migrate northwards. The species of tick infesting migratory birds is also detailed where these data are available. Study location (Reference) Latitude Hyalomma spp. infestation rate Ixodes spp. infestation rate Egypt (Hoogstraal et al. 1961) 29.31°N (Faiyum) 30.02°N (Giza) 30.05°N (Cairo) 13.3% (128/959 migratory birds; H. rufipes) 0% (0/959 migratory birds) Egypt (Hoogstraal et al. 1964) 30.84°N (Borg El Arab) 3.04% (54/1774 migratory birds; H. rufipes) 0.11% (2/1774 migratory birds) Morocco (Palomar et al. 2012) 31.79°N (Zouala) 3.85% (21/546 migratory birds; H. marginatum) 0% (0/546 migratory birds) Cyprus (Kaiser et al. 1974) 35.03°N 0.78% (172/22015 migratory birds; H. rufipes) 0.03% (6/22015 migratory birds; Ixodes eldaricus Djaparidze; Ixodes frontalis Linneaus, Ixodes redikorzevi Olenev) Spain (Foley-Fisher et al. 2012 and this study) 36.12°N 1.4% (6/430 migratory birds; H. marginatum) 0.93% (4/430 migratory birds) Italy and Greece (Wallmenius et al. 2014) 35.86°N (Antikythira) 40.56°N (Capri) 2.4% (357/14789 migratory birds; H. marginatum, H. rufipes) 0.1% (15/14789 migratory birds; I. frontalis) Switzerland (Poupon et al. 2006) 46.17°N 3.57% (2/56 migratory birds; H. marginatum) 1.79% (1/56 migratory birds; I. ricinus) Czech Republic (Hubalek et al. 1996) 48.75°N (Valtice) 0% 18.4% (27/147 migratory birds; I. ricinus) Great Britain (Jameson et al. 2012) 50.55°N (Portland) 0.67% (6/898 migratory birds; H. marginatum) 5.12% (46/898 migratory birds; I. ricinus, I. frontalis) Norway (Hasle et al. 2009) 58.10°N (Lista) 58.87°N (Jomfruland) 59°05N (Akerøya) 59.07°N (Store Færder) 0.07% (7/9768 migratory birds; H. rufipes) 7.25% (708/9768 migratory birds; I. rinicus, I. frontalis, Ixodes arboricola Schulze & Schlottke Sweden and Denmark (Olsén et al. 1995) 55.32°N (Christiansø) 55.39°N (Falsterbo) 56.94°N (Sundre) 57.03°N (Nidingen) 58.74°N (Landsort) 60.73°N (Eggegrund) 63.80°N (Stora Fjäderägg) 65.60°N (Sanskär) 0.028% (3/10575 migratory birds; H. marginatum) 2.96% (313/10575 migratory birds; I. ricinus) Of the four migratory bird species found here to be carrying Hyalomma spp. ticks in southern Spain, three breed in Great Britain (A. schoenobaenus, P. trochilus, and S. communis) and, therefore, some of those birds in Spain would be expected to continue their migration north to GB. As shown in Figure 1, the Hyalomma spp. tick infestation rate falls to <1% in migratory birds at GB latitudes, with the possibility that some of those Hyalomma spp. ticks entering GB may have been acquired by the birds in southern Europe rather than in Africa. Taken overall, the data reported here, together with predictions from previous studies (e.g., Gale et al. (2012)), suggest an extremely low, but non-negligible, risk of introduction of CCHFV into GB through Hyalomma spp. ticks on migratory birds. The identification of possible tick exchange with latitude through the published data collated here is important in refining this risk estimate. This paper highlights the need for continued monitoring of tick populations in the field to inform risk assessment for CCHFV entry into northern Europe. In particular, future work should focus on understanding what drives the over-dispersed statistical distribution of the number of ticks on migratory birds together with where birds acquire and drop Hyalomma spp. ticks. Acknowledgments We thank Richard Banham, Louise Kelly, Andrew Hill, and Robin Simons for their contributions to this study. We also thank Dr. Ali Bouattour of the Institut Pasteur, Tunis, for his help with tick identification. PMA is grateful to the University of Utrecht for supporting him with The Belle van Zuylen Chair. This study was funded as part of a Ph.D. studentship at the Animal and Plant Health Agency and Public Health England. REFERENCES CITED 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: 786– 793. Ergönül, Ö. and C.A. Whitehouse. 2007. Crimean Congo Haemorrhagic Fever: A Global Perspective. Springer. Estrada-Peña, A., A. Bouattour, J.L. Camicas, and A.R. Walker. 2004. Ticks of Domestic Animals in the Mediterranean Region: A Guide to Idenitification of Species. Netherlands: University of Zaragoza. Estrada-Peña, A., and J. de la Fuente. 2014. The ecology of ticks and epidemiology of tick-borne viral diseases. Antivir. Res. 108: 104– 128. 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: 179– 180. Foley-Fisher, M., P. Phipps, J.M. Medlock, P.M. Atkinson, B. Atkinson, R. Hewson, and P. Gale. 2012. Ticks on northward migrating birds in southern Spain during Spring, 2011. J. Vector Ecol. 37: 478– 480. Gale, P., R. Pitchers, and P. Gray. 2002. The effect of drinking water treatment on the spatial heterogeneity of micro-organisms: implications for assessment of treatment efficiency and health risk. Water Res. 36: 1640– 1648. Gale, P. and G. Stanfield. 2000. Cryptosporidium during a simulated outbreak. J. Am. Water Works Assoc. 92: 105– 116. Gale, P., B. Stephenson, A. Brouwer, M. Martinez, A. de la Torre, M. Bosch, M. Foley-Fisher, P. Bonilauri, A. Lindström, R.G. Ulrich, C.J. de Vos, M. Scremin, Z. Liu, L. Kelly, and M.J. Muñoz. 2012. Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds. J. Appl. Microbiol. 112: 246– 257. Hagemeijer, W.J.M. and M.J. Blair. 1997. The EBCC Altas of European Breeding Birds: Their Distribution and Abundance. T & AD Poyser, London. Hasle, G., G. Bjune, E. Edvardsen, C. Jakobsen, B. Linnehol, J.E. Røer, R. Mehl, K.H. Røed, J. Pedersen, and H.P. Leinaas. 2009. Transport of ticks by migratory passerine birds to Norway. J. Parasitol. 95: 1342– 1351. Hedenström, A., and J. Pettersson. 1987. Migration routes and wintering areas of Willow Warblers Phylloscopus trochilus (L.) ringed in Fennoscandia. Ornis Fenn. 64: 137– 143. Hoogstraal, H. 1972. Birds as tick hosts and as reservoirs and disseminators of tickborne infectious agents. Wiad. Parazytol. 18: 703– 706. Hoogstraal, H. 1979. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe and Africa. J. Med. Entomol. 15: 307– 417. Hoogstraal, H., M.N. Kaiser, M.A. Traylor, S. Gaber, and E. Guindy. 1961. Ticks (Ixodoidae) on birds migrating from Africa to Europe and Asia. Bull. World Hlth. Org. 24: 197– 212. 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: 355– 367. Hubalek, Z., J. F. Anderson, J. Halouzka, and V. Hajek. 1996. Borreliae in immature Ixodes ricinus (Acari: Ixodidae) ticks parasitizing birds in the Czech Republic. J. Med. Entomol. 33: 766– 771. 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: 95– 99. Kaiser, M.N., H. Hoogstraal and G. E. Watson. 1974. Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bull. Entomol. Res. 64: 97– 110. Lindeborg, M., C. Barboutis, C. Ehrenborg, T. Fransson, T.G.T. Jaenson, P.-E. Lindgren, Å. Lundkvist, F. Nyström, E. Salaneck, J. Waldenström, and B. Olsen. 2012. Migratory birds, ticks, and Crimean-Congo hemorrhagic fever virus Emerg. Infect. Dis. 18: 2095– 2097. Martyn, K.P. 1988. Provisional Atlas of the Ticks (Ixodoidea) of the British Isles. Cumbria: Institute of Terrestrial Ecology. Medlock, J.M., K.M. Hansford, A. Bormane, M. Derdakova, A. Estrada-Pena, J.-C. George, I. Golovljova, T.G.T. Jaenson, J.-K. Jensen, P.M. Jensen, M. Kazimirova, J.A. Oteo, A. Papa, K. Pfister, O. Plantard, S.E. Randolph, A. Rizzoli, M.M. Santos-Silva, H. Sprong, L. Vial, G. Hendrickx, H. Zeller, and W. Van Bortel. 2013. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites Vectors 6: 1. 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: 5997. Olsén, B., T.G. Jaenson, and S. Bergström. 1995. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl. Environ. Microbiol. 61: 3082– 3087. Palomar, A.M., A. Portillo, P. Santibáñez, D. Mazuelas, J. Artzaga, A. Crespo, Ó. Gutiérrez, J.F. Cuadrado and J.A. Oteo. 2012. Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg. Infect. Dis. 19: 260– 263. Poupon, M.-A., E. Lommano, P.-F. Humair, V. Douet, O. Rais, M. Schaad, L. Jenni, and L. Gern. 2006. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl. Environ. Microbiol. 72: 976– 979. Salewski, V. and P. Jones. 2006. Palearctic passerines in Afrotropical environments: a review. J. Ornithol. 147: 192– 201. Vorou, R.M. 2009. Crimean-Congo hemorrhagic fever in southeastern Europe. Int. J. Infect. Dis. 13: 659– 662. Wallmenius, K., C. Barboutis, T. Fransson, T.G.T. Jaenson, P.-E. Lindgren, F. Nystrom, B. Olsen, E. Salaneck, and K. Nilsson. 2014. Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasites Vectors 7: 318. Whitehouse, C.A. 2004. Crimean-Congo hemorrhagic fever. Antivir. Res. 64: 145– 160. Citing Literature Volume41, Issue1June 2016Pages 128-134 FiguresReferencesRelatedInformation