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First record of Hyalomma rufipes in the Czech Republic, with a review of relevant cases in other parts of Europe

Hubálek, Z.; Vojtíšek, J.; Sedlácek, P.; Rudolf, I.; Estrada-Peña, A.

Abstract

We found a male Hyalomma rufipes Koch, 1844 tick feeding on a horse grazing near Valtice, south Moravia, Czech Republic on October 24, 2019. The horse was born in Czechland and did not leave the country at least during the last five years. Relevant findings of Hyalomma ticks in other parts of central Europe are reviewed, including also records of pre-imaginal Hyalomma marginatum complex ticks on migrating birds all over Europe. Hubálek, Z.; Sedlácek, P.; Estrada-Peña, A.; Vojtíšek, J.; Rudolf, I.

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Jou nal P e-p oo Fi s eco d o Hyalomma ufipes in he Czech Republic, wi h a e iew o ele an cases in o he pa s o Eu ope Zdenek Hub´ alek (Concep ualiza ion) (In es iga ion) (Fo mal analysis) (W i ing - o iginal d a ) (W i ing - e iew and edi ing), Pa el Sedl´ aˇ cek, Agus ´ ın Es ada-Pe˜ na (In es iga ion) (Me hodology) (W i ing - e iew and edi ing) (Concep ualiza ion) (Valida ion), Jakub Voj ´ ıˇ sek (Me hodology), I o Rudol (Concep ualiza ion) (W i ing - o iginal d a ) (W i ing - e iew and edi ing) PII: S1877-959X(19)30512-6 DOI: h ps://doi.o g/10.1016/j. bdis.2020.101421 Re e ence: TTBDIS 101421 To appea in: Ticks and Tick-bo ne Diseases Recei ed Da e: 2 Decembe 2019 Re ised Da e: 23 Janua y 2020 Accep ed Da e: 21 Ma ch 2020 Please ci e his a icle as: {doi: h ps://doi.o g/ This is a PDF file o an a icle ha has unde gone enhancemen s a e accep ance, such as he addi ion o a co e page and me ada a, and o ma ing o eadabili y, bu i is no ye he defini i e e sion o eco d. This e sion will unde go addi ional copyedi ing, ypese ing and e iew be o e i is published in i s final o m, bu we a e p o iding his e sion o gi e ea ly isibili y o he a icle. Please no e ha , du ing he p oduc ion p ocess, e o s may be disco e ed which could a ec he con en , and all legal disclaime s ha apply o he jou nal pe ain. © 2020 Published by Else ie . 1 "Ticks and Tick-bo ne Diseases" Sho Communica ion Fi s eco d o Hyalomma u ipes Koch, 1844 in he Czech Republic, wi h a e iew o ele an cases in o he pa s o Eu ope Zdenek Hubálek1, Pa el Sedláček2, Agus ín Es ada-Peña3, Jakub Voj íšek1, I o Rudol 1 1Ins i u e o Ve eb a e Biology, Czech Academy o Sciences, 60365 B no, Czech Republic 2P o ec ed Landscape A ea "Pala a", Mikulo , Czech Republic 3Depa men o Pa asi ology, Facul y o Ve e ina y Medicine, 500-13 Za agoza, Spain Abs ac We ound a male Hyalomma u ipes Koch, 1844 ick eeding on a ho se g azing nea Val ice, sou h Mo a ia, Czech Republic on Oc obe 24, 2019. The ho se was bo n in Czechland and did no lea e he coun y a leas du ing he las i e yea s. Rele an indings o Hyalomma icks in o he pa s o cen al Eu ope a e e iewed, including also eco ds o p e-imaginal Hyalomma ma gina um complex icks on mig a ing bi ds all o e Eu ope. Keywo ds: Hyalomma ma gina um; Czechland; cen al Eu ope; ho se; mig a o y bi ds In oduc ion Hyalomma icks a e impo an ec o s o se e al pa hogenic agen s, e.g. C imean-Congo hemo hagic e e (CCHF) i us, Thogo o i us, Dho i i us, Wes Nile i us, Bhanja i us, Ricke sia cono ii, R. aeschlimannii, Anaplasma ma ginale, Theile ia annula a, Babesia caballi (Hoogs aal, 1979; Hubálek and Rudol , 2011; Bakhei e al., 2012). Finding Jou nal P e-p oo 2 We ound an adul Hyalomma ick eeding on he hind limb (close o he anal egion, unde ail) o a ho se (Czech wa mblooded ace, 24 yea s old) g azed a ishpond "Nesy " (48º.766 N, 16º.727 E) nea Val ice, dis ic Břecla (sou h Mo a ia, Czech Republic) on Oc obe 24, 2019. The ho se was bo n in he Czech egion called Czech-Mo a ian Highland and i did no lea e Czech Republic a leas du ing he las i e yea s. The animal egula ly g azed du ing he season and c ossed an a ea be ween he owns Val ice and Mikulo (dis ance o c. 10 km), e y close o he Czech-Aus ian bo de . The sampled ick was anspo ed o he labo a o y and iden i ied unde s e eomic oscope. The ick was ound o be a pa ially ed male o Hyalomma u ipes Koch, 1844, based on he mo phology o spi acula pla e and he se ae a ound i ha di e en ia e his species om he closely ela ed H. ma gina um Koch, 1844. P e iously, hese wo axa we e ega ded as wo subspecies o H. ma gina um complex, i.e., H. ma gina um ma gina um and H. ma gina um u ipes, bu ha e been aised o ull species s a us (Apanaske ich and Ho ak, 2008). The ick H. u ipes has ne e been eco ded in he Czech Republic be o e, ei he in p e-imaginal o adul s age. In e es ingly, one o us (P. S.) obse ed a simila , inge nail-sized adul ick wi h i o y- colou ed bands on long legs (which could be in e p e ed as an adul Hyalomma) on hind limb o a ho se in he same locali y also on Augus 21, 2018, bu he ick escaped and could no be examined in de ail. Discussion (a mini- e iew) We sea ched li e a u e o eco ds on adul Hyalomma ma gina um complex p esence in cen al Eu ope. These adul icks we e eco ded (Table 1) in Slo akia (a emale climbing on man's clo hes, 21 Augus 1981: Nosek e al., 1982), Ge many (Kampen e al., 2007; Chi imia- Doble e al., 2016, 2019; Oehme e al., 2017), Hunga y (Ho nok and Ho a h, 2012), Poland (Cube , 2016) and Aus ia (Dusche e al., 2018). Among hem, adul H. u ipes was de ec ed p e iously only in Hunga y and Ge many. Chi imia-Doble e al. (2019) concluded: "These esul s show ha exo ic ick species impo ed in o Ge many we e able o de elop om he nymphal o he adul s age" which may be alid o he whole cen al Eu ope. Ou side cen al Eu ope, Hans o d e al. (2019) ound an adul H. u ipes on a ho se in England (Do se ), 2018. Jou nal P e-p oo 3 The mos p obable mechanism o in oduc ion o he H. u ipes ick in o he Czech Republic could be he anspo as a la a o nymph on a mig a o y bi d, wi h he moul ing in o adul s age in sou h Mo a ia. Ha y Hoogs aal and his co-wo ke s we e he i s who s udied he po en ial o mig a o y bi ds o ca y ixodid icks, ec o s o se e al in ec ious agen s, on a wide geog aphic scale (Hoogs aal, 1967; Kaise e al., 1974; Nuo e a and Hoogs aal, 1963). Fo ins ance, Kaise e al. (1974) examined 20,528 bi ds mig a ing no hwa d in Cyp us du ing sp ing 1968. They ound 177 bi ds o be in es ed, mos o en by H. u ipes (217 la ae and 540 nymphs). Hasle e al. (2009) cap u ed bi ds mig a ing along he sou he n coas line o No way. They ound icks on 4.2%-6.9% o he bi ds, and wi h se en nymphs iden i ied as H. u ipes. The e we e many eco ds o la al and nymphal H. ma gina um complex on mig a ing bi ds a i ing in o Eu ope in he sp ing (Table 2). In he Czech Republic, h ee nymphs o H. ma gina um we e collec ed on wo T ee Pipi s (An hus i ialis) nea Val ice, 8 Ap . 1953; one nymph o H. ma gina um on a Blue h oa (Luscinia s ecica cyanecula) a Hodonín, 1 Ap . 1953 (Če ný and Balá , 1957). Čapek e al. (2014) collec ed a numbe o la al and nymphal H. ma gina um complex icks on mig a o y bi ds in cen al Mo a ia and eas e n Bohemia du ing he sp ings 2010-2012: in es ed a ian hos species we e G ea Reed Wa ble (Ac ocephalus a undinaceus), Eu asian Reed Wa ble (A. sci paceus), Ma sh Wa ble (A. palus is), Sedge Wa ble (A. schoenobaenus), Sa i's Wa ble (Locus ella luscinioides) and Common Nigh ingale (Luscinia mega hynchos). I aly is a e y impo an mig a o y ou e o many species o bi ds b eeding in cen al Eu ope, and he indings o bi ds ca ying Hyalomma imma u es a e he e well documen ed. Fo ins ance, Mancini e al. (2013) and Toma e al. (2014) collec ed icks on mig a o y bi ds in cen al I aly wi hin o ni hological su eys ca ied ou in 2010 and 2011. A o al o 137 icks we e collec ed om 41 mig a o y bi ds belonging o 17 species. Mos icks we e nymphs, wi h a p edominance o H. ma gina um and H. u ipes. De Libe a o e al. (2018) su eyed mig a o y bi ds o icks in 13 inging si es o Cen al and Sou he n I aly. A o al o 50,325 bi ds we e checked and 0.22% we e in es ed by Hyalomma spp., in ol ing 22 a ian species wi h a mean numbe o 1.6 Hyalomma ick pe in es ed bi d. The high p opo ion o Hyalomma icks indica es a po en ial isk o he dissemina ion o ick-bo ne pa hogens h ough in es ed mig a o y bi ds. In addi ion o bi ds and in e es ingly, Föld á i e al. (2011) eco ded one nymphal H. ma gina um eeding on hedgehog (E inaceus oumanicus) in he Budapes cen al ci y pa k. Jou nal P e-p oo 4 Conclusion Ou inding o one adul H. u ipes a ached o a hos does no mean ha his ick species has been es ablished in he Czech Republic. Bu conside ing he ac ha H. u ipes is an e icien ec o o , e.g., CCHF i us (Hoogs aal, 1979), he igilance o Hyalomma icks and hei su eillance o exo ic pa hogenic agen s in Eu ope is ecommendable. C edi Au ho S a emen ZH: Concep ualiza ion, In es iga ion, Fo mal analysis, O iginal d a wei ing, e iew and edi ing PS: Ma e ial, Tick sampling AEP: In es iga ion, Me hodology, W i ing ( e iew and edi ing), Concep ualiza ion, Valisa ion JV: Me hodology, Documen a ion IR: Concep ualiza ion, O iginal d a wei ing, e iew and edi ing Compe ing in e es None. Acknowledgmen We a e g a e ul o D . Dmi y A. Apanaske ich (Uni ed S a es Na ional Tick Collec ion, Geo gia Sou he n Uni e si y, S a esbo o, GA, U.S.A.) o his signi ican help wi h iden i ica ion o he ick specimen. Jou nal P e-p oo 5 Re e ences Apanaske ich, D.A., Ho ak, I.G., 2008. 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