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Host specificity of a bird-specialised endophilic ectoparasite, the tree-hole tick Ixodes arboricola

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Abstract

Host specialisation in parasites can be due to either limited exposure or limited adaptation to different host types. When the first barrier is lifted experimentally, the degree of adaptive specialisation can be studied. The tree-hole tick Ixodes arboricola is an endophilic parasite with a narrow host range, found in nest boxes used mainly by great and blue tits (Parus major, Cyanistes caeruleus) and to a lesser extent by pied flycatchers (Ficedula hypoleuca) and nuthatches (Sitta europaea). In the current study, we exposed two nestlings per nestbox of pied flycatchers (N = 14), blue tits (N = 18), great tits (N = 14), and nuthatches (N = 16) to ten I. arboricola nymphs each. We found no differences in attachment success 2 days after infestation (56 ± 4 % across species) nor were there any differences in tick engorgement weight (1.95 ± 0.03 mg across species), and moulting success was >90 % for ticks from all bird species. Hence, our data suggest that all bird species investigated here are suitable host species. This may enhance the ticks’ chances for persistence in cavities and dispersal among cavities inhabited by multiple host species, and supports the hypothesis that host use by ticks is limited by host ecology rather than by host specialisation.

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References

  • Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using Eigen and S4

  • Dhondt AA (2010) Effects of competition on great and blue tit reproduction: intensity and importance in relation to habitat quality. J Anim Ecol 79:257–265. doi:10.1111/j.1365-2656.2009.01624.x

    Article  PubMed  Google Scholar 

  • Dietrich M, Lobato E, Boulinier T, McCoy KD (2013) An experimental test of host specialization in a ubiquitous polar ectoparasite: a role for adaptation? J Anim Ecol. doi:10.1111/1365-2656.12170

    PubMed  Google Scholar 

  • Drès M, Mallet J (2002) Host races in plant–feeding insects and their importance in sympatric speciation. Philos Trans R Soc B 357:471–492. doi:10.1098/rstb.2002.1059

    Article  Google Scholar 

  • Fargallo JA, Johnston RD (1997) Breeding biology of the blue Tit Parus caeruleus in a montane Mediterranean deciduous forest: the interaction of latitude and altitude. J Fur Ornithol 138:83–92. doi:10.1007/bf01651654

    Article  Google Scholar 

  • Giorgi MS, Arlettaz R, Guillaume F et al (2004) Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138:648–654. doi:10.1007/s00442-003-1475-1

    Article  PubMed  Google Scholar 

  • Gómez-Díaz E, Morris-Pocock JA, González-Solís J, McCoy KD (2012) Trans-oceanic host dispersal explains high seabird tick diversity on Cape Verde islands. Biol Lett 8:616–619. doi:10.1098/rsbl.2012.0179

    Article  PubMed Central  PubMed  Google Scholar 

  • Gosler A (1993) The great tit. Hamlyn, London

    Google Scholar 

  • Heylen DJA, Matthysen E (2010) Contrasting detachment strategies in two congeneric ticks (Ixodidae) parasitizing the same songbird. Parasitology 137:661–667. doi:10.1017/s0031182009991582

    Article  CAS  PubMed  Google Scholar 

  • Heylen DJA, Matthysen E (2011) Differential virulence in two congeneric ticks infesting songbird nestlings. Parasitology 138:1011–1021. doi:10.1017/S0031182011000618

    Article  PubMed  Google Scholar 

  • Heylen DJA, Tijsse E, Fonville M et al (2013) Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol 29:663–673. doi:10.1111/1462-2920.12059

    Article  Google Scholar 

  • Heylen DJA, Van Oosten AR, Devriendt N et al (2014) Seasonal feeding activity of the tree-hole tick, Ixodes arboricola. Parasitology. doi:10.1017/S0031182014000225

    PubMed  Google Scholar 

  • Hillyard PD (1996) Ticks of north-west Europe: keys and notes for identification of the species. Published for the Linnean Society of London and the Estuarine and Coastal Sciences Association by Field Studies Council

  • Hoogstraal H, Aeschlimann A (1982) Tick-host specificity. Bull la Soc Entomol Suisse 55:5–32

    Google Scholar 

  • Hudde H, Walter G (1988) Verbreitung und Wirtswahl der Vogelzecke Ixodes arboricola. Vogelwarte 34:201–207

    Google Scholar 

  • Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92. doi:10.1007/bf01237699

    Article  Google Scholar 

  • Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190. doi:10.1046/j.1420-9101.2002.00377.x

    Article  Google Scholar 

  • Kempf F, De Meeus T, Vaumourin E et al (2011) Host races in Ixodes ricinus, the European vector of Lyme borreliosis. Infect Genet Evol 11:2043–2048. doi:10.1016/j.meegid.2011.09.016

    Article  PubMed  Google Scholar 

  • Klompen JSH, Black WC IV, Keirans JE, Oliver JH Jr (1996) Evolution of ticks. Annu Rev Entomol 41:141–161. doi:10.1146/annurev.en.41.010196.001041

  • Labruna MB, Souza SLP, Menezes AC et al (2002) Life-cycle and host specificity of Amblyomma tigrinum (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 26:115–125. doi:10.1023/A:1020957122256

  • Labruna MB, Cabrera RR, Pinter A (2009) Life cycle of Ixodes luciae (Acari: Ixodidae) in the laboratory. Parasitol Res 105:1749–1753. doi:10.1007/s00436-009-1621-8

    Article  PubMed  Google Scholar 

  • Legros M, Koella JC (2010) Experimental evolution of specialization by a microsporidian parasite. BMC Evol Biol 10:1471–2148. doi:10.1186/1471-2148-10-159

  • Liebisch G (1996) Biology and life cycle of Ixodes (Pholeoixodes) arboricola Schulze and Schlottke, 1929 (Ixodidae). In: Mitchell R, Hom DJ, Glen RN, Welboum WC (eds) Acarol. IX Vol. 1 Proc. Ohio Biological Survey, Columbus, OH, USA, pp 453–455

  • Lundberg A, Alatalo RV (1992) The pied flycatcher. Academic, San Diego

    Google Scholar 

  • Magalhães S, Forbes MR, Skoracka A et al (2007) Host race formation in the Acari. Exp Appl Acarol 42:225–238. doi:10.1007/s10493-007-9091-0

    Article  PubMed  Google Scholar 

  • Mainwaring MC (2011) The use of nestboxes by roosting birds during the non-breeding season: a review of the costs and benefits. Ardea 99:167–176. doi:10.5253/078.099.0206

    Article  Google Scholar 

  • Martins TF, Moura M, Labruna MB (2012) Life-cycle and host preference of Amblyomma ovale (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 56:151–158. doi:10.1007/s10493-011-9506-9

    Article  PubMed  Google Scholar 

  • Matthysen E (1998) The nuthatches. Academic, San Diego

    Google Scholar 

  • Mccoy KD, Boulinier T (2002) Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evol Ecol Res 4:441–456

    Google Scholar 

  • McCoy KD, Boulinier T, Tirard C, Michalakis Y (2001) Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. J Evol Biol 14:395–405. doi:10.1046/j.1420-9101.2001.00290.x

    Article  Google Scholar 

  • McCoy KD, Léger E, Dietrich M (2013) Host specialization in ticks and transmission of tick-borne diseases: a review. Front Cell Infect Microbiol. doi:10.3389/fcimb.2013.00057

    PubMed Central  PubMed  Google Scholar 

  • Nava S, Guglielmone AA (2013) A meta-analysis of host specificity in Neotropical hard ticks (Acari: Ixodidae). Bull Entomol Res 103:216–224. doi:10.1017/S0007485312000557

    Article  CAS  PubMed  Google Scholar 

  • Olegário MMM, Gerardi M, Tsuruta SA, Szabó MPJ (2011) Life cycle of the tick Amblyomma parvum Aragão, 1908 (Acari: Ixodidae) and suitability of domestic hosts under laboratory conditions. Vet Parasitol 179:203–208. doi:10.1016/j.vetpar.2011.01.056

    Article  PubMed  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

  • R Core Team (2013) R: a language and environment for statistical computing.

  • Rotolo F, Munda M (2013) Parfm: parametric frailty models in R. J Stat Softw 51:1–20

    Google Scholar 

  • Salman MD, Tarrés-Call J (2012) Ticks and tick-borne diseases: geographical distribution and control strategies in the Euro-Asia Region. CAB International, Wallingford

  • Sears BF, Schlunk AD, Rohr JR (2012) Do parasitic trematode cercariae demonstrate a preference for susceptible host species? PLoS One 7:e51012. doi:10.1371/journal.pone.0051012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sonenshine DE (1991) Biology of ticks. Oxford University Press, Oxford

    Google Scholar 

  • Špitalská E, Literák I, Kocianová E, Taragel’ová V (2011) The importance of Ixodes arboricola in transmission of Rickettsia spp., Anaplasma phagocytophilum, and Borrelia burgdorferi sensu lato in the Czech Republic, central Europe. Vector-Borne Zoonotic Dis 11:1235–1241. doi:10.1089/vbz.2010.0210

    Article  PubMed  Google Scholar 

  • Timms R, Read AF (1999) What makes a specialist special? Trends Ecol Evol 14:333–334. doi:10.1016/s0169-5347(99)01697-3

    Article  PubMed  Google Scholar 

  • Tripet F, Richner H (1997) The coevolutionary potential of a “generalist” parasite, the hen flea Ceratophyllus gallinae. Parasitology 115:419–427. doi:10.1017/s0031182097001467

    Article  PubMed  Google Scholar 

  • Vermeersch G, Anselin A, Devos K, et al. (2004) Atlas van de Vlaamse broedvogels 2000–2002. Mededelingen van het Instituut voor Natuurbehoud 23, Brussel

  • Walter G, Liebisch A, Streichert J (1979) Untersuchungen zur Biologie und Verbreitung von Zecken (Ixodoidea, Ixodidae) in Norddeutschland. Angew Ornithol 5:65–73

    Google Scholar 

  • White J, Heylen DJA, Matthysen E (2012) Adaptive timing of detachment in a tick parasitizing hole-nesting birds. Parasitology 139:264–270. doi:10.1017/s0031182011001806

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank F. J. B. Brosens, J. Elst and H. Pauwels for field assistance and the owners of Sterbos, Wuustwezel, for the permission to use this study area. This research was supported by FWO grant G.0049.10 to EM and an FWO postdoctoral fellowship to DJAH. The experimental protocol was approved by the Ethical Committee of the University of Antwerp and experiments on birds were licensed by the Agentschap voor Natuur en Bos.

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  1. University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    A. R. Van Oosten, D. J. A. Heylen & E. Matthysen

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  1. A. R. Van Oosten
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  2. D. J. A. Heylen
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  3. E. Matthysen
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Correspondence to A. R. Van Oosten.

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Van Oosten, A.R., Heylen, D.J.A. & Matthysen, E. Host specificity of a bird-specialised endophilic ectoparasite, the tree-hole tick Ixodes arboricola . Parasitol Res 113, 4397–4405 (2014). https://doi.org/10.1007/s00436-014-4116-1

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