Lack of resistance against the tick Ixodes ricinus in two related passerine bird species Dieter J.A. Heylen a, * , Maxime Madder b , Erik Matthysen a a Evolutionary Ecology Group, Department of Biology, University of Antwerp, Belgium b Department of Animal Health, Institute of Tropical Medicine, Antwerp, Belgium article info Article history: Received 30 March 2009 Received in revised form 17 June 2009 Accepted 10 July 2009 Keywords: Ixodes ricinus Songbird Resistance Tolerance abstract Although many wild bird species may act as reservoir hosts for tick-transmitted diseases and/or support long-distance dispersal of infected ticks, to date no research has been done on the extent to which song- birds may acquire resistance to ixodid ticks. Here we investigate whether two passerine species belong- ing to the family Paridae, the blue tit (Cyanistes caeruleus) and the great tit (Parus major), are able to acquire resistance after repeated infestations with Ixodes ricinus nymphs. As blue tits are less frequently exposed to I. ricinus in the wild than great tits, we expected I. ricinus to be less adapted towards the blue tit’s resistance mechanisms. Over the three infestation sessions we observed consistently high tick attachment rates and yields, high engorgement weights, and short engorgement and moulting durations, indicating that neither of the two songbird species is able to mount effective immune responses against I. ricinus nymphs after repeated infestations. As a consequence of the lack of resistance, birds were unable to prevent the direct harm (acute blood depletion) caused by tick feeding. Birds compensated the eryth- rocyte loss without reduction in general body condition (body mass corrected for tarsus length). The lack of resistance suggests that I. ricinus has a long co-evolutionary history with both avian hosts, which enables the tick to avoid or suppress the host’s resistance responses. Ó 2009 Australian Society for Parasitology Inc. All rights reserved. 1. Introduction Few studies have focussed on the interactions between ixodid ticks and avian hosts. Although many wild bird species may act as reservoir hosts for tick-transmitted diseases and support long- distance dispersal of ticks (Anderson et al., 1986; Olsen et al., 1993, 1995; Comstedt et al., 2006; Larsson et al., 2007), to date lit- tle information is available on the extent to which wild birds may acquire resistance to ticks. Population dynamics of hosts, vectors and their pathogens strongly depend on the ultimate outcomes of vector–host interactions (Anderson and May, 1978, 1979; Ran- dolph et al., 2002). Therefore, in order to gain insights into the epi- demiology of tick-transmitted diseases in the wild, it is essential to obtain knowledge of the hosts’ innate and acquired resistance to the ticks to which they are naturally exposed (Randolph, 1979; Randolph and Nuttall, 1994; Nunn et al., 2006). On a global scale, ticks and tick-transmitted diseases cause huge annual economic losses due to their negative impact on public health and livestock (Lehmann, 1993; Wikel, 1996; Zhang et al., 2006). During the last few decades there has been an increasing interest in the immunology of the host–tick interface and host resistance in particular. Since the work of Trager (1939), who re- ported that Guinea pigs were able to mount a very efficient im- mune response to the tick Dermacentor variabilis, many studies have reported on acquired resistance to ticks, especially in domes- tic mammals. Resistance to an ectoparasite reflects the ability of the host to recognise the antigens of the ectoparasite and to protect itself against harm from the parasite (Wakelin, 1996; Wikel, 1996). If the tick’s counter-measures to the host immune system are not effective, tick feeding and salivation will be hindered. Conse- quently premature detachments and hence reductions in engorge- ment weights occur, which result in reduced tick survival or offspring numbers. Ticks that remain attached to resistant hosts feed very slowly or not at all and many die in situ (Rechav, 1992; Hillyard, 1996; Wikel, 1996). The ability to acquire immunity in response to tick bites varies strongly amongst host species. It is assumed that in longer-estab- lished parasitic relationships, ticks are more likely to successfully evade or suppress the host’s rejection mechanisms (Ribeiro, 1989; Sonenshine, 1993). Few studies have investigated the phys- iological responses developed by natural hosts against ixodid ticks (e.g. Randolph, 1979; Fielden et al., 1992; Dutoit et al., 1994; Hughes and Randolph, 2001). This is surprising, since processes at the tick–host interface may influence the biology of ticks, as well as pathogen transmission (Randolph, 1979; Wikel, 1980; Fivaz et al., 1989; Randolph and Nuttall, 1994; Wikel et al., 1997). To our knowledge, the occurrence of resistance in natural tick-song- bird systems has not been examined to date. The aim of the work described in this paper was to investigate whether two passerine birds belonging to the family Paridae – the blue tit (Cyanistes caeruleus) and the great tit (Parus major) – are able 0020-7519/$36.00 Ó 2009 Australian Society for Parasitology Inc. All rights reserved. doi:10.1016/j.ijpara.2009.07.011 * Corresponding author. Tel.: + 32 3 265 34 70; fax: + 32 3 265 34 74. E-mail address: Dieter.Heylen@ua.ac.be (D.J.A. Heylen). International Journal for Parasitology 40 (2010) 183–191 Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara