Ixodes species

Mackenstedt, Ute, Jenkins, David & Romig, Thomas, 2015, The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas, International Journal for Parasitology: Parasites and Wildlife 4 (1), pp. 71-79 : 76-77

5. Ixodes species and the transmission of parasites/pathogens in peri-urban/urban areas

Ticks, mosquitoes and fleas are important arthropod vectors in the transmission of parasites and other pathogens, some of which are zoonotic. In the northern hemisphere, the majority of vector-borne infections are transmitted by ticks ( Randolph, 2001), especially Ixodes species that are highly competent vectors for a variety of different pathogens including parasites, bacteria and viruses ( Sonenshine and Roe, 2014). In general, the eco-epidemiology of zoonotic vector-borne diseases is still little understood, as it depends on the interaction of a vector with (often several) reservoir hosts and a pathogen which is transferred from the reservoir to the human host ( Pfäffle et al., 2013). Ixodes species have a three-host life cycle with larvae feeding predominantly on small mammals whereas adults prefer larger mammals. Nymphs tend to feed on small as well as large mammals. The most abundant tick in central Europe, Ixodes ricinus , has the capacity to feed on more than 300 different vertebrate host ( Bowmann and Nuttall, 2008), including small rodents, lizards, hares, hedgehogs as well as larger animals like deer, red foxes or wild boar. I. ricinus populations are usually associated with deciduous and mixed forests, but recent studies show that this tick species can also be highly abundant in peri-urban and urban areas ( Rizzoli et al., 2014). As already mentioned above, urbanization changes the local wildlife composition drastically. This has important consequences for tick densities, because the local composition of host species and their abundance affects the capacity of the environment to support tick populations. Roe deer ( Capreolus capreolus ), red foxes ( Vulpes vulpes ) and wild boar (Sus scrofa) are particularly important for the maintenance and the geographical distribution of I. ricinus , because they host all three different developmental stages of I. ricinus , can carry a large number of ticks and may migrate over long distances. Importantly, they are often attracted by peri-urban and urban areas ( Gassner et al., 2011; Medlock et al., 2013; Overzier et al., 2013; Rizzoli et al., 2014) Roe deer and other cervids as well as foxes or wild boar are important reservoir hosts of numerous pathogens which may be transmitted by ticks to humans, so their high abundances in peri-urban and urban areas increase zoonotic infection risks ( Medlock et al., 2013; Rizzoli et al., 2014; Sonenshine and Roe, 2014). Schorn et al. (2011) collected I. ricinus in several parks within different cities in southern Germany, which were found to contain Babesia and several bacterial pathogens. Interestingly, the composition of pathogens in “urban” ticks revealed differences when compared to woodlands. Overzier et al. (2013) collected more than 10000 I. ricinus ticks from four different urban parks, a pasture and a natural area in Bavaria, Germany. The prevalence of Babesia spp. was generally higher in the pasture and the natural area compared to the urban parks. Three species, Babesia microti , B. venatorum and B. capreoli , were detected in ticks collect- ed in the natural area, whereas in the pasture and the urban habitats only one species, B. venatorum , was frequent. It is important to note that B. venatorum may infect humans and that roe deer are reservoir hosts of this parasite ( Pfäffle et al., 2013; Rizzoli et al., 2014). Pichon et al. (1999) pointed out that tick abundance is positively correlated with deer abundance, and those habitats with high densities of deer or cervids in general are therefore areas with a higher risk of infection. Habitat fragmentation and landscape conversion may also favour high population densities of small mammals, mainly rodents, which are crucial as hosts for tick larvae and nymphs as well as important reservoirs for many tick transmitted pathogens ( Boyard et al., 2008; Paziewska et al., 2010; Medlock et al., 2013; Pfäffle et al., 2013; Rizzoli et al., 2014). The most prevalent tick-borne infection in the northern hemisphere is Lyme borreliosis. In northeastern North America, extensive studies were conducted on the interactions between Borrelia burgdorferi and the different hosts which are involved in the transmission of this pathogen from wild animals to humans ( Allan et al., 2003; LoGiudice et al., 2003). Adult Ixodes scapularis , as the most important vector, feeds on whitetailed deer ( Odocoileus virginianus ), which is important for the maintenance of the tick population and reaches high population densities in peri-urban areas. I. scapularis becomes infected with B. burgdorferi when feeding on Peromyscus leucopus , the whitefooted mouse which is the most competent reservoir host for the pathogen and reaches high population densities due to habitat fragmentation in the vicinity of humans settlements. An infected I. scapularis transmits the pathogen to humans. The importance of rodents and other small mammals as “bridge” hosts is more and more recognized, because some species are well adapted to urban environments, are competent reservoir host of many pathogens and may introduce the parasites or pathogens to new habitats ( Rizzoli et al., 2014). In addition, small mammals are maintenance hosts for different tick species, which means that pathogens can be exchanged between the different ticks. This host switch may be important because the behaviour and the habitat requirements of tick species differ concerning biotic and abiotic parameters ( Pfäffle et al., 2013; Sonenshine and Roe, 2014). European hedgehogs ( Erinaceus europaeus ) can serve as an example for such a host switch. They are common animals, well adapted to urban areas and are frequently infested with two different tick species ( I. ricinus and I. hexagonus ), both competent vectors for many pathogens. I. ricinus is a generalist, whereas I. hexagonus feeds almost exclusively on hedgehogs. I. hexagonus was shown to maintain a high infection rate of pathogens within hedgehog populations, whereas I. ricinus , becoming infected when feeding on hedgehogs, can transmit these pathogens to various other hosts due to their low host specificity ( Estrada-Penã and Jongejan, 1999; Skuballa et al., 2010). These socalled subcycles are important for maintaining stable pathogen populations in urban areas ( Pfäffle et al., 2013).

In summary, peri-urban and urban areas are complex and diverse ecosystems which can favour tick transmitted pathogens, although there are still many unsolved questions about the interactions of vectors, reservoir hosts and the transmission of pathogens to humans and/or domestic animals which need to be answered.