Coexistence of Pathogens in Host-Seeking and Feeding Ticks within a Single Natural Habitat in Central Germany

The importance of established and emerging tick-borne pathogens in Central and Northern Europe is steadily increasing. In 2007, we collected Ixodes ricinus ticks feeding on birds (n = 211) and rodents (n = 273), as well as host-seeking stages (n = 196), in a habitat in central Germany. In order to find out more about their natural transmission cycles, the ticks were tested for the presence of Lyme disease borreliae, Anaplasma phagocytophilum, spotted fever group (SFG) rickettsiae, Francisella tularensis, and babesiae. Altogether, 20.1% of the 680 ticks examined carried at least one pathogen. Bird-feeding ticks were more frequently infected with Borrelia spp. (15.2%) and A. phagocytophilum (3.2%) than rodent-feeding ticks (2.6%; 1.1%) or questing ticks (5.1%; 0%). Babesia spp. showed higher prevalence rates in ticks parasitizing birds (13.2%) and host-seeking ticks (10.7%), whereas ticks from small mammals were less frequently infected (6.6%). SFG rickettsiae and F. tularensis were also found in ticks collected off birds (2.1%; 1.2%), rodents (1.8%; 1.5%), and vegetation (4.1%; 1.6%). Various combinations of coinfections occurred in 10.9% of all positive ticks, indicating interaction of transmission cycles. Our results suggest that birds not only are important reservoirs for several pathogens but also act as vehicles for infected ticks and might therefore play a key role in the dispersal of tick-borne diseases.Lyme borreliosis is the most frequent arthropod-borne disease in the northern hemisphere (6), but other pathogens, such as intracellular bacteria of the order Rickettsiales (Anaplasma phagocytophilum, spotted fever group [SFG] rickettsiae), Francisella tularensis, and intraerythrocytic parasites of the genus Babesia, have gained more and more importance as tick-borne agents in Europe (52). The castor bean tick (Ixodes ricinus) has a three-host life cycle, which means that it ingests a blood meal in each life stage before it molts. When transovarial transmission of a pathogen is absent or very rare, as is the case with Borrelia spp. (63), A. phagocytophilum (10), and Babesia microti (15), detection of these agents in feeding larvae is an indication of pathogen transmission from an infected reservoir host to the tick. With the exception of SFG rickettsiae, which use ticks as the vector and reservoir, established and emerging pathogens are maintained by vertebrate reservoirs during their life cycles. Although methods for detection and characterization are constantly improving, the ecology of tick-borne pathogens, particularly their reservoir host specificity, is still not understood in detail.The agents of Lyme disease form a very heterogeneous complex, which can be subdivided into several clusters by phylogenetic analysis of genes (e.g., ospA) or noncoding regions. Several bird, rodent, and reptile species act as reservoirs for these spirochetes (32).Anaplasma phagocytophilum is the causative agent of human granulocytic anaplasmosis (HGA), an influenza-like illness of humans and domestic animals which is widespread in Europe. Sheep, deer, and rodents have been discussed as reservoir hosts for HGA agents (28, 31). Birds might be of importance in the dispersal of Anaplasma-infected ticks over long distances (18).At least half of the about 30 SFG rickettsiae distributed worldwide that have been described so far are known to be pathogenic for humans. Because efficient transovarial transmission of SFG rickettsiae from female ticks to larvae has been described for several species, e.g., Rickettsia parkeri, R. slovaca, and R. helvetica, the tick vector can also be regarded as a reservoir host (38). Some small mammals, like meadow voles and chipmunks, develop a strong rickettsemia which might allow transmission to parasitizing ticks (38). Although a vehicle function of birds is hypothesized (13), further investigations are needed to ascertain their possible role as reservoir hosts for SFG rickettsiae.Tularemia is a zoonotic disease caused by F. tularensis. In Germany, only the subspecies F. tularensis subsp. holarctica is prevalent, primarily in wild mammals (lagomorphs and rodents), but humans can become infected through the bite of hematophagous arthropods, by direct contact with infected animals (mostly hares), by ingestion of contaminated food or water, or by inhalation of infected aerosols (57). Potential vectors include ticks, mosquitos, and deer flies (40). However, in Germany, only ticks seem to play a relevant role. Movements of birds that excrete the bacteria with their feces might explain the transfer to islands and over long distances (35).Besides bacterial and viral agents, pathogenic parasites are also transmitted by I. ricinus. Protozoa of the genus Babesia invade erythrocytes and cause an often life-threatening malaria-like disease in humans and animals. Rodents are frequently infected with Ba. microti, but there is still no final evidence for a reservoir role of small mammals for pathogenic Babesia species. The main reservoirs of Babesia divergens are cattle and deer (15). Recently, we discovered that bird-feeding subadult ticks are frequently infected with Ba. divergens- and Ba. microti-like species, indicating an important role of migratory passerines as reservoirs and in the dispersal of Babesia spp. (18).The aim of the present study was to gain information about the cocirculation of five tick-borne pathogens in a single natural focus, especially regarding their preferred reservoir hosts and vehicles.