Abstract
The tick species infesting grazing animals in the countryside of 11 prefectures in Northern Greece were investigated during April–July and September–December of consecutive years 2003–2006. A total of 3,249 (1,952 males, 1,297 females) adult ticks were collected from goats, sheep, cattle and dogs. Ticks were identified as Ixodes ricinus (44.57%), Ixodes gibbosus (4.09%), Rhipicephalus bursa (19.14%), Rhipicephalus sanguineus, Rhipicephalus turanicus (5.79%), Hyalomma marginatum marginatum (12.40%), Dermacentor marginatus (0.31%) and Boophilus annulatus (4.43%). Rhipicephalus spp. and Hyalomma spp. were abundant in all prefectures, Ixodes spp. were present in 9/11 prefectures, Boophilus spp. in 4/11, while Dermacentor spp. were found only in one. Results of this study give an insight into the ecology of ticks and their potential of tick-borne diseases in the country.
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Many tick species are responsible for the transmission of a variety of pathogens to humans and livestock. Spotted fever group rickettsiae, babesia, borrelia, ehrlichia, anaplasma, as well as tick-borne encephalitis (TBE) virus and Crimean Congo Hemorrhagic fever (CCHF) virus are common tick-borne pathogens (Parola and Raoult 2001, Charrel et al. 2004). The knowledge of the incidence, the prevalence and the geographical distribution of the tick species in a region is helpful for the prevention and control of tick-borne diseases.
Greece is divided into ten regions, which are further subdivided into 54 prefectures. The most common climate is the typical Mediterranean, characterized by hot but not torrid summer and mild and short winter with moderate rainfalls. The typical evergreen Mediterranean scrub vegetation is widespread. A previous study on ticks collected of domestic animals in Northern Greece during 1983–86 revealed that the most common tick, found in all bioclimatic zones, was Rhipicephalus bursa, and that Rhipicephalus and Hyalomma ticks were active during spring-summer, while Ixodes spp., Haemophysalis spp. and Dermacentor marginatus were active mostly during autumn and winter (Papadopoulos et al. 1996). In another study, three species of Ixodid ticks (Ixodes gibbosus, R. bursa and D. marginatus) were collected from goats, and I. gibbosus was the most abundant and prevalent species collected from October to April (Papazahariadou et al. 1995). A recent study in Cephalonia Island revealed that a variety of tick species were present, some of them PCR-positive for C. burnetii and SFG rickettsiae (Psaroulaki et al. 2006).
In the present study we update the knowledge of the tick species parasitizing small mammals living permanently in farms located in the countryside of two regions (Macedonia and Thrace) of Greece, both in the northern part of the country. Tick collection was carried out during 2003–2006 in 9 of 13 prefectures of Macedonia, and in 2 of 3 prefectures of Thrace (Fig. 1). Specifically, the 9 prefectures of Macedonia were: Drama and Kavala from Eastern Macedonia—Serres, Kilkis, Halkidiki, Pella and Imathia from Central Macedonia—Florina and Kastoria from Western Macedonia. The two prefectures of Thrace were Evros and Xanthi. Ticks were collected from cattle, mainly sheep and goats, from 4 to 5 different areas of each prefecture. All farms were situated in hilly areas above 600 m, neighboring with forests of deciduous and evergreen vegetation (oaks and coniferous trees). A continuous movement of the herds during the day involved the entry into the forests and probably the acquisition of questing ticks from the thick low vegetation. The collection was conducted during April–July and September–December of each year. The farms were visited at least twice during the collection period. Ticks were put into tubes labeled with the place and date of collection, the animal species and the name of the breeder. Data concerning the altitude, latitude, longitude, vegetation and climate type of the area were recorded. The tick classification was performed using identification keys taking into account the external morphological characters (Estrada-Pena et al. 2004).
In total, 3,249 ticks were collected. All were adults (1,952 males, 1,297 females) belonging to the Ixodidae family. Most ticks were collected from goats (n = 2,042, 62.85%) and sheep (n = 869, 26.74%), followed by collection from cattle (n = 243, 7.47%) and dogs (n = 95, 2.92%). Ticks belonged to five genera: Ixodes (I. ricinus, I. gibbosus), Rhipicephalus (R. bursa, R. turanicus, R. sanguineus), Hyalomma (H. m. marginatum), Boophilus (B. annulatus) and Dermacentor (D. marginatus). Most common was I. ricinus (44.57%), while D. marginatus was the most seldom (0.31%). The distribution of ticks in each region is seen in Table 1. Rhipicephalus spp. and Hyalomma spp. were abundant in all prefectures, Ixodes spp. was found in all prefectures except two (Florina and Xanthi), Boophilus spp. was present in Kilkis, Pella, Halkidiki and Xanthi, while Dermacentor spp. was found only in Imathia.
Rhipicephalus bursa, the main vector of Babesia equi, Babesia ovis, Theileria ovis and Anaplasma ovis, was found in every farm tested and in all animal species. I. ricinus, the main vector of TBE virus, Borrelia burgdoferi and several rickettsiae and piroplasms was also found very often. However, a recent study on epidemiology of TBE in Greece revealed that the disease is very rare in Greece (Pavlidou et al. 2007); this is probably due to the absence of synchrony in the seasonal activity of larval and nymphal I. ricinus ticks (Randolph et al. 2000). I. gibbosus was much less common, found in only 3 prefectures (Imathia, Pella and Kastoria), showing similar distribution as in a previous study (Papadopoulos et al. 1996).
Concerning seasonality, I. ricinus was collected in November (n = 1,037/1,448, 71.61%) and June (n = 411/1448, 28.38%). Compared to other European countries, the autumn maximum activity period of this species is prolonged in Greece by 1–2 months, probably due to the milder winter, suggesting that ticks adapt themselves in local climatic and ecological conditions. I. gibbosus was collected mainly in November. Rhipicephalus spp. was collected during May-July (peak in June). H. m. marginatum was collected during June–July and October–November, while B. annulatus was present only in November. D. marginatus was collected during May–July.
Ticks were collected at areas with altitude more than 600 m, nearby evergreen forests, where the average humidity was approximately 80%. Studies from many European countries show that nowadays ticks are found in altitude of 1,200 m, as a result of the global warming phenomenon (Danielova et al. 2006). Because of the climatic changes, or changes in other factors that might affect tick population dynamics, studies on distribution and ecology of ticks have to be repeated over time to renew the existing knowledge and to provide data for reliable predictive models. The present study gives an update of the seasonal and geographical distribution and abundance of ticks in N. Greece, which might help the prediction of the disease transmission potential to humans and livestock.
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Pavlidou, V., Gerou, S., Kahrimanidou, M. et al. Ticks infesting domestic animals in northern Greece. Exp Appl Acarol 45, 195–198 (2008). https://doi.org/10.1007/s10493-008-9167-5
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DOI: https://doi.org/10.1007/s10493-008-9167-5