The survey results showed brown dog tick, Rh. sanguineus was the major tick species that infest domestic dogs island-wide. More than fifty years ago, Seneviratne in 1965 [20] reported Rh. sanguineus as the most frequently found tick on dogs in Ceylon (now Sri Lanka). It is also the most widespread dog tick worldwide [26]. This tick can be found on dogs living in both urban and rural areas, being highly adapted to live within human dwellings and being active throughout the year not only in tropical and subtropical regions but also in some temperate areas [26]. Although the dog is the main host, it has also been recorded on other animals like wild canids [27] and a wide range of wild and domestic animals of Sri Lanka including ox, horse, buffalo, cat, goat, sheep, and also humans [20, 22, 23, 28]. This indicates that free-ranging wild animals might be involved in its maintenance and dispersion through different regions. This could have implications in tick control and the epidemiology of tick-borne diseases, particularly in areas where dogs live in close contact with wildlife [26]. Studies have shown that some dog breeds appear to be more resistant than others to infestations by Rh. sanguineus [29]. The local mongrels crossbred with different breeds or crossbred with the local Sinhala hound or Sinhalese hound belonging to the species Sinhala sunakaya which is found in Sri Lanka and parts of India seem to be more resistant to tick bites, but further studies are needed to assess the dog breed susceptibility to ticks. This tick was attached everywhere on the dog but the preferred site was the head region, which is consistent with the description in the review of Dantas-Torres, 2010 [26] and therefore makes it difficult for dogs to remove them, whereas immatures feed on lower areas of the dog’s body (e.g., belly, rump, and hind legs), probably because of their more limited mobility [12]. Rhipicephalus sanguineus is the most important species from the veterinary standpoint as it is a vector of many pathogens affecting dogs and occasionally humans [26, 30, 31, 32]. It is known to carry many pathogens, including Babesia vogeli, Ehrlichia canis, Hepatozoon canis, Rickettsia conorii and Rickettsia rickettsii, the last two also been responsible for disease in humans [13]. Liyanaarachchi et al. (2015b) [24] detected DNA of spotted fever group rickettsiae in Rh. sanguineus collected from a domestic dog in Sri Lanka.
In addition to Rh. sanguineus, seven other species were recorded in dogs: Rhipicephalus haemaphysaloides, Haemaphysalis bispinosa, Haemaphysalis intermedia, Haemaphysalis turturis, Amblyomma integrum, Dermacentor auratus and Hyalomma sp. Previously, Seneviratne (1965) [20] reported six species of ticks, Rh. sanguineus, Rh. haemaphysaloides, H. intermedia, H. bispinosa, Boophilus sp, A. integrum (immature stages) collected from dogs in Sri Lanka. Later, Liyanaarachchi et al. (2015a) [22] recorded 14 species of ticks including, Rh. sanguineus, Rh. haemaphysaloides, H. intermedia, H. bispinosa, Rh. microplus, A. integrum, H. cuspidata, H. spinigera, H. aculeata, A. testudinarium, A. clypeolatum, Hy. isaaci and D. auratus from dogs. Out of the previously recorded six species, Rh. microplus, H. cuspidata, H. spinigera, H. aculeata, A. testudinarium and A. clypeolatum were not reported in the present study. Some of these rare species could be accidental occurrences due to close contact of dogs with livestock and wildlife.
Rhipicephalus haemaphysaloides was the second most common tick on dogs recorded from all over the island with a wide geographical distribution but is less common at elevations above 3000 ft. It was the dominant dog tick species in the Intermediate zone especially in Polonnaruwa, Nuwara-Eliya, Monaragala, Badulla and Mannar districts. Although rare in urban areas, it was common in rural areas and areas closer to the forests. It has a limited distribution in the world occurring over the Oriental and parts of the Palaearctic and Australasian zoogeographic regions from Afghanistan in the west to the Philippines and Indonesia in the east and the Indian subcontinent [20, 33, 34]. It is known to infest all domestic animals, including ox, water buffalo, and horse but more commonly seen on sheep and goats [20, 23]. This tick species has a great potential for the transmission of Kaysanur forest disease virus in India [35] and Rickettsia rhipicephali in Taiwan [36], and as the principal vector of bovine babesiosis (e.g. Babesia orientalis) in China [37].
Three species of Haemaphysalis were recorded in the present study: H. intermedia, H. bispinosa and H. turturis, among which H. intermedia was widely distributed in all the districts in all three agro-climatic zones but the abundance was low. In 1965, Seneviratne [20] also reported that H. intermedia was a widespread tick species in Sri Lanka and collected from all domestic animals throughout the island. These two species, H. bispinosa, and H. intermedia are the major goat tick in Sri Lanka [23] and it also infests cattle (unpublished observations). Globally, H. bispinosa has a limited geographical distribution, being restricted to certain parts of Southern India and Sri Lanka. Haemaphysalis turturis was a rare species found only from Kagalle, Kilinochchi and Trincomalee Districts.
Dermacentor auratus and Hyalomma sp. were recorded from only one location in the Kandy and Vavuniya Districts, respectively. The primary host of D. auratus in wild boar and the tick has an island-wide distribution and a rapid increase in the population has been observed due to restricting the killing of wild boars. Nymphs of D. auratus have been identified as the major tick species responsible for human otoacariasis in Sri Lanka [28, 38, 39]. Dogs also carry this tick species, and it is possible when the wild boars visit the human habitats, the engorged females, drop-off and lay eggs and larvae can be easily picked by dogs as well as humans. Hyalomma sp was only found from one location in the Dry Zone. According to the Seneviratne in 1965 [20], they collected ticks from buffalo, neat cattle and goats but not from the dogs. This result of the present study may be an accidental occurrence and may be due to their contact with cattle.
Immature stages of Amblyomma integrum were recorded from several locations in Rathnapura, Matara, Monaragala and Badulla districts. This species is very widespread in Sri Lanka and is more common in jungle areas [22]. According to Seneviratne 1965 [20], the incidence of A. integrum was lower in the higher elevations around Nuwara-Eliya which is similar to the present study and the more thickly populated parts of the Western Province which is not similar to the present study.
All the life stages except larvae of Rh. sanguineus and Rh. haemaphysaloides were found on dogs. Among adults, more females were present than males. The presence of more females has been reported in Shimada et al. 2003 [15] and the presence of more males has been reported in Dantas-Torres and Otranto 2011 [40] and Diyes & Rajakaruna 2015 [23]. Only nymphs of D. auratus and A. integrum and only adults of H. turturis and Hyalomma sp were recorded.
The three-host life cycle of Rh. sanguineus was successfully completed within an average of 98 days (70-126 days) and all three stages fed on the New Zealand white rabbits. The duration of the life cycle was shorter compared to the previous studies where it has taken 162-177 days to complete the life cycle [19, 41]. This might be due to the diverse conditions of temperature and relative humidity in which ticks were maintained, as well as the climatic conditions of different geographic regions. However, there might be also some strain-related differences [41]. The weight of the wild-caught females of this study was 133.2 (54-187) mg which is lower than previously recorded values (289.5 mg; [41]). Wild-caught females were removed deliberately from the host while in the study done by Dantas-Torres in 2008 [41] females were allowed to naturally drop off after feeding. The number of eggs laid, during this study was consistent with the previous records, however, with a lower mean number [19, 41]. Similarly, recorded pre-oviposition period, incubation period and parasitic periods of all three life stages were lower than previously recorded durations [19, 41]. The REI and RFI were 50.8±9.69 (22.0-70.0) and 9.1±5.01 (0-22.6) respectively. Dantas-Torres [41], reported an REI of 13 and an RFI of 13.2 for the same species in Italy. The egg-laying potential of an engorged female is directly related to her capacity to feed; therefore heavier females show the highest values in the number of eggs laid as well as the weight of the egg mass and after that a higher hatch rate. This would explain higher REI, Reproductive Affinity Index (RAI) and RFI in Italy population [41, 42].
The distribution and abundance of dog tick species may depend on many factors such as climatic factors such as temperature, humidity, rainfall, presence of other domestic and wild animals and management practices including usage of acaricides and the life cycle can be different from other geographic regions according to the different climatic factors present. Moreover, Dantas-Torres (2010) [26] highlights that in the era of globalization and climate changes; Rh. sanguineus is becoming increasingly relevant from a public health perspective. This tick has also been implicated in the transmission of pathogens of zoonotic concern (e.g., R. rickettsii) and recent studies have shown that Rh. sanguineus ticks exposed to high temperatures are more prone to bite humans [43]. This scenario highlights that the climate change could affect Rh. sanguineus populations of around the world and, consequently, the epidemiology of certain tick-borne infections [43].