Introduction

Ticks are obligate blood-sucking arthropods that ectoparasitize on every class of vertebrates in almost every region of the world. There are three generally recognized families of ticks which comprise the Ixodidae named as “hard ticks” (694 species), the Argasidae named as “soft ticks” (177 species), and the Nuttalliellidae represented by a single species confined in southern Africa (Oliver 1989; Sonenshine 1991). Except the eggs, ticks have three life stages including the larva, nymph, and adult (male and female), and each stage requires blood meal for further development. Although ticks have been recognized as animal/human ectoparasites for thousands of years (Balashov 1972), the global impacts of ticks has been recognized by their ability to transmit a variety of tick-borne pathogens to their hosts and by direct injury to livestock because of their feeding behaviour (Jongejan and Uilenberg 2004). Their detrimental impacts on humans and animals lead to a major concern in public health.

In Taiwan, the emergence of human babesiosis (Shih et al. 1997; Shih and Wang 1998), Lyme borreliosis (Shih and Chao 1998; Chao et al. 2011, 2013) and canine babesiosis (Lee et al. 2010) raises attention on the medical and veterinary importance of ticks. Indeed, the hard ticks of Ixodes granulatus and I. ovatus were identified as the incriminated vector ticks for various genospecies of Borrelia spirochetes (Chao et al. 2009, 2010, 2012, 2014). The brown dog tick, Rhipicephalus sanguineus, has been recognized as the principle vector responsible for the enzootic transmission of Babesia vogeli and B. gibsoni in Taiwan (Chao et al. 2016b, 2017). In addition, the agent of spotted fever rickettsia had also been detected in I. granulatus tick in Taiwan (Tsai et al. 2008).

Because of climatic and geographical factors, the tick species infesting canine hosts may not be the same around the world (Lindgren et al. 2000; Gray 2008). Although the brown dog tick, R. sanguineus, is the most widespread tick species around the world and is recognized as the dominant ectoparasite on dogs (Dantas-Torres 2010), many other species of hard ticks have been observed on dogs in different geographic areas/Countries. Dermacentor variabilis (American dog tick) is recognized as the major ectoparasite of canine hosts reported in West USA, Canada, and Mexico (Mcnemee et al. 2003). Ixodes ricinus and I. hexagonus are reported as the main ectoparasites of dogs in Great Britain and Ireland (Ogden et al. 2000), and D. reticulatus is common in Western and Central Europe from France to Hungary as the potential vector for Babesia canis (Nosek 1972; Kabowiak 2014; Jongejan et al. 2015; Olivieri et al. 2016). It is also the main tick species attaching to dogs in Hungary (Foldvari and Farkas 2005). Rhipicephalus sanguineus is reported as the dominant tick species in dogs in Africa, Latin America, Mediterranean countries, and the majority of Asian countries (Walker et al. 2000; Shimada et al. 2003a; Estrada-Pena et al. 2004; Ugbomoiko et al. 2008; Tinoco-Gracia et al. 2009; Changbunjong et al. 2009; Chao et al. 2010). Indeed, R. sanguineus has been recognized as the principle ectoparasite of dogs in Bangladesh, Thailand, Japan, and China (Teng and Jiang 1991; Shimada et al. 2003a; Islam et al. 2006; Changbunjong et al. 2009). Other tick species were also reported on dogs depending geographies. However, the hard tick species infesting dogs in Taiwan needs to be further defined.

Materials and methods

Collection of ticks from dogs

From May 2010 to April 2011 ticks infesting dogs were collected from various localities (25.02N, 121.51E; 25.02N, 121.57E; 25.08N, 121.56E; 25.09N, 121.53E; 25.09N, 121.58E; 25.09′N, 121.51E; 25.10N, 121.58E; 25.11N, 121.55E; 25.07N, 121.54E; 25.07N, 121.56E; 25.05N, 121.50E; 25.05N, 121.51E; 25.02N, 121.50E; 25.01N, 121.49E; 25.03N, 121.48E; 25.03N, 121.57E; 25.03N, 121.53E; 25.14N, 121.51E; 25.13N, 121.50E; 25.03N, 121.62E; 25.08N, 121.60E; 25.07N, 121.56E; 24.98N, 121.57E) of Taipei City in northern Taiwan (Fig. 1). All specimens of ticks were carefully removed from dogs (Fig. 2) and subsequently stored in 75% ethanol solution in separate vials until further identification.

Fig. 1
figure 1

Map of Taiwan showing the tick collection from various districts of Taipei City in northern Taiwan

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Fig. 2
figure 2

Inspection and collection of hard ticks infesting dogs. Pictures show attached (a) and engorged adults (b) in the ear, partial-engorged adult (c) attached on the elbow, and nymphs (d) attached between the fingers

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Species identification

Based on the pictorial keys of morphological characteristics, all these tick specimens were identified to the species level, as described previously (Shih and Chao 2011; Chao and Shih 2016). Ultrastructural observations by stereo-microscope were also used to delineate the morphological features of all stages of hard ticks infested on dogs in northern Taiwan. Briefly, tick specimens were cleaned by sonication in 75% ethanol solution for 5–10 min and then washed twice in sterile distilled water. Afterwards, each stage of tick specimen was placed on a glass slide and photographed using a stereo-microscope (SMZ 1500, Nikon, Tokyo, Japan) equipped with a fiber lamp. The external features of these ticks were recorded for species identification.

Results

Species and life stages

A total of 9467 ticks including 4204 females, 3405 males, 1635 nymphs and 223 larvae were collected from 2025 dogs (Table 1). All ticks were identified to the species level: R. sanguineus (8759), R. haemaphysaloides (218), H. hystricis (434), H. lagrangei (4), H. formosensis (1), and I. ovatus (51). Rhipicephalus sanguineus (92.5%) was the most dominant species followed by H. hystricis (4.6%), R. haemaphysaloides (2.3%), I. ovatus (0.54%), H. lagrangei (0.04%) and H. formosensis (0.01%) (Table 1).

Table 1 Species and life-cycle stage of hard ticks collected from dogs in northern Taiwan
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Monthly prevalence and infestation

The highest seasonal prevalence of hard ticks was collected in September (1541 specimens) followed by October (1406), August (1120), June (1034), July (1027), November (878), May (744), December (603), April (319), March (274), February (265), and January (256), as indicated in Table 2. In general, the distribution of adult and nymphal ticks can be observed from every month of the year. However, larval stage were only observed from May to November. In addition, the highest monthly prevalence for the three major tick species of R. sanguineus, R. haemaphysaloides and H. hystrics was recorded on September, March and August, respectively (Fig. 3). The average infestation is observed on dogs with a density of 4.68 ticks per dog and the highest seasonal infestation was observed in September with a density of 8.24 ticks per dog (Table 3).

Table 2 Monthly distribution of species and numbers of hard ticks collected from dogs in northern Taiwan
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Fig. 3
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Monthly prevalence of the three major tick species infesting dogs in northern Taiwan

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Table 3 Monthly infestation and density of hard ticks on dogs in northern Taiwan
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Discussion

This study is the first large scale survey of hard ticks ectoparasitizing canine hosts in Taiwan. Species identification of these collected ticks reveals six species. The brown dog tick (R. sanguineus) was the most abundant (92.5%) species found on dogs and all life-stages of R. sanguineus ticks were recovered from canine hosts. Rhipicephalus sanguineus is recognized as a three-host tick (Dantas-Torres 2010). Indeed, the R. sanguineus tick is highly prevalent either in urban or suburban areas of northern Taiwan, and the availability of canine hosts is highly favorable for the life cycle of R. sanguineus.

The hard ticks of H. hystricis and R. haemaphysaloides were determined as the second and third dominant species infesting canine hosts in northern Taiwan. In previous studies, the H. hystricis was found to be distributed in the southeast Asian Countries of India, Vietnam, China and Japan. The immature (larva and nymph) and mature (adult) ticks of H. hystrics infest rodents and large mammals including dogs, respectively (Hoogstraal et al. 1965). Rhipicephalus haemaphysaloides was recognized to be distributed in Pakistan, Nepal, India, Indonesia, China and Taiwan (Walker et al. 2000; Yin and Luo 2007). In this study, all developmental stages of H. hystricis ticks were collected from dogs, but only adult and nymphal stages of R. haemaphysaloides were observed on dogs (Table 2). All these ticks were found to be most abundant in the suburban and rural areas of northern Taiwan. In addition, Ehrlichia and Anaplasma have been detected in H. hystricis and R. haemaphysaloides ticks (Parola et al. 2003; Kuo et al. 2018). Thus, their vectorial capacity for tick-borne pathogens requires further investigations.

Although the hard ticks of I. ovatus, H. formosensis, and H. lagrangei had been reported in Asia (Hoogstraal et al. 1973a, b; Teng and Jiang 1991; Robbins 2005), these tick species are rarely collected from dogs in Taiwan. In Japan, the I. ovatus was more frequently found on cats kept near woodland area (Shimada et al. 2003). In our previous study, we also collected I. ovatus ticks from stray cats in the suburban region of northern Taiwan and the causative agent of Lyme disease spirochete (Borrelia garinii) was isolated from this tick specimen (Chao et al. 2014). In this survey, only adult and nympal ticks of I. ovatus were collected from dogs and most ticks were collected during the winter season (Table 2). This seasonal prevalence of I. ovatus ticks observed on dog may imply the possibility of other mammals or rodents serving as the hosts for the larval tick in the natural cycle of I. ovatus tick and need to be further identified in Taiwan.

In conclusion, this large scale survey reveals six species of hard ticks ectoparasitizing canine hosts in northern Taiwan. Because dogs are recognized as the company animal and are closely associated with humans, further investigations on the prevalence of tick-borne pathogens in these tick species may help to evaluate the impact on human health in Taiwan.