J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 276 http://jad.tums.ac.ir Published Online: September 30, 2018 Original Article Ixodid Tick Vectors of Wild Mammals and Reptiles of Southern India K. G. Ajith Kumar 1, *Reghu Ravindran 1, Joju Johns 2, George Chandy 2, Kavitha Rajagopal 3, Leena Chandrasekhar 4, Ajith Jacob George 5, Srikanta Ghosh 6 1Department of Veterinary Parasitology, College of Veterinary and Animal Sciences, Pookode, Lakkidi, Kerala, India 2Centre for Wildlife Studies, College of Veterinary and Animal Sciences, Pookode, Lakkidi, Kerala, India 3Department of Livestock Products Technology, College of Veterinary and Animal Sciences, Pookode, Lakkidi, Kerala, India 4Department of Veterinary Anatomy, College of Veterinary and Animal Sciences, Pookode, Lakkidi, Kerala, India 5Department of Veterinary Pathology, College of Veterinary and Animal Sciences, Pookode, Lakkidi, Kerala, India 6Entomology Laboratory, Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, India (Received 7 Mar 2015; accepted 15 June 2018) Abstract Background: We aimed to focus on the ixodid ticks parasitizing wild mammals and reptiles from Wayanad Wildlife Sanctuary, Western Ghat, southern India. Methods: The taxonomic identification of ticks collected from wild mammals and reptiles was performed based on the morphology of adults. Results: We revealed eight species of ticks including, Amblyomma integrum, Rhipicephalus (Boophilus) annulatus, Haemaphysalis (Kaiseriana) spinigera, H. (K.) shimoga, H. (K.) bispinosa, H. (Rhipistoma) indica, Rhipicephalus haemaphysaloides and R. sanguineus s.l. collected from nine species of wild mammals while four tick species Ablyomma kraneveldi, A. pattoni, A. gervaisi and A. javanense parasitizing on four species of reptiles. The highest host richness was shown by H. (K.) bispinosa and R. haemaphysaloides parasitizing six and five different host spe- cies, respectively. Reports of R. (B.) annulatus on sambar deer, A. javanense and A. kraneveldi on python as well as A. pattoni on Indian rat snake are the new host records from this region. Conclusion: Eight species of ticks parasitizing on nine species of wild mammals and four species of parasitizing on four species of reptiles were identified. The highest host richness was shown by H. (K.) bispinosa and R. haemaphy- saloides. H. spinigera as the vector of KFD was also identified in this study. Keywords: Ticks, Wild mammals, Reptiles, Wayanad, South India Introduction Ticks (Ixodida) are obligate, non-permanent ectoparasites of terrestrial vertebrates (1). They are exclusively haematophagous in all feed- ing stages of their life cycle and have con- siderable medical and veterinary importance (2). Besides, causes great economic losses to the livestock worldwide (3). Currently, 904 valid tick species have been listed through- out the world (4–13). Ticks parasitize a wide range of vertebrate hosts and transmit a vari- ety of pathogenic agents than any other group of arthropods (14, 15). Heavy infestation can cause blood loss, reduced weight gain and lowered milk production, even some tick spe- cies downgrade quality of hides (16). It is estimated that 80 per cent of world’s live- stock population is suffering from the del- eterious effects of ticks (17). Nearly, 106 Argasid and Ixodid tick spe- cies infesting domestic, wild and game animals were documented from India (18). The ix- odid tick R. (B.) microplus is the most prev- *Corresponding author: Dr Reghu Ravindran, E- mail: drreghuravi@yahoo.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 277 http://jad.tums.ac.ir Published Online: September 30, 2018 alent and economically important species in- festing livestock in India (19). On the global basis the losses incurred by livestock indus- try due to TTBDs was estimated in the range of 14000 to 18000 million US $ / year (16). The annual cost of control of TTBDs in India has been estimated as US $ 498.7 million (20). From the stand point of global biodiversity conservation, ticks are playing a significant role, as they are able to affect the fitness of wild life species by spill over epizootic out- breaks (21). Moreover, wild animals can act as reservoirs of infectious organisms and ticks can transmit them into domestic animals and humans. Over the last few decades approxi- mately 75 per cent of emerging diseases, in- cluding zoonoses, having wildlife origin (22). Western Ghats or the Sahyadri of south- ern India with an area of 17,000km2 run par- allel to the west coast of peninsular India stretching from Cape Comorin (or Kanyakuma- ri) in the south to the Surat Dangs in Gujarat in the North. Human and livestock popula- tion existing as high densities in this region (23, 24). Wayanad Wildlife Sanctuary (76º02’ to 76º 27’ East longitude and 11º 35’ to 11º 51’ North latitude) with an area of 344 sq. km. is set lofty on the majestic Western Ghats with altitude ranging from 650 to 1150m above the sea level. Rich in wild animals biodiver- sity, the sanctuary is an integral part of the Nilgiri biosphere reserve. Deadly tick borne viral infections like Ky- asanur forest disease (KFD) were reported from humans in Karnataka (25) and Kerala (26, 27) with or without mortality and Crimean-Con- go haemorrhagic fever (CCHF) from Gujarat while CCHFV-specific antibodies were detect- ed in human samples from Kerala (28). Pre- vious reports on tick vectors of wildlife of southern India are scanty. Hence, an active surveillance was initiat- ed to document the possible ixodid tick vec- tor species from the free ranging mammals and reptiles of the Western Ghats of Wayanad of Kerala, India. Materials and Methods Study area Study are comprised of the entire Waya- nad Wildlife Sanctuary (76º 02’ and 76º 27’ East Longitude and 11º 35’ and 11º51’ North Latitude) and adjoining area in the Wayanad District of Kerala, India. Animal and tick collection Wild animals are regularly brought to the College of Veterinary and Animal Sciences, Pookode by the officials of Department of Forest, Kerala for postmortem examination (animals died due to hunterattack, malicious poisoning or trapped), treatment and for health checkup prior to release back into the forest. Dead animals are surveyed in a short-time window (within 24 hoursafter death). A total of 46 wild mammals of 16 different species and 23 reptiles of nine species were included in the present study (Table 1). Body of these animals was examined for the presence of adults and engorged nymphs of tick. Adult ticks were collected in glass tubes and imme- diately transported to the parasitology labor- atory for identification. If identification was not possible on day of collection, the collect- ed ticks were stored for 24h in Boardman’s solution I (17% ethanol, 3% ether and 80% water). Then, for long term storage, they were transferred to solution II (80% ethanol, 15% water, 5% glycerol) to which 1% chlorform is added to prevent the colour change. Engorged live nymphs were immediately placed in BOD incubator at 28 °C and RH 85% for moulting to adults. Tick identification The taxonomic identification was performed based on the morphology of adult ticks accord- ing to standard keys and monographs (29–36). http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 278 http://jad.tums.ac.ir Published Online: September 30, 2018 Results Out of 46 wild mammals and 23 reptiles, 12 species of ixodid ticks belonging to five genera were identified (Table 1, Fig. 1). Of the 16 mammalian host species, seven were free from any tick infestation. Amongst the iden- tified tick species, Haemaphysalis (Kaiseria- na) bispinosa Neumann, 1897 was the most prevalent species while Rhipicephalus san- guineus s.l. Latreille, 1806 was the least. Ticks belonging to the genus Hyalomma, Ixodes and Dermacentor were not identified in the pre- sent study. Amongst the tick species collected from reptiles, Amblyomma gervaisi Lucas, 1847 was retrieved from three species of pythons, i.e., at a time only one species of tick was collected from each python. Sambar, spotted, barking and mouse deers, wild pig, tiger and leopard were infested with more than one species of tick. A minimum of three species of ticks were retrieved from each of the 11 examined sambar deers, with a total of six species identified in them. All the wild pigs examined were par- asitized by A. integrum and R. haemaphy- saloides with the exception R. sanguineus s.l. found only in one animal. In all mamma- lian species, ticks were present throughout the body with more infestation on the external surface of the ear pinna and neck. In snakes, ticks were attached between and below the scales with no ticks were seen attached to the ventral aspect of the body. Only A. gervaisi Lucas, 1847 could be collected from monitor lizards. Male A. gervaisi was collected from the lateral side of the body, axilla of the left forelimb and the periphery of cloaca / ventral depression just behind cloaca. Female ticks were collected from the axillary region and between the toes of forelimbs. Table 1. Species of ticks detected on the wild mammals and reptiles of Wayanad region of Western Ghats No. Name of wild animal host examined Number of host examined Tick Species No. of tick collected Life stage (Nymph (N) /Adults(A)) 1 Sambar deer [Cervus unicolor Kerr, 1792] 11 Amblyomma integrum Karsch, 1879 Rhipicephalus (Boophilus) annulatus Say, 1821 R. haemaphysaloides Supino, 1897 H. (Kaiseriana) bispinosa Neumann, 1897 Haemaphysalis (Kaiseriana) spinigera Neumann, 1897 H. (K.) shimoga Hoogstraal and Trapido, 1964 85 36 40 96 35 27 10 Adult Adult Nymph Adult Adult Adult Adult 2 Spotted deer [Axis ax- is (Erxleben, 1777)] 2 R. (B.) annulatus Say, 1821 R. haemaphysaloides Supino, 1897 H.(K.) bispinosa Neumann, 1897 10 14 26 Adult Adult Adult 3 Barking deer [Muntiacus muntjak (Zimmermann, 1780)] 4 R. (B.) annulatus Say, 1821 R. haemaphysaloides Supino, 1897 H.(K.) bispinosa Neumann, 1897 5 12 42 Adult Adult Adult 4 Mouse deer [Moschio- laindica (Gray, 1852)] 2 H.(K.) bispinosa Neumann, 1897Haemaphysalis (K.) spinigera Neumann, 1897 20 5 Adult Adult 5 Gour [Bos frontalis Lambert, 1804] 1 H. (K.) shimoga Hoogstraal and Trapido, 1964 5 Adult 6 Wild pig [Sus scrofa Linnaeus, 1758] 4 Amblyomma integrum Karsch, 1879 R. haemaphysaloides Supino, 1897 R. sanguineus s.l. Latreille, 1806 10 10 5 Adult Adult Adult http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 279 http://jad.tums.ac.ir Published Online: September 30, 2018 7 Tiger [Panthera tigris (Linnaeus, 1758)] 1 H. (K.) bispinosa Neumann, 1897 48 Adult 8 Leopard [Pantherapardus (Linnaeus, 1758)] 3 R. haemaphysaloides Supino, 1897 H.(K.) bispinosa Neumann, 1897 H. (Rhipistoma) indica Warburton, 1910 8 10 5 Adult Adult Adult 9 Malabar giant squirrel [Ratufa indica (Erxleben, 1777)] 2 H. (K.) spinigera Neumann, 1897 5 Adult 10 Leopard cat [Prionailurus bengalensis (Kerr, 1792)] 4 Nil Nil Nil 11 Bonnet macaque [Macaca radiata (Geoffroy Saint- Hilaire, 1812)] 7 Nil Nil Nil 12 Slender loris [Loris tardi- gradus (Linnaeus, 1758)] 1 Nil Nil Nil 13 Small Indian civet cat [Viverricula indica (Geof- froy Saint-Hilaire, 1803)] 1 Nil Nil Nil 14 Common Palm civet [Paradoxurus her- maphroditus (Pallas, 1777)] 1 Nil Nil Nil 15 Indian Giant Flying squir- rel [Petaurista philippen- sis (Elliot, 1839)] 1 Nil Nil Nil 16 Indian Grey Mangoose [Herpestes edwardsii (É. Geoffroy Saint-Hilaire, 1818] 1 Nil Nil Nil 17 Monitor lizard [Varanus bengalensis bengalensis (Linnaeus 1758)] 2 Amblyomma gervaisi Lucas, 1847 8 Adult 18 Python [Python mo- lurus Linnaeus, 1758] 5 A. gervaisi Lucas, 1847 A. javanense Supino, 1897 A. kraneveldi Anastos, 1956 5 4 3 Adult Adult Adult 19 Cobra [Naja na- ja Linnaeus 1758] 1 A. gervaisi Lucas, 1847 2 Adult 20 Indian Rat snake [Ptyas mucosa Linnaeus 1758] 3 A. pattoni Neumann, 1910 2 Adult 21 Russel viper [Daboia russelii Shaw and Nodder 1797] 1 Nil Nil Nil 22 Ceylone cat snake [Boiga ceylonensis (Günther, 1858)] 2 Nil Nil Nil 23 Montane Trinket Snake [Coelognathus Helena monticollaris (Schulz, 1992)] 3 Nil Nil Nil 24 Common Vine Snake [Ahaetulla nasu- ta Lacépéde 1789] 3 Nil Nil Nil 25 Checkered keel back [Xenochrophis pis- cator Schneider 1799] 3 Nil Nil Nil Table 1. Continued … http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 280 http://jad.tums.ac.ir Published Online: September 30, 2018 Fig. 1. Amblyomma gervaisi Male: dorsal view (a) ventral view(b), A. kraneveldi Female: dorsal view (c) ventral view (d), A. pattoni Male: dorsal view (e) ven- tral view (f), A. integrum Male: dorsal view (g) ven- tral view (h), A. integrum Female: dorsal view (i), A. javanense Female: dorsal view (j) ventral view (k), cleared specimen of Rhipicephalus (B.) annulatus Male: dorsal view (l), cleared specimen of Haema- physalis (Kaiseriana) bispinosa Male: ventral view (m), H. indica- Male: dorsal view (n) ventral view (o), H. shimoga Male: ventral view (p), H. (Kaiseriana) spinigera Male: ventral view (q): R. haemaphy- saloides Male: ventral view (r), R. sanguineus s.l. Male: ventral view (s). (Figures not to scale) Discussion Among the reported species of ticks from India, A. testudinarium, D. auratus, H. bispi- nosa, H. spinigera, H. intermedia, Hyalomma anatolicum anatolicum, H. marginatum isaaci, H. hussaini, H. detritum, H. kumari, B. mi- croplus, I. acutitarsus, I. ovatus, N. mon- strosum, R. haemaphysaloides and R. turani- cus are the most widely distributed ticks of cattle, buffalo, sheep and goat (37). Among this species, I. acutitarsus and I. ovatus were reported mainly from eastern and north-east- ern states of the country (19). Haemaphysa- lis bispinosa and R (B.) microplus are preva- lent throughout India, while H. spinigera is restricted to southern states, central zones, Oris- sa and Meghalaya (19). A total of 23 species of ticks were reported in domestic and wild animals from the different parts of Kerala State (19, 38, 39). The species of ixodid ticks reported from Kerala include, R.(B.) annula- tus, R.(B.) microplus, R.(B.) decoloratus, R. sanguineus s.l., R. haemaphysaloides, R. tu- ranicus, H. bispinosa, H. intermedia, H. acule- ata, H. cuspidata, H. knobigera, H. turturis, H. spinigera, H. anatolicum, H. marginatum isaaci, H. hussaini, A. integrum, N. mon- strosum, and N. keralensis (38, 39). A total of 35 species of ticks were reported from sambar deer throughout its native range and introduced habitats (40) which include 11 species from two extreme ends of India, south- ern (comprising Karnataka and Kerala states) and the northeastern ends (Assam). The pos- sibility of spreading of ticks from the north- eastern states to the southern state is very difficult as there is no practically animal movement practically between these states. Only five species of ticks were recorded from the Karnataka and one (H. sambar) from Kerala (40). In the present study, six species of ticks were recorded on sambar deer from Wayanad, Kerala, none of the specimen was conforming to the morphology of H. sambar. As well as, in the present study, R. (B.) an- nulatus recorded for the first time on sambar deer showing the status of a new host for this species. Among all the sambar deer exam- ined, at least three species of ticks were ob- served in each animal, and the presence of A. integrum was a constant feature. In the pre- sent study, R. (B.) annulatus, R. haemaphy- saloides and H. (K.) bispinosa were also rec- orded on both spotted deer (Axis axis) and http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 281 http://jad.tums.ac.ir Published Online: September 30, 2018 barking deer as previously reported by Miran- puri (41). The presence of A. integrum, R. haema- physaloides and R. sanguineus s.l. in wild boars observed in the present study so agrees with the tick-host relationship (41). Less fre- quency of R. sanguineus s.l. in wild pig in the present study corroborates with previous report (42). Sus scrofa is a major host for adults of D. auratus, which also infests bear, rhinoceros and deer of primary and second- ary forests (mostly at altitude below 400m) of India, Sri Lanka, Nepal, Bangladesh, Burma, Thailand, Vietnam, Laos, Peninsular Malaysia, and Sumatra (43). We could not record this species from any wild animals. However, an adult male D. auratus was re- cently recorded from a man trekking through the forest of Wayanad region (44). Literature reveals H. (K.) bispinosa was not recorded from leopards and tigers in Western Ghats (45). However, Haemaphysalis sp. was reported in leopard at Nagpur, Maharashtra (46). Similarly, a distinctive small member of the H. (K.) bispinosa group, H. (K) rama- chandrai, was recorded on sambar deer, barking deer, chital deer, tiger, leopard, do- mestic cattle, buffalo and goats from forest lowlands of the Himalayan foothills of India and Nepal. H. bipsinosa is a ubiquitous medi- cally important parasite of domestic animals in India transmitting various diseases in do- mestic animals (19). The present finding of R. haemaphysaloides and H. (Rhipistoma) indica infestations in leopard corroborated with previous findings (36, 41). Four species of ticks were collected from four out of the eight species of snakes exam- ined in the present study. Based on the avail- able reports, A. javanense and A. kraneveldi on python and A. pattoni on Indian rat snake are the new records. Recent survey on ticks of snakes in the north Western Ghats record- ed only A. gervaisi on two species of snakes viz., Indian rat snake and spectacled cobra. Amblyomma gibsoni, A. varanensis and A. ger- vaisi were previously reported in monitor liz- ard (34, 47, 48). However, A. gervaisi was the only tick species observed in monitor lizards in the present study. The major infectious organisms of rumi- nants transmitted by common tick species in India are, Theileria annulata (transmitted by Hyalomma anatolicum and H. marginatum isaaci), Babesia bigemina, Anaplasma mar- ginale and Ehrlichia bovis (transmitted by R. (B.) microplus), B. motasi (transmitted by Haemaphysalis spp.) and B. ovis (transmitted by Rhipicephalus spp.) (37). The occurrence of T. annulata and B. bigemina was reported from the whole India while A. marginale, E. bovis and E. phagocytophila is confined to some restricted zones. Hepatozoon canis, Ehr- lichia canis, Mycoplasma haemocanis, Ana- plasma platys, B. vogeli and B. gibsoni are the TBD pathogens found infecting dogs in India due to the potential tick vectors, Rhip- icephalus (most commonly) and /or Haema- physalis ticks (49). In humans, Lyme disease, Kyasanur For- est Disease (KFD), Crimean-Congo Hemor- rhagic Fever (CCHF) and babesiosis are some of the important tick borne zoonoses report- ed from India (25, 50). Human babesiosis and CCHF were reported from Gujarat state (50, 51) of northern India. Kyasanur forest disease (KFD) was originally recognized as a febrile illness in the Shimoga district of Kar- nataka state of India (52). During 2013, only single case of Kyasanur forest disease (KFD) was reported without any mortality in hu- mans from Wayanad, Kerala (26) while elev- en confirmed cases, one death and eight sus- pected cases were already reported in the month of February 2015 (27). The principal vector for KFD, H. (K.) spinigera was identified in the present study. Dermacentor auratus reported previously from a human (44) from Wayanad can also act as vector for the disease. Hence, it could be possible that KFD may spread into more and more areas of Kerala in future. Lyme disease in humans was documented from http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … 282 http://jad.tums.ac.ir Published Online: September 30, 2018 northern and north eastern India (53, 54). Lyme disease was reported recently from Wayanad too (26, 55) even though its tick vector could not be established. The information gathered in the present study will be useful for public health special- ists, medical professionals, zoologists, para- sitologists and other professionals for de- signing tick control strategies for the entire southern India to prevent the possible emer- gence of newer tick borne diseases especial- ly zoonoses. Conclusions Twelve species of ticks from wild mam- mals and reptiles were recorded from south- ern India suggesting the contribution of wild life for tick abundance and prevalence in the tick fauna of this region. Haemaphysalis (K.) bispinosa was common among the wild un- gulates and the large carnivores. As well as, H. (K.) spinigera, the principal vector for Ky- asanur Forest disease (KFD) was identified in the present study. The data presented will be helpful for designing ticks and tick-borne disease control programs in this region of the country. Acknowledgements Financial supports from Indian Council of Agricultural Research (NAIP C2066, NFBS FARA/BSA-4004/2013-14, NASF/ABA-6015/ 2016-17) and Kerala State Council for Science, Technology and Environment (022/YIPB/KBC/ 2013 and 010/14/SARD/13/CSTE) are thank- fully acknowledged. We report no conflict of interests of any kind among the authors. References 1. Sonenshine DE (1991) Biology of Ticks. Volume 1. Oxford University Press, New York. 2. Walker DH, Fishbein DB (1991) Epidemio- logy of rickettsial diseases. Eur J Epi- demiol. 7(3): 237–245. 3. 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