J -Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Vectors of …

Original Article Ixodid Tick Vectors of Wild Mammals and Reptiles of Southern

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 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 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, integrum, (Boophilus) annulatus, (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 , A. javanense and A. kraneveldi on python as well as A. pattoni on Indian rat 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 of (14, 15). Heavy infestation can ectoparasites of terrestrial vertebrates (1). They cause blood loss, reduced weight gain and are exclusively haematophagous in all feed- lowered milk production, even some tick spe- ing stages of their life cycle and have con- cies downgrade quality of hides (16). It is siderable medical and veterinary importance estimated that 80 per cent of world’s live- (2). Besides, causes great economic losses to stock population is suffering from the del- the livestock worldwide (3). Currently, 904 eterious effects of ticks (17). valid tick species have been listed through- Nearly, 106 Argasid and Ixodid tick spe- out the world (4–13). Ticks parasitize a wide cies infesting domestic, wild and game range of vertebrate hosts and transmit a vari- were documented from India (18). The ix- ety of pathogenic agents than any other group odid tick R. (B.) microplus is the most prev- 276 * Corresponding author: Dr Reghu Ravindran, E- http://jad.tums.ac.ir mail: [email protected] Published Online: September 30, 2018

J Arthropod-Borne Dis, September 2018, 12(3): 276–285 K. G. A Kumar et al.: Ixodid Tick Vectors of … alent and economically important species in- Materials and Methods festing livestock in India (19). On the global basis the losses incurred by livestock indus- Study area try due to TTBDs was estimated in the range Study are comprised of the entire Waya- of 14000 to 18000 million US $ / year (16). nad Wildlife Sanctuary (76º 02’ and 76º 27’ The annual cost of control of TTBDs in India East Longitude and 11º 35’ and 11º51’ North has been estimated as US $ 498.7 million (20). Latitude) and adjoining area in the Wayanad From the stand point of global biodiversity District of Kerala, India. conservation, ticks are playing a significant role, as they are able to affect the fitness of Animal and tick collection wild life species by spill over epizootic out- Wild animals are regularly brought to the breaks (21). Moreover, wild animals can act College of Veterinary and Animal Sciences, as reservoirs of infectious organisms and ticks Pookode by the officials of Department of can transmit them into domestic animals and Forest, Kerala for postmortem examination . Over the last few decades approxi- (animals died due to hunterattack, malicious mately 75 per cent of emerging diseases, in- poisoning or trapped), treatment and for health cluding zoonoses, having wildlife origin (22). checkup prior to release back into the forest. Western Ghats or the Sahyadri of south- Dead animals are surveyed in a short-time ern India with an area of 17,000km2 run par- window (within 24 hoursafter death). A total allel to the west coast of peninsular India of 46 wild mammals of 16 different species stretching from Cape Comorin (or Kanyakuma- and 23 reptiles of nine species were included ri) in the south to the Surat Dangs in Gujarat in the present study (Table 1). Body of these in the North. and livestock popula- animals was examined for the presence of tion existing as high densities in this region adults and engorged nymphs of tick. Adult (23, 24). Wayanad Wildlife Sanctuary (76º02’ ticks were collected in glass tubes and imme- to 76º 27’ East longitude and 11º 35’ to 11º diately transported to the parasitology labor- 51’ North latitude) with an area of 344 sq. km. atory for identification. If identification was is set lofty on the majestic Western Ghats with not possible on day of collection, the collect- altitude ranging from 650 to 1150m above ed ticks were stored for 24h in Boardman’s the sea level. Rich in wild animals biodiver- solution I (17% ethanol, 3% ether and 80% sity, the sanctuary is an integral part of the water). Then, for long term storage, they were Nilgiri biosphere reserve. transferred to solution II (80% ethanol, 15% Deadly tick borne viral infections like Ky- water, 5% glycerol) to which 1% chlorform is asanur forest disease (KFD) were reported from added to prevent the colour change. Engorged humans in Karnataka (25) and Kerala (26, 27) live nymphs were immediately placed in BOD with or without mortality and Crimean-Con- incubator at 28 °C and RH 85% for moulting go haemorrhagic fever (CCHF) from Gujarat to adults. while CCHFV-specific antibodies were detect- ed in human samples from Kerala (28). Pre- Tick identification vious reports on tick vectors of wildlife of The taxonomic identification was performed southern India are scanty. based on the morphology of adult ticks accord- Hence, an active surveillance was initiat- ing to standard keys and monographs (29–36). 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. 277 http://jad.tums.ac.ir Published Online: September 30, 2018

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Results tick. A minimum of three species of ticks were Out of 46 wild mammals and 23 reptiles, retrieved from each of the 11 examined sambar 12 species of ixodid ticks belonging to five , with a total of six species identified in genera were identified (Table 1, Fig. 1). Of the them. All the wild examined were par- 16 mammalian host species, seven were free asitized by A. integrum and R. haemaphy- from any tick infestation. Amongst the iden- saloides with the exception R. sanguineus tified tick species, Haemaphysalis (Kaiseria- s.l. found only in one animal. In all mamma- na) bispinosa Neumann, 1897 was the most lian species, ticks were present throughout the prevalent species while Rhipicephalus san- body with more infestation on the external guineus s.l. Latreille, 1806 was the least. Ticks surface of the ear pinna and neck. belonging to the genus , and In , ticks were attached between were not identified in the pre- and below the scales with no ticks were seen sent study. attached to the ventral aspect of the body. Amongst the tick species collected from Only A. gervaisi Lucas, 1847 could be collected reptiles, Lucas, 1847 was from monitor lizards. Male A. gervaisi was retrieved from three species of pythons, i.e., collected from the lateral side of the body, at a time only one species of tick was collected axilla of the left forelimb and the periphery of from each python. Sambar, spotted, barking cloaca / ventral depression just behind cloaca. and mouse deers, wild , tiger and leopard Female ticks were collected from the axillary were infested with more than one species of 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 Number of host Tick Species No. of tick Life stage host examined examined collected (Nymph (N) /Adults(A)) 1 Sambar deer [Cervus 11 Amblyomma integrum Karsch, 1879 85 Adult unicolor Kerr, 1792] Rhipicephalus (Boophilus) annulatus Say, 36 Adult 1821 R. haemaphysaloides Supino, 1897 40 Nymph H. (Kaiseriana) bispinosa Neumann, 96 Adult 1897 Haemaphysalis (Kaiseriana) spinigera 35 Adult Neumann, 1897 H. (K.) shimoga Hoogstraal and Trapido, 27 Adult 1964 10 Adult 2 Spotted deer [Axis ax- 2 R. (B.) annulatus Say, 1821 10 Adult is (Erxleben, 1777)] R. haemaphysaloides Supino, 1897 14 Adult H.(K.) bispinosa Neumann, 1897 26 Adult 3 Barking deer [Muntiacus 4 R. (B.) annulatus Say, 1821 5 Adult muntjak (Zimmermann, R. haemaphysaloides Supino, 1897 12 Adult 1780)] H.(K.) bispinosa Neumann, 1897 42 Adult 4 Mouse deer [Moschio- 2 H.(K.) bispinosa Neumann, 20 Adult laindica (Gray, 1852)] 1897Haemaphysalis (K.) spinigera 5 Adult Neumann, 1897 5 Gour [Bos 1 H. (K.) shimoga Hoogstraal and Trapido, 5 Adult frontalis Lambert, 1804] 1964 6 Wild pig [Sus 4 Amblyomma integrum Karsch, 1879 10 Adult scrofa Linnaeus, 1758] R. haemaphysaloides Supino, 1897 10 Adult R. sanguineus s.l. Latreille, 1806 5 Adult

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Table 1. Continued …

7 Tiger [Panthera tigris 1 H. (K.) bispinosa Neumann, 1897 48 Adult (Linnaeus, 1758)] 8 Leopard [Pantherapardus 3 R. haemaphysaloides Supino, 1897 8 Adult (Linnaeus, 1758)] H.(K.) bispinosa Neumann, 1897 10 Adult H. (Rhipistoma) indica Warburton, 1910 5 Adult 9 Malabar giant squirrel 2 H. (K.) spinigera Neumann, 1897 5 Adult [Ratufa indica (Erxleben, 1777)] 10 Leopard cat [Prionailurus 4 Nil Nil Nil bengalensis (Kerr, 1792)] 11 Bonnet macaque [Macaca 7 Nil Nil Nil radiata (Geoffroy Saint- Hilaire, 1812)] 12 Slender loris [Loris tardi- 1 Nil Nil Nil gradus (Linnaeus, 1758)] 13 Small Indian civet cat 1 Nil Nil Nil [Viverricula indica (Geof- froy Saint-Hilaire, 1803)] 14 Common Palm civet 1 Nil Nil Nil [Paradoxurus her- maphroditus (Pallas, 1777)] 15 Indian Giant Flying squir- 1 Nil Nil Nil rel [Petaurista philippen- sis (Elliot, 1839)] 16 Indian Grey Mangoose 1 Nil Nil Nil [Herpestes edwardsii (É. Geoffroy Saint-Hilaire, 1818] 17 Monitor lizard [Varanus 2 Amblyomma gervaisi Lucas, 1847 8 Adult bengalensis bengalensis (Linnaeus 1758)] 18 Python [Python mo- 5 A. gervaisi Lucas, 1847 5 Adult lurus Linnaeus, 1758] A. javanense Supino, 1897 4 Adult A. kraneveldi Anastos, 1956 3 Adult 19 Cobra [Naja na- 1 A. gervaisi Lucas, 1847 2 Adult ja Linnaeus 1758] 20 Indian Rat snake [Ptyas 3 A. pattoni Neumann, 1910 2 Adult mucosa Linnaeus 1758] 21 Russel viper [Daboia 1 Nil Nil Nil russelii Shaw and Nodder 1797] 22 Ceylone cat snake [Boiga 2 Nil Nil Nil ceylonensis (Günther, 1858)] 23 Montane Trinket Snake 3 Nil Nil Nil [Coelognathus Helena monticollaris (Schulz, 1992)] 24 Common Vine Snake 3 Nil Nil Nil [Ahaetulla nasu- ta Lacépéde 1789] 25 Checkered keel back 3 Nil Nil Nil [Xenochrophis pis- cator Schneider 1799]

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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- Fig. 1. Amblyomma gervaisi Male: dorsal view (a) ern (comprising Karnataka and Kerala states) ventral view(b), A. kraneveldi Female: dorsal view (c) ventral view (d), A. pattoni Male: dorsal view (e) ven- and the northeastern ends (Assam). The pos- tral view (f), A. integrum Male: dorsal view (g) ven- sibility of spreading of ticks from the north- tral view (h), A. integrum Female: dorsal view (i), A. eastern states to the southern state is very javanense Female: dorsal view (j) ventral view (k), difficult as there is no practically animal cleared specimen of Rhipicephalus (B.) annulatus movement practically between these states. Male: dorsal view (l), cleared specimen of Haema- physalis (Kaiseriana) bispinosa Male: ventral view Only five species of ticks were recorded (m), H. indica- Male: dorsal view (n) ventral view (o), from the Karnataka and one (H. sambar) from H. shimoga Male: ventral view (p), H. (Kaiseriana) Kerala (40). In the present study, six species spinigera Male: ventral view (q): R. haemaphy- of ticks were recorded on sambar deer from saloides Male: ventral view (r), R. sanguineus s.l. Wayanad, Kerala, none of the specimen was Male: ventral view (s). (Figures not to scale) conforming to the morphology of H. sambar. As well as, in the present study, R. (B.) an- Discussion nulatus recorded for the first time on sambar deer showing the status of a new host for this Among the reported species of ticks from species. Among all the sambar deer exam- India, A. testudinarium, D. auratus, H. bispi- ined, at least three species of ticks were ob- nosa, H. spinigera, H. intermedia, Hyalomma served in each animal, and the presence of A. anatolicum anatolicum, H. marginatum isaaci, integrum was a constant feature. In the pre- H. hussaini, H. detritum, H. kumari, B. mi- sent study, R. (B.) annulatus, R. haemaphy- croplus, I. acutitarsus, I. ovatus, N. mon- saloides and H. (K.) bispinosa were also rec- strosum, R. haemaphysaloides and R. turani- orded on both spotted deer (Axis axis) and cus are the most widely distributed ticks of 280 http://jad.tums.ac.ir Published Online: September 30, 2018

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barking deer as previously reported by Miran- vaisi were previously reported in monitor liz- puri (41). ard (34, 47, 48). However, A. gervaisi was The presence of A. integrum, R. haema- the only tick species observed in monitor physaloides and R. sanguineus s.l. in wild lizards in the present study. boars observed in the present study so agrees The major infectious organisms of rumi- with the tick-host relationship (41). Less fre- nants transmitted by common tick species in quency of R. sanguineus s.l. in wild pig in India are, Theileria annulata (transmitted by the present study corroborates with previous Hyalomma anatolicum and H. marginatum report (42). Sus scrofa is a major host for isaaci), Babesia bigemina, Anaplasma mar- adults of D. auratus, which also infests bear, ginale and Ehrlichia bovis (transmitted by R. rhinoceros and deer of primary and second- (B.) microplus), B. motasi (transmitted by ary forests (mostly at altitude below 400m) Haemaphysalis spp.) and B. ovis (transmitted of India, , Nepal, Bangladesh, by Rhipicephalus spp.) (37). The occurrence Burma, Thailand, , Laos, Peninsular of T. annulata and B. bigemina was reported Malaysia, and Sumatra (43). We could not from the whole India while A. marginale, E. record this species from any wild animals. bovis and E. phagocytophila is confined to However, an adult male D. auratus was re- some restricted zones. canis, Ehr- cently recorded from a man trekking through lichia canis, Mycoplasma haemocanis, Ana- the forest of Wayanad region (44). plasma platys, B. vogeli and B. gibsoni are Literature reveals H. (K.) bispinosa was not the TBD pathogens found infecting dogs in recorded from leopards and tigers in Western India due to the potential tick vectors, Rhip- Ghats (45). However, Haemaphysalis sp. icephalus (most commonly) and /or Haema- was reported in leopard at Nagpur, Maharashtra physalis ticks (49). (46). Similarly, a distinctive small member In humans, Lyme disease, Kyasanur For- of the H. (K.) bispinosa group, H. (K) rama- est Disease (KFD), Crimean-Congo Hemor- chandrai, was recorded on sambar deer, rhagic Fever (CCHF) and babesiosis are some barking deer, chital deer, tiger, leopard, do- of the important tick borne zoonoses report- mestic cattle, buffalo and goats from forest ed from India (25, 50). Human babesiosis lowlands of the Himalayan foothills of India and CCHF were reported from Gujarat state and Nepal. H. bipsinosa is a ubiquitous medi- (50, 51) of northern India. Kyasanur forest cally important parasite of domestic animals disease (KFD) was originally recognized as a in India transmitting various diseases in do- febrile illness in the Shimoga district of Kar- mestic animals (19). The present finding of nataka state of India (52). During 2013, only R. haemaphysaloides and H. (Rhipistoma) single case of Kyasanur forest disease (KFD) indica infestations in leopard corroborated was reported without any mortality in hu- with previous findings (36, 41). mans from Wayanad, Kerala (26) while elev- Four species of ticks were collected from en confirmed cases, one death and eight sus- four out of the eight species of snakes exam- pected cases were already reported in the month ined in the present study. Based on the avail- of February 2015 (27). The principal vector for able reports, A. javanense and A. kraneveldi KFD, H. (K.) spinigera was identified in the on python and A. pattoni on Indian rat snake present study. reported are the new records. Recent survey on ticks previously from a human (44) from Wayanad of snakes in the north Western Ghats record- can also act as vector for the disease. Hence, ed only A. gervaisi on two species of snakes it could be possible that KFD may spread into viz., Indian rat snake and spectacled cobra. more and more areas of Kerala in future. Lyme Amblyomma gibsoni, A. varanensis and A. ger- disease in humans was documented from 281 http://jad.tums.ac.ir Published Online: September 30, 2018

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