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Home , Amblyomma gervaisi, Rat snake, Sibynophis subpunctatus, Trinket snake, Uropeltidae, Uropeltis macrolepis

SAMPLING,DISTRIBUTION,DISPERSAL Infestation on Wild in Northern Part of of

PRANAV PANDIT,1,2 RUTA BANDIVDEKAR,1,2 G. GEEVARGHESE,3 1 3,4 SATISH PANDE, AND OMKAR MANDKE Downloaded from https://academic.oup.com/jme/article/48/3/504/882162 by University Of California user on 09 June 2021

J. Med. Entomol. 48(3): 504Ð507 (2011); DOI: 10.1603/ME10164 ABSTRACT In total, 167 individuals of 30 of snakes belonging to 22 genera and Þve families were examined for tick infestation from November 2008 to March 2010. Only two species of snakes, mucosa (L., 1758) (Indian rat ) and Naja naja (L., 1758) (spectacled cobra), were found infested by . All ticks collected were identiÞed to be gervaisi [previously Aponomma gervaisi (Lucas, 1847)]. The average prevalence of these ticks on Indian rat snakes (n ϭ 48) was 29.16%, with abundance of 7.02 ticks per individual; on spectacled cobras (n ϭ 20), average prevalence was 30.00%, with abundance of 6.9 ticks per individual. The nymphs and males were predominant. All the ticks were found on the dorsal aspect of the body of the snake, and no ticks were recorded on the head, tail, or ventral body. The rate of tick infestation was highest in scrubland and was lowest in evergreen forests. Female Indian rat snakes showed higher tick infestation rates than male Indian rat snakes. Using MannÐWhitney U test, we found that longer snakes of both species had signiÞcantly higher rate of tick infestation in both the species of snakes.

KEY WORDS Amblyomma, Aponomma, Indian , spectacled cobra

Hard ticks are hematophagus parasites that are im- Stenos et al. 2003). Aponomma ticks are known to portant vectors of many viral, bacterial, rickettsial, and cause tick paralysis in the Coluber constrictor priapus protozoal diseases of humans and domestic . (southern black racer) (Hanson et al. 2007). They are known to parasitize a variety of vertebrate Aponomma ticks are vectors of Aeromonas hydrophilia hosts, including wild animals. Hard ticks belong to that causes bacterial stomatitis and pneumonia in subfamily Ixodoidea, order Acarina, class Arachnida snakes (Marcus 1981). The aim of the current study is (Sharif 1928). Although there are numerous articles on to record the prevalence of infestation of tick on the infestation of ticks on different hosts, both domestic different species of wild snakes found in western Ma- and wild animals, information on tick infestation on rep- harashtra and Karnataka, India. tiles is rare or scanty in India. Ticks found on generally belong to Amblyomma (formerly Materials and Methods Aponomma). The Life cycle of Aponomma lucasi War- burton has been studied under laboratory conditions Study Area. The study was conducted in the north- (Bhat and Nikam 1986). In the previous reports from ern part of western Ghats area from November 2008 India by Geevarghese and Dhanda (1995) and Ghosh et to March 2010, covering different seasons, i.e., winter, al. (2007), Aponomma gervaisi (Lucas, 1847), Aponomma summer, and monsoon. The study localities included leave Neumann, Aponomma lucasi Warburton, and Pune (18Њ 31Ј6.34Љ N, 73Њ 51Ј24.14Љ E), Saswad (18Њ Aponomma pattoni (Neumann) have been recorded on 20Ј34.60Љ N, 74Њ 1Ј47.52Љ E), Lonavala (18Њ 44Ј53.00Љ N, hosts. Some of these species are either synonyms 73Њ 24Ј26.00Љ E), Jejuri (18Њ 16Ј35.85Љ N, 74Њ 9Ј43.79Љ E), or invalid as per the recent classiÞcation (Horak et al. Tahmini (18Њ 26Ј48.85Љ N73Њ 25Ј49.96Љ E), Shirwal (18Њ 2002, Klompen et al. 2002, Barker and Murrell 2004). 9Ј9.24Љ N, 73Њ 58Ј46.94Љ E), Amboli (15Њ 57Ј52.98Љ N, 74Њ Human pathogens such as Coxiella burneti and Rick- 0Ј12.86Љ E), Bhimashankar (19Њ 4Ј21.11Љ N, 73Њ 32Ј9.81Љ ettsia honei are known to be transmitted by Aponomma E), Badalapur (19Њ 9Ј0.00Љ N, 73Њ 16Ј0.00Љ E), Kas (17Њ ticks (now Amblyomma); these ticks are known to 41Ј60.00Љ N, 73Њ 49Ј60.00Љ E) in Maharashtra state and infest humans accidentally in India (Tenderio 1953, Agumbe (13Њ 30Ј25.76Љ N, 75Њ 5Ј40.89Љ E) in Karnataka Stephen and Rao 1979, Prakashan and Ramani 2003, state of India. In brief, the study area covered different , including evergreen forest, semi-evergreen 1 ELA Foundation, C-9, Bhosale Park, Sahakar Nagar, Pune-411 009, forest, dry deciduous forest, scrubland, and agricul- India. tural and human habitations. 2 These authors contributed equally to this work. Collection of Ticks. Snakes were randomly sampled 3 National Institute of Virology, 20-A, Dr. Ambedkar Rd., Pune-411 001, India. for tick infestation as and when they were rescued 4 Corresponding author, e-mail: [email protected]. with the help of local snake rescuers from different

0022-2585/11/0504Ð0507$04.00/0 ᭧ 2011 Entomological Society of America May 2011 PANDIT ET AL.: TICK INFESTATION ON SNAKES 505

Table 1. Snake species collected, -wise, with prevalence of tick infestation

No. snake Prevalence of Habitat Snake speciesa specimens A. gervaisi (%) Dry deciduous forest 9 IRS, BR, CTS, RV, SK 11.111 Evergreen forest 53 BCS, MPV, CVS, BPV, CKS, BTS, FCS, LSNS, MS, PS, UB, SC, YSWS 0 Human settlement 54 CKS, BR, LSS, SK, CTS, CWS, DBS, GK, RIS, RV, SC, RKS, SSV 9.260 Scrubland 40 BR, BCS, CKr, CSB, IRS, RSB, SSV, SC, SK 27.5 Semi-evergreen forest 11 BPV, BK, BTS, GK, IRS, MTS, SC 27.272

a CSB, common sand boa (Gongylophis conicus); RSB, red sand boa (Eryx johnii); CKS, common kukri snake (Oligodon arnensis); BR, banded racer (Argyrogena fasciolata); BCS, BeddomeÕs cat snake (Boiga beddomei); BK, BeddomeÕs keelback (Amhiesma beddomei); BTS, common Downloaded from https://academic.oup.com/jme/article/48/3/504/882162 by University Of California user on 09 June 2021 bronzeback tree snake (Dendrelapis tristis); SK, Striped keelback (Amphiesma stolatum); CKS, cheackered keelback (Xenochrophis piscator); FCS, ForstenÕs cat snake (Bioiga forsteni); CTS, common ( helena helena); CVS, common vine snake (Ahaetulla nasuta); CWS, common wolf snake (Lycodon aulicus); DBS, DumerilÕs black-headed snake ( subpunctatus); GK, green keelback (Macropisthodon plumbicolor); IRS, Indian rat snake (); LSNS, lesser striped necked snake (Liopeltis calameria); MTS, montane trinket snake (Coelognathus helena monticollaris); RKS, RussellÕs kukri snake (Oligodon taeniolatus); YSWS, yellow-spotted wolf snake (Lycodon flavomaculatus); CKr, common krait (Bungarus caeruleus); SC, Spectacled cobra (Naja naja); LSS, large-scaled shieldtail ( macrolepis macrolepis); MS, mahabaleshwar shiledtail ( mahabaleshwarlensis); PS, PhipsonÕs shieldtail (Uropeltis pepsonii); UB, shieldtail snake (Uropeltis bicatinata); BPV, bamboo pit viper (Trimeresurus gramineus); MPV, Malabar pit viper (Trimeresurus malabaricus); RV, RussellÕs viper (Daboia russelii); SSV, saw-scaled viper (Echis carinatus). localities. Description of various habitats from where Differences in the prevalence of Ptyas mucosa (L., the snakes were examined and other details were 1758) (Indian rat snake) and Naja naja (L., 1758) recorded in a Þeld book. Snake species were identiÞed (spectacled cobra) infestation, prevalence in males with the help of Þeld guides (Whitaker and Captain and females of Indian rat snake, and prevalence of 2004) and from prior experience. The length, sex, and infestations in different habitats with the overall prev- body parts where ticks were collected, and certiÞed alence observed were compared using Fisher exact snake rescuerÕs names were recorded. Overall body test. Lengths of Indian rat snakes and spectacled co- condition, including emaciation, wounds, and status of bras were correlated with presence of tick infestation molt of the snake, also was noted. Emaciated snake was using MannÐWhitney U test. Statistical analyses were easily identiÞed by palpating the whole body for mus- carried out using the XLSTAT statistical package and cle thickness. Snakes during molt were reexamined for the results were considered signiÞcant at P Ͻ 0.05. tick infestation before and after the molting. Each rescued snake was carefully restrained phys- Results ically by experience rescuers, and head, body, and tail (ventral and dorsal sides) were carefully examined for Representativeness of Samples and Prevalence. We ticks or any other ectoparasitic fauna, such as other examined 167 snakes of 30 species belonging to 22 acarines or insects, lodged in between the scales genera and Þve families (, , Colu- within 24 h of rescue. All the ticks present on the body bridae, , and ) for tick infestation. of the snakes were collected and preserved in 70% Habitat, number of snakes and species sampled, and ethanol for later identiÞcation of species and life stage. number of ticks collected from all the localities are Photographic documentation was done to examine depicted in Table 1. the lodging habits of ticks. All snakes were released by Only two species, Indian rat snake and spectacled rescuers. cobra, were found to be positive for tick infestation in Statistical Analysis. Tick prevalence was deter- this study. No other ectoparasitic infestations were mined according to the equation [(no. of parasitized found. All ticks collected from snakes were identiÞed snakes)/(total no. of snakes] ϫ 100, and tick abun- as A. gervaisi (Fig. 1a and b). The prevalence and dance was determined according to the equation abundance of tick infestation for Indian rat snake was [(no. of ticks)/(no. of snakes)] (Margolis et al. 1982). 29.16% and 7.02 (n ϭ 48), whereas for spectacled

Fig. 1. Photos of A. gervaisi. (a) A. gervaisi female dorsal view. (b) A. gervaisi female ventral view. (c) A. gervaisi lodged in between scales of Indian rat snake. (Photo credit: Rohan Pandit; online Þgure in color.) 506 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 48, no. 3 Downloaded from https://academic.oup.com/jme/article/48/3/504/882162 by University Of California user on 09 June 2021 Fig. 2. (a) Box plot showing lengths in meters of infested and noninfested Indian rat snake. (b) Box plot showing lengths in meters of infested and noninfested spectacled cobra. cobra, the values were 30.00% and 6.9, respectively species, Indian rat snake and spectacled cobra, were (n ϭ 20). The prevalence in female Indian rat snakes found to be infested by ticks. It is not still clear (50.0%; n ϭ 22) was found to be signiÞcantly higher whether other species of snakes are refractory or sus- than that of male Indian rat snakes (11.76%; n ϭ 17) ceptible. Ticks adapted to speciÞc habitat type en- (P ϭ 0.0183). Lengths of the Indian rat snakes and counter only those vertebrates adapted to the same spectacled cobras showed signiÞcant differences habitat (Mullen and Durden 2002). Thus, it might be when correlated with presence of infestation by using possible that there might be ecological reasons behind the MannÐWhitney U test (Indian rat snake U ϭ 366.0, host speciÞcity of A. gerviaisi to Indian rat snake and P ϭ 0.004; spectacled cobra U ϭ 73.50, P ϭ 0.007) (Fig. spectacled cobra, but the other reasons such as evo- 2a and b). An Indian rat snake that was about to molt lutionary history and ability of ticks to avoid host and was heavily infested with ticks was kept at a rejection must be studied in detail. In terms of ecology, proper place for its molting; 187 ticks were recorded the maximal parasitism was recorded on the snakes before molting. After molting, the snake retained all collected in scrublands (P ϭ 0.024) because Indian rat ticks. snake and spectacled cobra were scarcely sampled Tick Population Structure and Lodging Habits. Of from evergreen (P ϭ 0.004) and semi-evergreen for- 475 A. gervaisi ticks, 40.69% were males, 16.86% were ests (P ϭ 0.15) during the study. Snakes collected from females, 34.01% were nymphs, and 8.43% were larvae. urban areas also were infested. Ticks were lodged between the scales, with the ca- The difference in the prevalence of males and fe- pitulum safely hiding below a scale. When present, males of Indian rat snake might be because of their one to four ticks were observed per scale (Fig. 1c). breeding behavior where females are supposed to get Under one scale, either only males, only females, or more exposure to infestation. Other infestation studies both or mixed stages of adults, nymphs, and larvae conducted on ball python (Python regius) (Aubret et were recorded. All ticks were found on the dorsal al. 2005) and on western fence (Sceloporus oc- aspect of the body of the snake. Two ticks were pres- cidentalis) (Eisen and Eisen 1999) have indicated ent on the hood of a spectacled cobra. No tick was higher tick burden on males than females. In our study, found on the tail or ventral aspect of any snake. snakes having longer length were found to be more to Relationship Between Habitat and Prevalence. be infested in both Indian rat snake and spectacled The prevalence of infestation in different habitats (Ta- cobra. This difference might be because of the age ble 1), such as dry deciduous forest (11.11%; n ϭ where older snakes are more likely to be exposed to 9) (P ϭ 1.00), semi-evergreen forest (27.27%; n ϭ 11) infestation than the younger snakes. Degenhardt and (P ϭ 0.15), and human habitations (9.25%; n ϭ 54) Degenhardt (1965), while studying the tick infestation (P ϭ 0.80), was found to be almost similar with that of on snake subocularis, observed that juveniles prevalence observed irrespective of habitat (11.97%; and younger snakes are less likely to be found infested n ϭ 167). However, prevalence in evergreen forest with tick infestation. Our study has shown that the (0.0%; n ϭ 53) (P ϭ 0.004) was signiÞcantly less, and molting habit of snakes does not affect tick parasitism prevalence in scrubland (27.5%; n ϭ 40) (P ϭ 0.024) because the number of ticks recorded before and after was signiÞcantly higher than the overall observed the molting remained the same. prevalence (11.97%; n ϭ 167).

Discussion Acknowledgments The study was intended to generate a baseline data We are grateful to the National Institute of Virology, Pune, of tick infestation on snakes found in northern part of for the help in laboratory work as well as the use of the western Ghats of India. Previous studies on tick in- museum facility for tick studies. We also are very thankful to A. C. Mishra (National Institute of Virology, Pune). We festation on reptiles are from monitor lizard (Varanus express our gratitude to the ELA Foundation for facilitating bengalensis) and Indian rat snake (Harakare et al. the Þeld data collection. We are thankful to Kavita Bandi- 2007a,b). This is the Þrst time that such kind of ex- vadekar (Deccan Ecolab) for laboratory facilities and to Vilas tensive surveillance has been carried out in India. 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