New Records of Small Mammal Hosts for Five Ectoparasite Species from Sri Lanka

Ticks and fleas act as vectors for a number of zoonotic diseases, hence are medically important. Handful of studies carried out in Sri Lanka to date have reported 6 tick species and 11 flea species from murine rodents and shrews. Here, we report ticks and fleas infesting murine rodents and shrews collected from 18 selected sites in two districts in Sri Lanka, Kurunegala and Kandy. Two species of ticks (Rhipicephalus haemaphysaloides and Haemaphysalis spinigera), an unidentified Haemaphysalis larva and a flea Xenopsylla cheopis were found from Kurunegala. From Kandy, four species of ticks (R. haemaphysaloides, H. spinigera, Ixodis ceylonensis and Dermacentor auratus) and three species of fleas (X. cheopis, Stivalius phoberus and Stivalius aporus) were collected. Rhipicephalus haemaphysaloides was recorded from Rattus rattus, Bandicota indica, Mus fernandoni, Golunda ellioti and Suncus murinus; H. spinigera from R. rattus, B. indica and S. murinus; I. ceylonensis from M. cervicolor and R. rattus; D. auratus from R. rattus; both X. cheopis and S. phoberus were collected only from R. rattus; S. aporus from R. rattus and M. fernandoni. Though, all species of parasites reported here have been previously recorded from Sri Lanka, D. auratus and H. spinigera are reported for the first time from murine rodents and shrews. We also report here several new host records for the country: R. haemaphysaloides from B. indica, G. ellioti and S. murinus; H. spinigera from B. indica and S. murinus; D. auratus and S. aporus from R. rattus; larvae of I. ceylonensis from M. cervicolor.


INTRODUCTION
Ticks and fleas are medically important ectoparasitic arthropods infesting humans and other animals such as mammals, birds, reptiles and amphibians (Guglielmone et al., 2010). Fourteen genera and 702 species of ticks are recognized globally. They transmit a great variety of infections than any other blood sucking arthropod, and are only second to mosquitoes in terms of public health and veterinary importance (Mullen and Durden, 2002). Other than disease transmission, their attachment causes local inflammation and even anaphylactic reactions, toxicoses and paralysis in both humans and animals (Mullen and Durden, 2002;Radostits et al., 2006). Intra aural migration of ticks termed as otoacariasis in humans is a serious problem in rural areas, which has been reported from south Africa, south America and Asia including Sri Lanka (Dilrukshi et al., 2004;Somayaji and Rajeshwari, 2007). Otoacariasis in animals may lead to severe bacterial infections. Debilitation and death caused by hemoparasitism, toxicoses and paralysis are major causes contributing to the economic losses in livestock industry (Mullen and Durden, 2002).
From Sri Lanka, 35 species of ticks (Seneviratna, 1965;Walker et al., 2000;Dilrukshi, 2006;Kolonin, 2009) have been recorded. Most comprehensive study on ticks to date is a survey of hard ticks on both wild and domestic species of mammals, birds and reptiles around the country by Seneviratna (1965). Later studies have concentrated more on a single host species or a group. Among them are ticks of goats in the dry zone (Halim et al., 1983), cattle ticks of Sri Lanka (Dilrukshi, 2006) and ticks of murine rodents and shrews (Yathramullage et al., 2014). One recent large scale study reported ticks infesting domestic and wild mammals and humans around the country (Liyanarachchi et al., 2013 and. Ceylon Journal of Science 45(3) 2016: 29-38 DOI: http://doi.org/10.4038/cjs.v45i3.7398

RESEARCH ARTICLE
Fleas mainly infest mammals and birds. There are 246 genera and about 2,575 species and sub species of fleas recorded worldwide. They are vectors for many bacterial diseases such as plague, Murine typhus, Q fever and tularemia around the world (Stenseth et al., 2008). They also serve as intermediate hosts of tape worm species that occasionally infect humans such as Diphilidium caninum of dogs and cats and Hymenolepis diminuta of rodents. They also cause flea bite allergies, dermatitis in humans and animals, and anemia in animals when present in large numbers (Mullen and Durden, 2002).
In Sri Lanka, 20 species of fleas have been recorded (Iyengar, 1973). Much of the contribution to the knowledge on indigenous flea fauna in Sri Lanka was from W. W. A. Phillips (1980), a prominent Zoologist who worked on mammals and birds of Sri Lanka in the 1930s. He recorded 11 species of fleas from 16 species and subspecies of rodents and shrews, during the course of his mammal surveys (Phillips, 1980). New flea species, Nosopsyllus ceylonensis and some other already known species collected during Phillips's surveys have been described or reported by Smith (1953). Many publications are also available on rat fleas as a result of extensive plague investigations carried out throughout the country during the early part of 20 th century (Hirst, 1933). A smaller study on ectoparasites of rats recorded four species of fleas from R. rattus kandianus (Thompson, 1938). A recent study reported two species of fleas from three species of endemic small mammals; Stivalius aporus from Suncus montanus and Mus fernandoni; Nosopsyllus tamilanus from Solisorex pearsoni (Yathramullage et al., 2014).
Here, we report species of ticks and fleas collected from murine rodents and shrews from two districts in Sri Lanka.

Study sites
Parasites were collected during the period between 2013 to 2014. Small mammals were captured using 40 mesh traps placed in each site for four consecutive days. Eight localities were sampled in Kurunegala: Bogollagama (07˚47'N, 80˚10'E, elevation 80m), Herathgama (07˚52'N,

Collection of parasites and identification
Parasites were collected by combing hair and manually picking using a pair of forceps and stored in 70% alcohol. They were observed under stereo (×45) and light microscopes (×400). Some specimens were mounted on glass slides with or without potassium hydroxide clearing for identification and also to keep as reference material. All ticks and fleas and their speciesspecific characteristics and other important structures were photographed using a digital camera connected to stereomicroscope and Zeiss light microscope and imaging system. Measurements were taken using photomicrographs in image J software. Ticks were identified with the help of taxonomic keys and species descriptions in Kirwan (1935); Kohls (1950); Trapido et al. (1964); Seneviratna (1965); Rajagopalan and Boshell (1966); Walker et al. (2000) and fleas with Hopkins and Rothschild (1953) and Mardon (1981).

DISCUSSION
All the tick and flea species recorded here have been previously reported from Sri Lanka, but D. auratus and H. spinigera are reported for the first time from murine rodents and shrews. We also report new host species for R. haemaphysaloides, H. spinigera, I. ceylonensis, D. auratus and S. aporus. Of the ticks, R. haemaphysaloides have previously been reported from many domesticated and farm animals such as dog, cat, cattle, water buffalo, sheep, goat, pig, horse, chicken, and from wild animals such as blacknaped hare, wild boar, mouse deer, barking deer, spotted deer, pangolin, wild buffalo, bear and owl. Immature stages of this tick species were recorded from humans (Dilrukshi, 2006, Liyanarachchi, 2014. Through the present study, three new host species are added to the above list; B. indica, G. ellioti and S. murinus. Outside Sri Lanka R. haemaphysaloides has been recorded in South and South East Asian countries and China; adults from large and middle sized mammals and immature stages from small mammals including rodents and insectivores (Kolonin, 2009). Haemaphysalis spinigera has been previously recorded from domesticated animals like dog, cat, cattle, chicken and in wild animals such as leopard, sloth bear, forest wagtail, porcupine and sambar from Sri Lanka (Senevirathna, 1965;Dilrukshi, 2006;Liyanaarachchi, 2013 and. Bandicota indica and S. murinus are new hosts reported here for this species. In Nepal, India, China and Vietnam, adults of H. spinigera have been reported from large ungulates, carnivores and immature stages from small and middlesized mammals and birds. Ixodis ceylonensis is a species described from Sri Lanka (Kohls, 1950), which was first reported from mongoose, Herpestes smithii zeylanicus collected by W. W. A. Philips (1946). It was later recorded from R. rattus kandianus, Ceylon rudi mongoose (Senavirathna, 1965), Crocidura miya, S. montanus and Solisorex pearsoni (Yathramullage et al., 2014). From India it was reported from Rattus sp., Bandicota sp., Mus booduga, G. ellioti, jungle cat, leopard cat, wild monkey and squirrel. The chief host of I. ceylonensis was identified as S. murinus in India (Rajagopalan and Boshell, 1966). Here we report a new host for this species, M. cervicolor. Dermacentor auratus has been previously recorded from dog, chicken, wild boar, Sambar and sloth bear from Sri Lanka. Wild pig Sus scorfa is considered as the main host of adult D. auratus. In the present study we found D. auratus nymph from R. rattus in Hantana area, where wild pigs are abundant, which may be hosting adult ticks. Outside Sri Lanka D. auratus has been recorded from south and south east Asian countries and China. Other than in wild pigs it is also found in domestic pig, bear, rhinoceros and deer (Kolonin, 2009). Immature stages are known to be parasitic chiefly on Rattus spp., carnivores, badgers, civets, mongooses, cats, leopards and tigers.
Some of the above reported species are known to act as vectors for many human diseases and hence, this report is of medical importance too. Both R. haemaphysaloides and H. Spinigera have been identified as principal vectors for Kyasanur Forest Disease (Kolonin, 2009), a viral disease endemic in India. Immature stages of D. auratus frequently parasitize humans and cause paralysis and facial palsy and it is a major species causing intra aural tick infestation. It is also identified as a carrier of Kyasanur forest disease virus, Rickettsia and Anaplasma strains (Hoogstral and Wassef, 1985;Ajithkumar et al., 2012).
All flea species found in the present study have been reported previously from rodents and shrews studied here. Stivalius aporus, a flea which was originally described from India from a field rat, was later found from several other murine rodents (Millardia meltada, R. rattus, Rattus nitidus), shrews (Suncus sp.), domestic cat, tree shrews and squirrel, Callosciurus flavimanus (Mardon, 1981). In Sri Lanka it has been recorded from four murine rodents, Rattus ohiensis, M. booduga, M cervicolor, M. fernandoni and a shrew, S. montanus (Hirst, 1933;Phillips, 1980;Mardon, 1981;Yathramullage et al., 2014). Stivalius phoberus is an endemic flea. It has been recorded from murine rodents (R. rattus, R. ohiensis, R. montanus, M. mayori, M. musculus and B. indica), S. montanus, squirrel Funambulus palmarum and jungle cock (Hirst, 1933;Smit, 1953;Mardon, 1981, Yathramullage et al., 2014. Xenopsylla cheopis, the oriental rat flea had originated from Egypt and distributed worldwide through ships carrying rats. Rattus rattus and R. norvegicus are the main hosts of X. cheopis, however it also feeds on primates including humans. It is a vector for Yersina pestis, causative agent for plague, which has caused huge historic pandemics and epidemics, still present in western United States of America and in parts of Asia and Africa. It is the main vector for Rickettsia typhi, the causative agent for Murine typhus and carries tapeworm of rats and mice, H. diminuta (rat tapeworm) and Hymenolepis nana (mouse tapeworm).