Introduction
There are around 250 species of wild carnivores distributed throughout the globe, out of which eight families comprising 60 species are found in India (Acharjyo 2002). The latin word “carnivores” means ‘meat-eater’ and the order Carnivora includes animals which predominantly eat meat as well as animals that occasionally eat meat and are in fact omnivores, such as bears and civets. Carnivores are kept in zoological gardens or wildlife parks for the purpose of education, exhibition and gene conservation (Khatun et al. 2014). The health of these animals requires special attention as conditions in captivity facilitate development of viral, bacterial and parasitic infections. These are of major concern as they pose a serious threat to the animals and persons who come in contact with the animals, like zoo keepers and veterinarians. In their natural habitat felids range over large areas, have low parasitic exposure and consequently low genetic resistance against parasitic infections (Raja et al. 2014). In captivity, for example in zoological gardens, the problem of parasitic infections in these animals can aggravate and pose a serious threat (Muoria et al. 2005). Parasitic infections are not only responsible for the morbidities of animals but heavier infections may actually be fatal (Chhabra & Pathak 2013). There is a woeful paucity of detailed studies of parasitic diseases of wild animals in India and mostly only case reports are available. This review compiles all available case reports and other studies of the parasitic diseases of wild felids in India.
Methods
A majority of the infections found in wild felids in captivity are helminthic infections. Therefore, we have analysed the incidences of parasitic infections by species. All the literature included in the analyses is listed and organized as per parasite species in the tables below.
Nematode infections
Toxocara infections
Toxocara, which were not identified to species level, have been found both during regular faecal examination and during necropsies in different parts of India. Health problems caused by various species of Toxocara were found predominantly in younger animals (Kumar & Rao 2003). Parasite eggs and adult parasites were recovered from Leopard Cats, Bengal Tigers, Asiatic Lions, Leopards and Snow Leopards. Necropsy, coprology and molecular identification reports of the parasites in wild felids are listed in Table 1.
Toxascaris leonina infections
Toxascaris leonina is an intestinal parasite commonly found in domestic cats, dogs and foxes, but related wild species also frequently get infected with the parasite and serve as definitive hosts for this species. Cases of various wild felids infected with T. leonina, including Jungle Cat Felis chaus, Royal Bengal Tigers Panthera tigris tigris, Asiatic Lions Panthera leo persica and Leopards Panthera pardus were documented from different parts of India. The parasite was found during coprology and at necropsy, but molecular confirmation of the parasite was carried out only once by Pawar et al. (2012) in Nehru Zoological Park, Hyderabad. The reports of this parasite from different zoological gardens of the country are listed in Table 2.
Ancylostoma (Hookworm) infections
Hookworm species including Ancylostoma and Uncinaria species have been recorded from wild felids throughout the globe and are currently known to occur in more than 24 wild animal species. Ten species of hookworms belonging to three genera of the family Ancylostomatidae have been found in a variety of felids. In the past, several new species of Ancylostomatidae were described from India: Maplestone (1939) described Uncinaria felidis from a Leopard Cat in Kolkata and Rao (1939) described Arthrocephalus gambiensis from Common Mongoose in Chennai. Dubey & Pande (1961) found that A. caninum could infect Jungle Cats by entering the lumen of the intestine from outside through the serosa. In 1985, Agarwal found Ancylostoma paraduodenale in the Asiatic Lion in India. The species was reported in felids for the very first time in 1951 by Biocca. This hookworm causes cutaneous larva migrans in humans, thus possesses significant zoonotic potential. The different reports of the hookworms are listed in Table 3.
Dirofilaria immitis infections
This parasite is also known as heartworm of dogs and requires mosquitoes as vectors for its transmission. The definitive host of the parasite is the dog, but it has also been found in wild felids including the Golden Cat, Royal Bengal Tigers, Asiatic Lions and Leopards. Reports of D. immitis infections in wild felids are listed in Table 4.
Other nematode infections
A number of other nematode parasites were less frequently recorded from wild felids. Baylis & Dubney (1922) reported Galonchus pernicious, a new species of hookworm from a leopard and this species was also found in the intestines of a lion cub (Patnaik et al. 1971). Eggs of spirurids and Capillaria species were found on faecal examination at Coimbatore and Thrissur (Varadhrajan et al. 2001). The only acanthocephalan from felids, an Oncicola species, was recorded in Assam (Patnaik & Acharjyo 1970). A list of parasites found sporadically and their hosts and the places of recovery is given in Table 5.
Trematode infections
Paragonimus infections
The most commonly encountered trematode infection in free-living and captive wild felids is paragonimiasis. Paragonimus was generally found embedded in cysts in the lung parenchyma and rarely caused the death of the infected animal. Histopathology showed bronchial hyperplasia due to mononuclear cell infiltration under the epithelial lining (Parihar & Shrivastava 1988). At Nandankanan Zoo, a necropsied Golden Cat and Royal Bengal Tiger were found to be infected with Paragonimus westermani (Rao & Acharjyo 1984, 1991). Cysts containing one or more reddish oval shaped flukes were macroscopically observed in one or both lungs in combination with patches of atelectasis and emphysema (Rao & Acharjyo 1991). P. westermani was also found during necropsies of tigers from different parts of the country including Corbett National Park in Uttar Pradesh (Arora & Das 1988), Kanha National Park in Madhya Pradesh (Parihar & Shrivastava 1988), Vandalur Zoological Park in Tamil Nadu (Latha et al. 2000) and Assam State Zoo in Guwahati (Nashiruddullah & Chakraborty 2001). The species was also reported from a Clouded Leopard by Hiregoudar & Pethkar (1970) and was found in a Leopard during post mortem and coprological examination in Thiruvananthapuram Zoo (Pythal et al. 1993; Varadhrajan & Pythal 1999).
Sano et al. (1994) recovered Paragonimus eggs from four tigers and one Jungle Cat at Kanha National Park. These eggs differed from the eggs of P westermani and raised the question of the existence of a new species of Paragonimus in India.
In 1970, the trematode Euparyphium malayanum was found at the necropsy of a Jungle Cat in Baranga Zoo in Odisha (Patnaik & Acharjyo). Coprological evidence of Euparyphium species was also found recently in Nandankanan Zoo (Mahali et al. 2010). Nanophyetes salmincola was identified in faecal examinations of lions and leopards at Maharajbagh Zoo in Odisha (Dhoot et al. 2002) and Schistosoma species eggs were found during faecal examination of lions at Nandankanan Zoo in Odisha (Mahali et al. 2010). Clinical cases of schistosomiasis were reported from lions of Maharashtra (Shrikhande et al. 2002).
Cestode infections
The most common cestode infection encountered in wild felids was echinococcosis. Both adult and metacestode stages were recovered from captive and rescued free-ranging wild felids. The adult stages cause catarrhal enteritis in wild animals and the parasite deserves particular attention due to its significant zoonotic potential (Acharjyo 2004). Easwaran et al. (2003) found Echinococcus granulosus and Taenia species during necropsies in Leopard Cats at Thekkady in Kerala. Pande et al. (1970) recorded Spirometra species from the lions of the zoological garden of Lucknow. Taenia pisiformis and Spirometra erinaceae were the two cestode species reported in Bengal Tigers at Baranga Zoo (Patnaik & Acharjyo 1970) and Taenia taeniformis was reported from the tigers of Corbett National Park (Gaur et al. 1980). Sharma et al. (1983) found Taenia jaipurensis in lions in India. Diphyllobothrium species infection was recorded during the post mortem of a male leopard at Thiruvananthapuram Zoo (Varadhrajan & Pythal 1999). Diphyllobothrium latum was the most common species of cestode reported at faecal examination of leopards and was found at several places, for example, in Thrissur (Varadharajan et al. 2001) and Maharajbagh zoo in Nagpur (Dhoot et al. 2002). Fecal examination of a Leopard cub from Baranga Zoo identified another cestode, Mesocestoides lineatus (Patnaik & Acharjyo 1970). Spirometra erinaceae was reported at a necropsy from a Jungle Cat in Baranga Zoo (Patnaik & Acharjyo 1970) and unidentified Spirometra species were reported from tigers at Vandalur (Latha et al. 2000) and leopards at Rajkot Zoo (Parsani et al. 2001) and Maharajbagh Zoo (Gawande et al. 2007). Recently, Taenia taeniaeformis and Spirometra mansonoides were recovered during the necropsy of a leopard found in a forest near Shimoga in Karnataka (Ananda et al. 2011) and Hymenolepis and Dyphyllobothrium species were identified from faecal samples at Thrissur Zoo (Varadharajan et al. 2001). Recently, Joyeuxiella pascalei was reported at a necropsy from a Jungle Cat at Puducherry (Das et al. 2011). Cases of hydatidosis were found in lions and jaguars at necropsy at Nagpur zoo (Ganorkar et al. 1997) and Chennai Zoological Park (Sathasivam et al. 2009), respectively.
Protozoan infection in wild felids
The most common protozoan infections reported in wild felids are trypanosomiasis, babesiosis and coccidiosis. Large cats, mainly tigers, are frequently infected with T. evansi (Acharjyo 2000) and the reported signs include anorexia, pyrexia, panting, occasional convulsions and sudden death (Chaudhury et al. 1986; Devasena & Shobhamani 2006). The various protozoan infections reported are listed in Table 6.
Ectoparasitic infection in wild felids
Fleas, ticks and mites are the ectoparasites reported in wild felids in India. Ticks, mainly Haemaphysalis spp., were reported by Geevarghese et al. (1997) and the main tick species reported were H. cuspidata on leopards, H. silvafelis on Jungle Cats and H. kinneari on tigers. Amblyomma hebraeum and another unidentified Amblyomma species were reported on tigers in Assam Zoo in two separate studies by Geevarghese et al. (1997) and Nashiruddullah & Chakraborty (2001). Sarcoptes scabei infection was reported in lions of Bikaner Zoo (Gaurav & Singh 1999) and infestation of Leopard Cats with Ctenocephalides felis felis was reported by Islam (2010).
Treatment of parasitic infections
The therapeutic management of parasitic infections in captive wild felids mainly consists of drug application targeting the specific parasite. Ivermectin was used to treat a mixed infection of Toxocara, Ancylostoma and tapeworm in Sundarban tigers brought to Alipur Zoo (Sur et al. 2001). Ivermectin was also used to treat toxocariasis in lions, which proved resistant to piperazine at MC Zoological Park (Singla et al. 2003).
Singh et al. (2006) used piperazine adipate and pyrantel pamoate to control Toxocara cati, Toxascaris leonina and hookworm infections in tiger cubs, adult tigers, lion cubs and treated panthers and leopards infected with hookworms with ivermectin. Amongst these drugs piperazine adipate was the most effective in controlling ascarids and 30 days after treatment the animals were parasite free. However in lions treated with pyrantel pamoate, T. leonina was recorded again 30 days after the treatment demonstrating its inefficacy to control the parasitic infection. Similarly, Dehuri et al. (2013) found ivermectin ineffective in the control of ascarids and hookworms in lions and reported reoccurrence of the parasites only a few days after treatment.
Triquin (quinapyramine sulphate and quinapyramine chloride) was used successfully to treat trypanosomiasis in wild felids (Gupta et al. 2009; Sahoo et al. 2009). Despite a thorough literature search we found that no successful treatment of babesiosis in wild felids was reported. And though ticks are commonly found on wild felids, their distribution, prevalence or treatment has not yet been studied comprehensively in India.
Conclusions
Parasitic disease studies of wild felids are not only important with respect to the animal’s health but also important for their zoonotic potential. At present there is an information gap. A detailed epidemiological study targeting parasites of the felids should be carried out to obtain a clear picture of parasitism in India. Regular faecal examinations should be supported and supplemented with post mortem findings. Identification of the parasites and diagnosis of parasitic diseases needs to be improved using molecular techniques and the pathophysiology of several helminthic species. Administration of effective drugs with wide safety margins targeting a specific parasitic species and better management practices such as routine cleaning and disinfection, correct disposal of waste and clean food presentation should be adopted wisely, as all play important roles in reducing parasite infections in captive wild animals.
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