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REVIEW ARTICLE Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An Overview

K. Muraleedharan

Professor, University Head and Professor (Retired), University of Agricultural Sciences, Bengaluru-560 065, India, Present Address: No. B 3, Yasoram Tejus Apartments, Vennala High School Road, Vennala, Kochi-682 028, Kerala, India. Abstract Many species of wild carnivores were maintained in zoos and

national parks of Karnataka state. They were found infected with different

*Corresponding Author: gastrointestinal helminths mainly comprised of Toxocara, Toxascaris, Ancylostoma, strongyles, Taenia and Spirometra based on coprological and K. Muraleedharan post-mortem examinations. Rare incidence of Paragonimus, Diphyllobothrium and Physaloptera was also reported. The pathological Email: [email protected] effects associated with helminths were indicated. Depending upon the severity and the type of infections, the infected animals exhibited different grade of clinical signs leading to morbidity and mortality. Regarding protozoan infections, Isospora felis in tiger and and three rare eimerian

species, Eimeria hartmanni, E. novowenyoni and a new species E.

Received: 15/05/2016 anekalensis in panther were identified. Mortality from haemoflagellate, Trypanosoma evansi was occasionally reported in tigers and rarely in other Revised: 18/06/2016 carnivores. PHA and PCR were standardized for the diagnosis of cryptic form of T. evansi in captive wild animals. Three isolates of trypanosomes Accepted: 21/06/2016 from canine, leopard and lion with decending order in their virulence were obtained. Routine medications with anthelmintics, coccidiostats and chemoprophylactics against T. evansi checked most of the parasitic problems. Effective monitoring and surveillance of infection, control of

anthelmintic resistance and implementation of improved sanitary measures

and avoidance of access to intermediate hosts have been stressed.

Keywords: Captive Carnivores, Endoparasites, Incidence, Pathological Findings, Treatment and Control.

1. Introduction and Veterinary Biologicals (IAH and VB), Bengaluru, Karnataka State is endured with considerable Veterinary Section, Mysore Zoo, Mysuru and Wild variety of wildlife which includes mainly carnivores Animal Disease Laboratory at Bannerghatta Biological such as tigers, lions, leopards and jaguars. The well- Park, Bengaluru, besides other veterinary diagnostic maintained Sri Chamarajendra Zoological Gardens laboratories of the state. Moreover, the recent (Mysore Zoo) at Mysuru as well as 21 wildlife establishment of Institute of Wildlife Veterinary sanctuaries and five national parks are exclusively for Research, Doddaluvara, and Kodagu by KUAFSU has protecting these animals. Occasional disease problems a major step forward to take care of management and are of great concern to the health of these animals. health of wild animals. The present review is an Besides bacteria, viruses and rickettsia, many parasites assemblage of available information from publications are common to wild and domestic animals and they are and other relevant sources on the occurrence of inter-transmissible and even communicable to human endoparasites and the diseases caused by them in wild who are in close contact with them. The carnivores of Karnataka state. epidemiological studies on the prevalence and incidence of these parasites are important to know the 2. Source of Information status of various infections and to take up control Systematic surveys and routine examinations measures. Now adequate facilities are available to based on coprology (CE) provided information on the detect parasitism, even up to molecular levels, at four prevalence of helminths and protozoan cysts in veterinary colleges functioning at Bengaluru, Bidar, carnivores under captivity at Mysore Zoo, Mysuru and Hassan and Shivamogga, Institute of Animal Health Bannerghatta National/Biological Park (BPP),

Veterinary Research International | April-June, 2016 | Vol 4 | Issue 2 | Pages 54-62 © 2016 Jakraya Publications (P) Ltd Muraleedharan… Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An overview

Bengaluru and Tiger and Lion Safari (TLS), Tyavarekoppa, Shivamogga. The faecal samples were 3.2.1 Helminths and Coccidia usually examined after centrifugal sedimentation or Comparatively higher percentage of lions had floatation techniques. The number of worms voided in ascarid infection. Muraleedharan et al. (1990) faeces or collected from dead animals at post-mortem documented an unusual incidence of 100.00% of (PM) examinations was counted and the required ascarid infections in lions of Mysore Zoo, of which number was processed for identification. Their 86.67% had Toxascaris infection and the remaining locations in hosts and the lesions produced were noted 13.33% had combination of Toxocara and Toxascaris (vide also Section 4). The nematode parasites were infections. Infection with strongyles alone and predominant followed by cestodes and coccidial strongyle with ascarid was reported from BBP, infections in carnivores. In spite of chronic helminthic Bengaluru (Jayagopla Reddy et al., 1992). Three infections, most of the animals did not exhibit any repeated screening of 360 faecal samples collected alarming clinical signs except occasional diarrhoea. from more than 100 lions over a period of one year The results of coprological examinations done by (2003 to 2004) at BBP, 203 samples (56.39%) were various workers showing the number and percentages found positive for ova of Toxascaris leonina . However, of positive samples for helminthic and protozoan the samples collected randomly from these lions one infections are presented host-wise in Table 1 and 2 month after deworming did not reveal any parasitic respectively. eggs (Chandranaik et al ., 2008). Renukaprasad et al. (2011) had recorded catarrhal type of enteritis due T. 3. Tiger ( Panthera Tigris ) leonina at BBP, Bengaluru in lion cubs and parasitic cysts (cysticercus and hydatid) were recovered from 3.1 Coccidia and Helminths liver, lungs and kidneys of tigers at autopsy. The lions The faecal samples from three tiger cubs of of TLS, Shivamogga harboured higher percentage of Mysore Zoo were found positive for oocysts which Toxocara infection, either alone or mixed with were identified as of Isospora felis after sporulation. strongyles and coccidial infections (Ananda et al ., The oocysts were pale brown, ovoid and measured 36- 2012; Ananda, 2015; Ananda et al ., 2016c). 47 x 25-39 µm. Micropyle, oocyst polar granule and residuum were absent. The sporocysts were ellipsoidal 3.3 Leopard/ Panther (Panthera Pardus ) to almost spherical in shape and were colorless. The sporozoites measured 17-23 x 16-20 µm and they were 3.3.1 Helminths sausage-shaped with one end slightly narrower than the Results of earlier surveys on gastrointestinal other. The sporocysts were without Stieda body and the (GI) parasites of leopards of BBP (1981-82), Bengaluru residuum was large and composed of granules. and Mysore Zoo (1990) revealed that they were free Sporulation time was 48 hr (Muraleedharan and from any infection. Coprological examinations of Vasanthi, 1984). Survey conducted on the prevalence samples collected from leopards once in every three of gastro-intestinal parasites of animals of Mysore Zoo months for a period of one year showed high infections revealed that Toxocara, Toxascaris , Ancylostoma and of Toxascaris leonina and Ancylostoma sp., either coccidia were the common infections of tigers single or some with combinations (Chandranaik et al ., (Muraleedharan et al ., 1990). At BBP, Bengaluru, 2005). The recent reports from TLS, Shivamogga Jayagopla Reddy et al . (1992) recorded strongyles and indicated higher percentage of Toxocara and coccidia while Renukapasad et al . (2011) noticed Spirometra as well as Taenia and Spirometra infections coccidial oocysts in faecal sample examinations. Based in leopards (Ananda, 2015; Ananda et al . 2012; on PM examinations, T. leonina infection causing Ananda et al. , 2016c). catarrhal type of enteritis causing death in tiger cubs and the common presence of cysticercus and hydatid in 3.3.2 Coccidia liver, lungs and kidneys of tigers were reported A panther cub from the hilly area of Anekal, (Renukapasad et al ., 2011). Recently Ananda (2015) Bengaluru (rural) district was brought to the Veterinary and Ananda et al. (2012, 2014a, 2014b, 2015; 2016a; College Hospital, Bengaluru for treatment with the 2016c) observed ova of Ancylostoma sp., Toxocara sp. , history of digestive disturbances, running down Strongyle spp., Taenia sp. and Spirometra sp. as single condition and frequent scratching of the body. The or mixed infections as well as oocysts of coccidia in faecal samples revealed the ova of Ancylostoma sp. and tigers of TLS, Shivamogga. oocysts of coccidia. The three types of oocysts identified on sporulation were Eimeria hartmanni 3.2 Lion (Panthera Leo ) (8%) , E. novowenyoni (12%) , and a new species –

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Table 1: Prevalence of helminth infections in wild carnivores

Location Species Proc. Ex. + % Helminths Reference Mysore Zoo, Tigers CE 19 *8 42.10 Toxascaris with Muraleedharan et al. Mysuru (Panthera tigris ) Isospora (3) (1990) 5 26.32 Ancylostoma BBP, Bengaluru Tigers CE 7 3 42.86 Strongyles Jayagopala Reddy et al . (1992) BBP, Bengaluru Tiger cubs PM - - - Toxascaris leonina Renukaprasad et al . (2011) BBP, Bengaluru Tiger PM - - - Cysticercus Renukaprasad et al. (2011) Hydatid cysts Bandipur area Tiger PM 1 1 - Paragonimus kelli- Renukaprasad et al. (2011) coti TLS, Shivamogga Tigers CE 12 *8 66.67 Toxocara Ananda et al. (2012) Ancylostoma, Taenia and Spirometra TLS, Shivamogga Tigers CE 11 *9 81.82 Toxocara Ananda et al. (2014a) Ancylostoma, Taenia and Spirometra with coccidian TLS, Shivamogga Tigress, 16yr PM 1 1 - Ancylostoma Ananda et al . (2014b) TLS, Shivamogga Tigers CE 15 *12 80.00 Toxocara Ananda (2015) Strongyle and Spirometra with coccidian TLS, Shivamogga Tigers CE 9 *8 88.89 Taenia with Ananda et al . (2016c) Spirometra and Toxocara Kakanakote, Tigress, 8yr PM 1 *1 - Taenia Dharanesh et al. (2016a) Mysuru dt. taeniaeformis and Ancylostoma Kakanakote , Tigress, 8 yr PM 1 1 - Paragonimus west- Dharanesh et al. (2016b) Mysuru dt. er mani i Mysore Zoo, Lions CE 15 *13 86.67 Toxascaris with Muraleedharan et al. (1990) Mysuru (P. leo ) *2 13.33 Toxocara (2) BBP, Bengaluru Lions CE 8 *3 37.50 Strongyle spp. with Jayagopala Reddy et al . *1 12.50 ascarid (1) (1992) BBP, Bengaluru Lions PM - - - Cysticercus Renukaprasad et al. (2011) Hydatid cysts BBP, Bengaluru Lions CE 360 203 56.39 Toxascaris leonina Chandranaik et al . (2008) BBP, Bengaluru Lion cubs PM - - - Toxascaris leonina Renukaprasad et al .(2011) TLS, Shivamogga Lions CE 7 3 42.85 Toxocara Ananda et al . (2012) TLS, Shivamogga Lions CE 12 5 41.67 Toxocara with Ananda (2015) *2 16.67 Strongyle and coccidia (2) TLS, Shivamogga Lions CE 4 3 75.00 Toxocara Ananda et al . (2016 c) Anekal , Panther cub CE 1 1 - Ancylostoma Rajasekariah et al. (1971) Bengaluru dt. (P. pardus ) BBP, Bengaluru Panthers CE 5 1 20.00 Ascarids Jayagopala Reddy et al . 1 20.00 Coccidia (1992) BBP, Bengaluru Leopards CE 46 18 39.13 Toxascaris leonina Chandranaik et al . (2005) (P. pardus ) 26 56.52 Ancylostoma *15 32.61 both species, mixed BBP, Bengaluru Panther cub PM - - - Toxascaris leonina Renukaprasad et al .(2011) BBP, Bengaluru Panther BS 1 1 - Microfilariae Renukaprasad et al. (2011) Shivamogga Leopard, 12 yr, PM 1 *1 - Taenia Ananda et al . (2011) Forest male taeniaeformis and

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Spirometra TLS , Shivamogga Leopards CE 10 4 40.00 Toxocara Ananda et al. (2012) TLS, Shivamogga Leopards CE 21 4 19.05 Spirometra Ananda (2015) 10 47.62 Toxocara TLS, Shivamogga Leopard, 9yr, PM 1 *1 - Taenia Ananda et al . (2016a) female taeniaeformis and Spirometra Chickkamagaluru Leopard, 2yr, PM 1 1 - Physaloptera sp. Ananda et al . (2016b) forest female TLS, Shivamogga Leopards CE 14 *6 42.86 Taenia and Ananda et al . (2016c) Spirometra Mini Zoo, Hassan Jaguar ( P. onca ) PM 1 *1 - Hydatid cysts and Muraleedharan et al . (2010) Ancylostomes Mysore Zoo Jaguar CE - - - Toxocara sp. Anon (2012-13) Mysore Zoo, Jackal CE 3 1 33.33 Ancylostoma Muraleedharan et al. (1990) Mysuru (Canis aureus ) TLS, Shivamogga Jackals CE 2 2 - Toxocara sp. Ananda et al . (2012) TLS, Shivamogga Jackals CE 6 *3 50.00 Strongyle and Ananda (2015) Toxocara TLS, Shivamogga Jackals CE 2 2 - Strongyle (with Ananda et al . (2016c) Eimeria ) Mysore Zoo, Golden cat CE 1 1 - Ancylostoma Muraleedharan et al. (1990) Mysuru (Felis temmincki ) Mysore Zoo, Jungle cats CE - - - Ancylostoma sp. Anon (2012-13) Mysuru (F. chaus ) Mysore Zoo, Striped hyaena CE 3 1 33.33 Trichuris ova Muraleedharan et al. (1990) Mysuru (Hyaena hyaena ) TLS, Shivamogga Hyaena CE 1 1 - Strongyle Ananda et al. (2016c) Mysore Zoo, Sloth bears CE 5 *1 20.00 Ascarid (with Muraleedharan et al. (1990) Mysuru (Melursus coccidia) ursinus ) BBP, Bengaluru Sloth bear CE 1 1 - Taenia sp. Renukaprasad et al. (2011) Mysore Zoo, Carnivores CE - - - Toxocara Anon (2010-11) Mysuru Strongyle spp . Diphyllobothrium Proc. : Procedure ; Ex.: No. examined ; +: No. positive ; %: Percent positive ; # adults in faeces ; *: mixed infection; CE: Coprological Examination ; BS: Blood smear examination; PM: Post-mortem examination

Table 2: Prevalence of protozoan infections in wild carnivores

Location Species Proc. Ex. + % Parasites Reference Mysore Zoo, Tiger cubs PM 3 3 100.0 Trypanosoma evansi Seshadri et al . (1983) Mysuru (Panthera tigris ) Mysore Zoo, Tiger cubs CE 2 1 - Isospora felis Muraleedharan and Vasanthi Mysuru (1984) Mysore Zoo, Tigers CE 19 *3 15.79 Isospora with Muraleedharan et al. (1990) Mysuru Toxascaris Tigers BS 5 5 100.0 T. evansi Renukaprasad et al . (1991) Mysore Zoo Tigress PM 1 1 - T.evansi Ziauddin et al. (1992a) BBP, Bengaluru Tigers CE 7 *1 14.29 Coccidia with Jayagopala Reddy et al . strongyle (1992) BBP, Bengaluru Tigers CE - - - Coccidia Renukaprasad et al. (2011) TLS, Shivamogga Tigers CE 11 *9 81.81 Coccidia with Ananda et al . (2014a) Strongyle , Toxocara and Spirometra TLS, Shivamogga Tigers CE 15 *12 80.00 Coccidia with Ananda (2015) Strongyle , Toxocara and Spirometra

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TLS, Shivamogga Lions CE 12 *2 16.67 Coccidia with Ananda (2015) Strongyle and Toxocara BBP, Bengaluru Panther/Leopard CE 5 1 20.00 Coccidia Jayagopala Reddy et al . (P. pardus ) (1992) BBP, Bengaluru Panther BS - - - T. evansi Renukaprasad et al . (2011) Anekal, Panther cub CE 1 *1 - Eimeria hartmanni , Rajasekariah et al. (1971) Bengaluru (R) dt. E. novowenyoni and E. anekalensis TLS, Shivamogga Jackal CE 2 *2 - Eimeria with Ananda et al . (2016c) strongyles Mysore Zoo Wolf PM 1 1 - T. evansi Ziauddin et al. (1992b) Mysore Zoo Wolf BS 1 1 T. evansi Renukaprasad et al . (2 011) Mysore Zoo Striped hyaena CE 5 1 20.00 Coccidia Muraleedharan et al. (1990) (Hyaena hyaena ) BBP, Bengaluru Hyaena BS - - - T. evansi Renukaprasad et al. (2011) BBP, Bengaluru Sloth bears CE Coccidia Renukaprasad et al. (2011) Proc. : Procedure ; Ex.: No. examined ; +: No. positive ; %: Percent positive ; *: mixed infection; CE: Coprological Examination ; BS: Blood smear examination; PM: Post-mortem examination

E. anekalensis (80%). Their morphological characters 3.7 Golden Cat ( Felis Temmincki ) and Jungle have been presented in Table 3. Catarrhal enteritis in Cat ( Felis Chaus ) panther cubs due to Toxascaris leonina were reported Golden cat and jungle cat of Mysore Zoo were at BBP, Bengaluru and microfilaria infection was found infected with Ancylostoma sp. (Muraleedharan et observed in the blood smears of panther of forest area al. , 1990; Anon, 2012-2013). of Shivamogga (Renukaprasad et al. , 2011). 3.8 Sloth Bear (Melursus Ursinus ) 3.4 Jaguar (Panthera Onca ) Concurrent infection of ascarid and coccidia The hydatid ( Echinococcus ) cysts of different was recorded in a sloth bear of Mysore Zoo sizes were noticed in the liver of a jaguar belonged to (Muraleedharan et al. , 1990). Coccidial oocysts were Mini Zoo, Hassan at PM examination. Ten hookworms observed at BBP, Bengaluru (Renukaprasad et al ., of Ancylostoma sp. were recovered from the duodenum 2011), besides Taenia spp. causing enteritis. which showed congestion (Muraleedharan et al ., 2010). Toxocara infections were also reported in jaguars of 4. More on Symptoms/ Autopsy Findings Mysore Zoo by coproscopy (Anon, 2012-2013).

4.1 Tiger 3.5 Jackal ( Canis Laureus ) One nursing tiger of BBP, Bengaluru had In jackals, four types of parasitic infections persistent diarrhoea with inappetance and showed were reported. One jackal of Mysore Zoo had moderate mixed infection of strongyles and coccidia, but all the infection of Ancylostoma (Muraleedharan et al. , 1990) other carnivores were symptomless carriers and the additional presence of Toxocara and strongyle (Jayagopala Reddy et al ., 1992). Three fatal cases of along with this infection was reported (Anon, 2012- helminthosis among tigers occurred at intervals were 2013). At TLS, Shivamogga, ova of Toxocara sp. were reported. One Bengal tigress aged about 16 years of noticed in jackals (Ananda et al. , 2012), but in later TLS, Shivamogga died after chronic illness. The screening, strongyle infections were found along with autopsy revealed anaemic mucus membrane and Toxocara (Ananda, 2015). Mixed infection of eimerian enlarged liver. Intestinal mucosa showed petechial oocysts and strongyle eggs was also reported recently haemorrhages. Numerous live Ancylostoma sp. were (Ananda et al ., 2016c). recovered especially from duodenal region (Ananda et al ., 2014b). The second tigress of eight year old 3.6 Stripped Hyaena ( Hyaena hyaena ) rescued from Kakanakote beet and section, Rajiv Trichuris ova in faecal samples of hyaena of Gandhi National Park, Mysuru district brought to Mysore Zoo (Muraleedharan et al. , 1990) and Mysore Zoo in poor condition, but died later. The Toxocara and strongyles of TLS, Shivamogga (Ananda autopsy revealed that its intestine was fully packed et al. , 2016c; Ananda et al. , 2012) were reported. with worms which were identified as Taenia taeniaeformis and Ancylostoma sp. The third one was a tigress of the same age and also belonged to the same

Veterinary Research International | April-June, 2016 | Vol 4 | Issue 2 | Pages 54-62 © 2016 Jakraya Publications (P) Ltd 58 Muraleedharan… Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An overview area, died due to lung fluke infection. The PM lesions On the basis of information provided in the showed anaemic mucus membrane and lungs severely 2011-2012 Annual Report of Mysore Zoo, 1032 faecal congested with numerous cystic lesions. Each cyst materials were examined and Toxocara , strongyle sp ., contained coffee-bean shaped worms in pairs. The Diphyllobothrium latum and Isospora felis oocysts pulmonary complications include pneumonia, were detected in carnivores while during 2012-13, bronchitis, bronchiectasis, lung abscess, pleural 1109 samples were subjected for screening of which effusion, and emphysema. The worms were identified 208 (18.76%) were positive for various ova. A study as lung fluke Paragonimus westermanii. The fluke conducted at Wild Animal Disease Diagnostic measures 9.5 x 4.5mm. The oral sucker and acetabulum Laboratory at Bannerghatta from 2005-10 revealed the are placed not far away from each. The intestinal caeca presence of parasitic ova/cysts in faecal samples of extend up to the posterior end. The lobed testes are lions, tigers, jackals and panthers. located at the posterior end. The lobed ovaries are placed posterior to acetabulum. The uterus coil is 6. Trypanosoma Evansi located to the right of the acetabulum. The vitelline T. evansi was rarely encountered infection, but glands are occupying almost the lateral field. The ova mortality from trypanosomosis was fairly high. A collected from sputum and faecal samples are 94 x 60 review by Muraleedharan (2015) had dealt the present µm in size, yellowish, oval-shaped with thick shell and status of T. evansi infection in domestic and captive often asymmetrical with one end flattened and other carnivores of Karnataka. An outbreak of end with operculum (Dharanesh et al. , 2016a, b). trypanosomosis in carnivores especially in tigers and Another species of lung fluke, P. kellikoti was also mortality were reported. Difficulty felt for early recovered earlier from the lungs of tigers in Bandipur diagnosis of T. evansi infection by direct blood forest area of Mysure district (Renukaprasad et al . examinations might be the main reason for sudden (2011). fatality. Renukaprasad et al . (1991) had experienced that initial examinations of blood of ailing animals did 4.2 Lion not reveal any infection, but T. evansi infection was The symptoms of occasional diarrhoea, confirmed by 12 th day following repeated unthriftiness and pot-bellied appearance were noticed examinations. Clinical trypanosomosis was noticed in only in a few young animals infected with Toxascaris tigers, lions, panther, hyaena and wolves of BBP, leonina and adult lions with heavy infections had loose Mysore Zoo, and TLS, Shivamogga. The stools. Further two lions, died by cause other than haematological values in affected tigers revealed severe parasitism, revealed large number of adult T. leonina in anaemic changes characterized by low RBC count, entire GI tract (Chandranaik et al ., 2008). reduced haemoglobin and PCV values with anisocytosis (Renukaprasad et al ., 2011). Sero- 4.3 Leopard diagnostic test, PCR was standardized for diagnosis of Leopards infected with heavy load of Toxocara T. evansi infection in captive wild animals by Shailaja and Ancylostoma , either alone or combined, had et al. (2005). Sen Gupta et al. (2010) had detected occasional diarrhoea and unthriftiness. Pot-bellied canine, lion and leopard isolates. Lakkundi (2010) appearance was noticed in young animals having studied the genetic profile of these isolates. The canine mixed infections. But adult leopards, though heavily isolates were most virulent, followed by leopard and infested with these parasites, showed no noticeable the lion isolates were least virulent. The PHA test was clinical symptoms except occasional loose stool carried out to detect carrier status of T. evansi and the (Chandranaik et al ., 2005). Numerous tapeworms, efficacy of the test on the serum samples of tigers, Taenia taeniaeformis and Spirometra mansonides were lions, leopards and jaguars whose blood smears proven recovered at autopsy from the intestinal tract of a negative for T. evansi infection has been presented in twelve and nine year old dead leopards of the forest Table 4. The lower carrier condition in carnivores of area of Shivamogga (Ananda et al ., 2011; Ananda et the Zoo reflects the effective prophylactic regime al ., 2016a). Similarly, from a two year old female followed in them rather than the free range animals leopard died due to injury in the forest of having frequent exposure to vectors (Lakundi, 2010). Chikkamagaluru district, a few nematodes of the genus Physaloptera were recovered from the pyloric end of 7. Control Programmes and Treatment stomach (Ananda et al ., 2016b). For control of nematode infections, removal of top soil and turning over the soil, grazing animals in 5. General Findings rotation, application of lime wash and other hygienic measures are practiced in Mysore Zoo. Quarterly -

Veterinary Research International | April-June, 2016 | Vol 4 | Issue 2 | Pages 54-62 © 2016 Jakraya Publications (P) Ltd 59 Muraleedharan… Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An overview

Table 3: Morphology of eimerian of oocysts recorded from panther

Characters Eimeria hartmanni Eimeria novowenyoni Eimeria anekalensis Rastegaieff, 1930 Rastegaieff, 1929 Rajasekariah et al .,1971 Oocyst shape Elongated, oval to ellipsoidal Almost circular Ovoid with one end with flattened end slightly tapered Oocyst size 20-22.5 x14-19 µ 18-20 µ in diameter 22-30 x 18-22 µ Oocyst wall Enveloped by two Enveloped by two Smooth and colourless membranes, internal clearer membranes; internal than external thicker (1.5 µ) than external (0.5 µ) Micropyle Inconspicuous Absent Present Sporocyst number Four, spindle-shaped, Four, ellipsoidal Four, spindle-shaped, and shape irregularly arranged inside irregularly arranged the oocysts inside the oocysts Sporocyst size 9.5-10 x 6-8 µ 10 x 6 µ 10-15 x 5-8 µ Stieda body Present Absent Present, clearly defined Sporozoites number, Two spindle-shaped, clear Two spindle-shaped, Two spindle-shaped shape and size granular at the rounded 7-12 x 3-6 µ end and clear at the pointed end , 8 x 4 µ Polar granule Absent Absent Present Oocyst residuum Absent Absent Absent Sporocyst residuum Absent Absent Absent Sporulation time 40 -42 hr 40-42 hr 40 -42 hr

Table 4: PHA test results of captive carnivores negative for T. evansi by routine test

Location Species of a nimals and number tested Tigers Leopards Lions Jaguars Tested +ve Teste +ve Teste +ve Teste +ve d d d Mysore Zoo 4 1 6 1 - - 2 2 TLS, 11 7 6 5 2 2 - - Shivamogga BBP, Bengaluru 14 9 3 3 43 30 - - Total 29 17 15 9 45 32 2 2 Per cent positive 58.62 60.0 71.11 100 deworming has been done regularly to all the animals Overcrowding of animals in enclosures, being and the faecal samples are examined before and after precipitating factors for re-infections of parasites, deworming for confirming the efficacy of treatment. In should be avoided. Most of the parasitic infections positive cases, medications have been repeated after 20 recorded from carnivorous animals are of zoonotic days. Quarterly chemoprophylaxis against importance and those handling them should be aware to Trypanosoma evansi infection is regularly practiced follow all hygienic cares to prevent infection to them. (Anon, 2010-2011; 2011-12; 2012-13). But studies on Since Spirometra infection is repeatedly reported in the schedule of medications and the dosage rates tigers of Shivamogga region, the possibility for human followed to wild animals of Karnataka are lacking. The sparganosis in the area cannot be ruled out. Cross information of anthelmintic treatments have been done transmission of common infections of wild and elsewhere have been compiled for the benefits of zoo domestic animals are best controlled by avoiding the veterinarins (Narayana Bhat, 2008). However, studies same grazing areas. have to be undertaken on this aspect to know the Suitable methods have to be explored to study comparative efficiency of newer drugs. the exact nature of parasitic problems encountered by wildlife deep inside the forest which might be different 8. Conclusion from those under captivity. Pursuing the doctorate programme at Indian Institute of Science, Bengaluru

Veterinary Research International | April-June, 2016 | Vol 4 | Issue 2 | Pages 54-62 © 2016 Jakraya Publications (P) Ltd 60 Muraleedharan… Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An overview

Watve (1992) presented many interesting aspects of Park, Karnataka) . In short, understanding of all the host parasite interactions of wild mammalian host factors involved in the disease transmission and community based on wild animals of Mudumalai, implementation of appropriate control measures should Tamilnadu (a continuation of the Bandipur National be a part of protection and conservation of wildlife.

References Ananda KJ (2015). Studies on prevalence of endo-parasitic Anon (2012-2013). Annual report of Sri Chamarajendra infection in wild carnivores maintained under captive Zoological Gardens, Mysure. Veterinary Section , pp: state. Journal of Parasitic Diseases . pp: 1-4. DOI: 28-46. 10.1007/s12639-014-0640-2. Chandranaik BM, Srinivasa Murthy, Dilip Das, Mamatha GS, Ananda KJ, Krishnamurthy CM, Adeppa J and Renukaprasad C and Krishnappa G (2005). Chandrashekar S (2014a). Prevalence of Helminthiasis in leopards ( Panthera pardus ) at gastrointestinal parasites in big cats maintained in Bannerghatta Biological Park. Zoos ’Print Journal , 20: captivity. 24 th National Congress of Veterinary 1934. Parasitology, 5-7 February, 2014, CVAS, Mannuthy, Chandranaik BM, Dilip Das, Mamatha GS, Harish BR, Thrissur, Kerala, S.3.33, p: 116 . Shivaraj C, Renukaprasad C and Krishnappa G (2008). Ananda KJ, Manjunath SS, Vinay S and Prasad RV (2016a). A study on prevalence of ascarids in lions ( Panthera Concurrent infection of Taenia taeniaeformis and leo ). Journal of Veterinary Parasitology, 22: 85-86. Spirometra mansonoides infection in a free range Dharanesh NK, Ananda KJ, Ramesh KR, Kshama LM, leopard ( Panthera pardus ). 25 th National Congress of Umashankar KS, Giridhar P and Byre Gowda SM Veterinary Parasitology , 17-19 February, 2016, (2016a). Gastrointestinal parasitic infections in a royal TNVASU, Chennai , p: 213. Bengal tiger ( Panthera tigris tigris ). 25 th National Ananda KJ, Pradeep BS, Satheesha SP and Dhanalakshmi S Congress of Veterinary Parasitology, 17-19 th February, (2016b). Occurrence of Physaloptera sp. and 2016, TNVASU, Chennai, p: 68. Rhipicephalus sanguineus in a free range leopard. 25 th Dharanesh NK, Ananda KJ, Ramesh KR, Kshama LM, National Congress of Veterinary Parasitology, 17-19 Umashankar KS, Giridhar P and Byre Gowda SM February, 2016, TNVASU, Chennai, p: 215. (2016b). Paragonimus westermanii infection in a wild Ananda KJ, Vinay S, Malatesh DS and Dhanalakshmi S royal Bengal tiger ( Panthera Tigris ). 25 th National (2016c). Incidence of endo-parasitic infection in wild Congress of Veterinary Parasitology , 17-19 February, animals maintained at Shivamogga, Karnataka. 25 th 2016, TNVASU, Chennai, p: 240. National Congress of Veterinary Parasitology , 17-19 Jayagopala Reddy NR, Jagannath MS, D’Souza PE, Abdul February, 2016, TNVASU, Chennai. pp: 212-213. Rahman S and Basavarajappa K (1992). Prevalence of Ananda KJ, Chandrashekar S, Naravi Y, Ramesha K and gastrointestinal parasites in wild animal and captive Devaraj M (2012). Prevalence of gastrointestinal birds at Bannerghatta National Park, Bangalore. Indian parasites of wild animals maintained under captive Journal of Animal Sciences , 62: 1046-1048. state. 22 nd National Congress of Veterinary Lakkundi JN (2010). Molecular and serological studies on Parasitology, College of Veterinary Science and trypanosomosis with special reference to captive wild Animal Husbandry, Mathura, DUVASU, 15-17 March, animals. Ph.D Thesis, KVAFSU, Bidar, Karnataka. 2012, 2(21): 28. Muraleedharan K (2015). An update on Trypanosoma Ananda KJ, Anjan Kumar KR, Krishnmurthy CM, Adeppa J, infection in livestock of Karnataka state, India. Manjunath SS and Chandrashekar S (2014b). Hook Veterinary Research International , 3: 46-54. worm infection ( Ancylostoma spp. ) in a Bengal tiger Muraleedharan K and Vasanthi I (1984). Coccidial infection (Panthera tigris tigris ) - a case report, 24 th National in tiger ( Panthera tigris ) cubs. Indian Journal of Congress of Veterinary Parasitology, 5-7 February, Parasitology , 8: 285-286. 2014 at CVAS, Mannuthy, Thrissur, Kerala, S.3.34, p: Muraleedharan K, Vasanthi I, Ziauddin, KS and Srinivasan K 116. (1990). A survey of gastro-intestinal parasites of Ananda KJ, Kavitha Rani B, Ramesha K, Swethashree MJ, animals of Zoological Gardens at Mysore. Mysore Ranjitha VH, Nagaraj KH and Prasad RV (2011). Journal of agricultural Sciences , 24: 250-256. Tapeworm infection in a leopard: A case report. 21st Muraleedharan K, Seshadri SJ, Srinivasa Gowda RN and National Congress of Veterinary Parasitology, Bombay Appaji, 2010. Cancer of eye in a jaguar ( Panthera Veterinary College, Mumbai, 5-7th January, S3-P11, p: onca ). Zoos’ Print Journal , 25(12): 33. 125. Narayana Bhat M (2008). Parasitic diseases of wild animals Anon (2010-2011). Annual report of Sri Chamarajendra and their control. In : XI National Training Programme , Zoological Gardens, Mysure. Veterinary Section , pp: Centre of Advanced Studies in Veterinary Parasitology, 34-64. Veterinary College (KVAFSU), Hebbal, Bangalore-560 Anon (2011-2012). Annual report of Sri Chamarajendra 024, November10-30, 2008, pp: 130-137. Zoological Gardens, Mysure. Veterinary Section , pp: Rajasekariah GR, Hegde KS, Srinivasa Gowda RN, Abdul 43-66. Rahman S and Subba Rao HA (1971). A study of some parasites from panther cub ( Felis pardus , Linn,) with

Veterinary Research International | April-June, 2016 | Vol 4 | Issue 2 | Pages 54-62 © 2016 Jakraya Publications (P) Ltd 61 Muraleedharan… Endoparasites of Wildlife (Carnivores) of Karnataka State, India - An overview

description of Eimeria anekalensis , N. Sp. Mysore trypanosomiasis in tiger cubs from Mysore Zoo. Journal of Agricultural Sciences , 5: 404-409. Annual Conference and National Symposium, Indian Renukaprasad C, Babu MM, Ramaiah HM and Gopal T Association of Veterinary Parasitology , Bangalore, (1991). Incidence of trypanosomiasis in captive wild Abstract, WL-9. felidae at Bannerghatta National Park, India. In : Shailaja V, Venkatesha MD, Renukaprasad C, Jaykumar SR Proceedings International Seminar on Veterinary and Krishnappa G (2005). Standardization of Medicine in wild and captive animals, Bangalore, Nov. polymerase chain reaction (PCR) for diagnosis of 8-10, Abstract 9.7, p: 29. trypanosomiasis in captive wild animals. Intas Polivet , Renukaprasad C, Shilpa and Sudharani (2011). Parasitic 6: 207-208. infections in wild animals. In XIV National Training Ziauddin KS, Muraleedharan K and Seshadri SJ (1992a). Programme, Centre of Advanced Faculty Training in Some pathological observations on trypanosomiasis in Veterinary Parasitology, Veterinary College a tigress at Mysore Zoo. Indian Journal of Wild Life (KVAFSU), Hebbal, and Bangalore-560 024. Health Management , 1: 38-39. Compendium , pp: 30-33. Ziauddin KS, Muraleedharan K and Seshadri SJ (1992b). Sengupta PP, Balumahendiran M, Suryanaryana VVS, Trypanosomiasis in a wolf at Mysore Zoo - A case Raghavendra AG, Shome BR, Gajendragad MR and report. Indian Journal of Wild Life Health Prabhudas K (2010). PCR-based diagnosis of surra Management , 1: 47. targeting VSG gene: experimental studies in small Watve MG (1992). Ecology of host-parasite interactions in a laboratory rodents and buffalo. Veterinary wild mammalian host community in Mudumalai, Parasitology , 171: 22-31. southern India. Ph.D Thesis submitted to Indian Seshadri SJ, Muraleedharan K, Ziauddin S, Ananth and Institute of Science , Bangalore. Keshava Murthy BS (1983). A note on the pathology of

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