BIOLOGIA (PAKISTAN) 2014, 60 (2), 211-218 PKISSN 0006 – 3096 (Print) ISSN 2313 – 206X (On-Line) Prevalence of Endoparasites in African Lion – Panthera leo *ABDUL QAYYUM KHAN SULEHRIA1, GULNAZ MOQEEM1, YASSER SALEEM MUSTAFA2, 3 ZAHID SHARIF MIRZA & SUMERA MUSHTAQ 1 1 Department of Zoology, GC University, Lahore, Pakistan Provincial Diagnostic Laboratory, Cooper Road, Lahore, Pakistan 3 Fisheries Research & Training Institute, Manawan, Batapur, Lahore, Pakistan 2 ABSTRACT The incidence of endoparasites in African lion, Panthera leo, present in Lahore Zoo and Lahore Safari Park has been investigated. The study was conducted from January, 2012 to July, 2012 during which 147 fecal samples were collected from 21 African lions, including male, female and cubs, divided into three groups on the basis of age. The prevalence of cestodes was 33.3% in females while prevalence of nematodes was 33.3% and 66.7% in males and females, respectively. Trematodes were not found in any lion. It was recorded that prevalence of endoparasites was greater in female lions (38.9%) as compared to male lions (28.5%). Key words: Lion, Endoparasite, Cestode, Nematode, Trematode INTRODUCTION Zoological gardens exhibit wild animals for aesthetic, educational, recreational and conservation purposes (Varadharajan & Pythal, 1999). The African lion (Panthera leo) is a big cat that belongs to genus Panthera (Nowak, 1999). Wild lions are found in Sub-Saharan Africa and in Asia while endangered species of lions are present in Gir Forest National park in India. Captive animals are more likely to contract diseases because animals live in close proximity to each other. When animals are housed together from different geographical areas or there are plans to reintroduce animals into wild environment, they have more opportunities to transfer parasites (Viggers et al., 1993). Wild animals carry a variety of parasites in their free living stage but they do not cause disease unless under stress (Gaur et al., 1979). Parasites with direct lifecycle and host range are the greatest threat for the animals (Fowler & Miller, 1999). Diseases that are caused by parasites comprise one of the major problems resulting in even morbidity and mortality in these animals while in captivity (Rao & Acharjyo, 1984) the effects range from sub-clinical to death. Collectively, helminths are the most prevalent and taxonomically diverse group of parasites in both wild and captive animals *Corresponding author: [email protected] (Pedersen et al., 2005). The major groups of these metazoan parasites include the Platyhelminthes, Nematoda and Acanthocephala. Life cycles of helminth parasites are extremely complicated with different hosts for different developmental stages or simple with only a single host (Schneider & Tenter, 2006). Zoo animals under captivity are prone to almost all types of diseases. So these parasitic diseases, especially helminthic infection, are major problem of zoo animals (Varadharajan & Kandasamy, 2000). Zoo animals harbour a large number of parasites. These parasites affect animal health and cause mortality, morbidity or both (Deshmukh et al., 2009). Under captivity the health status of zoo animals varies with different factors e.g., management, feeding, environment, sanitation and close association of animals and seasonal variation affect the health of animals (Kashid et al., 2003). This project was designed to study the incidence of endoparasites in the African lion in the Lahore Zoo, Lahore and Lahore Safari Park. MATERIALS AND METHODS Experimental Animals and Study Area The present study was conducted on the African lion (Panthera leo) during January, 2012 to July, 2012. The samples were collected from 21 lions including male, female and cubs kept under captivity at Lahore Zoo located at 90-Shahra-e- 212 A. Q. K. SULEHRIA ET AL Quaid-e-Azam and Lahore Safari Park at Raiwind Road, Lahore. In the Lahore Zoo, lions in captivity were kept in indoor enclosures with wired fence. While in Lahore Safari Park, lions were provided with semi-natural environment such as man-made hills, hideouts and dens. They were kept in outdoor vicinity with dense vegetation consisting of trees, bushes and grass. BIOLOGIA (PAKISTAN) The age of the African lion was determined by studying eruption sequence of deciduous and permanent teeth of both jaws and the wear of permanent teeth (Smuts et al., 1978). Lions were divided into 3 groups depending upon their age e.g., Group A (≤1 Year), Group B (1-9 years) and Group C (10-20 years) (Table I). Table I: Age-wise population of Lion (Panthera leo) at Lahore Zoo and Lahore Safari Park Sr. Number of lions Age groups of lions No. 1. n 1=7 Group A Group B Group C ≤ 1 Year 1 - 9 Years 10-20 Years (23.8%) (47.6%) (28.5%) M F M F M F - - 3 0 1 3 (14.2%) (42.9%) (42.9%) 2. 3. n 2 =14 N =21 3 2 4 3 1 1 (21.4%) (14.2%) (28.5%) (21.5%) (7.14%) (7.14%) 3 2 7 3 2 4 (14.3%) (9.5%) (33.4%) (14.2%) (9.5%) (19.1) n 1 = Total number of lions present in Lahore Zoo, Lahore. n 2 = Total number of lions present in Lahore Safari Park, Lahore N = Total number of lions present in Lahore Zoo and Lahore Safari Park, Lahore. M = Male; F = Female The total number of lions present in Lahore Zoo and Lahore Safari Park were 21 out of which 7 (33.3%) lions were present in Lahore Zoo and 14 (66.7%) lions were present in Lahore Safari Park. There were 4 (57.1%) male lions and 3 (42.9%) female lions in Lahore Zoo but no cub was observed. In Lahore Safari Park 5(35.8%) male lions, 4(28.9%) female lions, 3(21.4%) male cubs and 2(14.2%) female cubs were present. Sample Collection In total, 147 faecal samples were collected. The scats were collected by using standardized collection protocol. Each sample was sealed in plastic zip lock bags. The bags were labelled with name of lion, sex, age, date, time of collection and locality. The samples were carried in ice box. Sample Processing in Laboratory The samples were taken to the Provincial Diagnostic Laboratory, Livestock and Dairy Development, 16-Cooper Road, Lahore. The processing of samples and detection of parasites were done there. In order to preserve, faecal samples were transferred to sterile vials containing 30ml of 10% formalin. The detection and quantification of parasites were done by using Sedimentation-Floatation Concentration (Zinc Sulphate) method described by Ezenwa, 2003 and Sedimentation Technique by Monson-Bhar & Bell (1982). PREVALENCE OF ENDOPARASITES IN AFRICAN LION – PANTHERA LEO VOL. 60 (2) 213 RESULTS Identification of Parasites Parasites were identified by studying the morphology and size of the eggs (Fig., 1) as described by Soulsby (1982) and Sloss et al. (1994). Fig., 1: Ova of Taenia sp., and Toxocara sp. Statistical Analysis The data collected was analyzed applying Percentage (Steel & Torrie, 1997). by The present study revealed that cestodes and nematodes were the most prevalent helminths found in lions. In Lahore Zoo, no lion was found positive for cestode, in Group A and B, however, 1 (33.3%) female lion was found positive for cestode infection in Group C. It was recorded that in Group B, the prevalence of nematodes among male lions of Lahore Zoo was 33.3% as 1 out of 3 lions was infected with nematode. While no female lion, present in this group, was found positive for nematode. In Group C, out of three 2(66.7%) female lions were found positive for nematode infection. No male lion was found having nematode infection in this group. No lion, in any group, was found positive for trematodes in Lahore Zoo. In Lahore Zoo, only 1(33.3%) female lion in Group C was carrying mixed infection while lions present in all other groups were found negative for mixed infection (cestode+nematode) (Table II). Table II: Prevalence of endoparasites in Lions of Lahore Zoo Sr. No. 1. Age Groups and Number of lions Group A (≤1 year) Prevalence of Cestodes (Taenia sp.) Prevalence of Nematodes (Toxocara sp.) M F M - - - 1 1 (33.3%) (33.3%) F - Prevalence of Trematodes Prevalence of Mixed infection (Cestode+Nematode) M F M F - - - - - - - - - - - M=0; F=0 2. Group B (1-9 years) - - M=3; F=0 3. Group C (10-20 years) - - - 2 (66.7%) 1 (33.3%) M=1; F=3 M = Male; F = Female In Lahore Safari Park, no lion was found infected with cestode in Group A. In Group B only 1(25%) male lion was found positive while all females were negative for cestodes. In Group C 214 A. Q. K. SULEHRIA ET AL 1(100%) female lion was found positive for cestode infection. Prevalence of nematodes among the lions of Lahore Safari Park was high. In Group A only 1(50%) female lion was found positive for nematode. In Group B, 1(25%) male lion was found positive for nematodes while no female was found having nematodes. In Group C, 1(100%) male and 1(100%) female were found positive for nematodes. BIOLOGIA (PAKISTAN) All lions present in Lahore Safari Park were found negative for trematodes. In Lahore Safari Park, all lions present in Group A were found negative for mixed infection (cestode+nematode). In Group B, 1(25%) male lions were found positive for mixed infection while in Group C only 1(100%) female lion was found having mixed infection (cestode+nematode) (Table III). Table III: Prevalence of endoparasites in Lions of Lahore Safari Park Sr. No. 1. Age Groups and Number of lions Group A (≤1 year) Prevalence of Cestodes (Taenia sp.) M F - - Prevalence of Nematodes (Toxocara sp.) M 1 - M=3; F=2 2. Group B (1-9 years) 1 (25%) F (50%) 1 - - (25%) Prevalence of Trematodes Prevalence of Mixed infection (Cestode+Nematode) M F M F - - - - - - - - 1 - (25%) M=4; F=3 3. Group C (10-20 years) - 1 1 1 (100%) (100%) (100%) - 1 (100%) M=1; F=1 M = Male; F = Female Table IV: Prevalence of endoparasites in Lions in Lahore Zoo and Lahore Safari Park Sr No. Locality Total No. of Lions Prevalence of Cestodes (Taenia sp.) Prevalence of Nematodes (Toxocara sp.) Prevalence of Trematodes Prevalence of Mixed infection Total prevalence of endoparasites 1. Lahore Zoo 7 1 (14.28%) 3 (42.8%) - 1 (14.28%) 5 (71.4%) 2. Lahore Safari Park 14 2 (14.28%) 4 (28.5%) - 2 (14.2%) 8 (57.1%) 3. Total 21 3 (14.28%) 7 (33.3%) - 3 (14.28%) 13 (61.9%) Among cestodes only Taenia sp., was observed. Similarly, among nematode only Toxocara sp., was found. It was recorded that prevalence of cestodes (Taenia sp.) was 1(14.28%), prevalence of nematodes (Toxocara sp.) was PREVALENCE OF ENDOPARASITES IN AFRICAN LION – PANTHERA LEO VOL. 60 (2) 3(42.8%) and prevalence of mixed infection was 1(14.28%) among the lions of Lahore Zoo. In Lahore Safari Park prevalence of cestodes (Taenia sp.) was recorded as 2(14.2%), prevalence of nematodes (Toxocara sp.) was 4(21.5%) and prevalence of mixed infection was 2(14.28%). 215 Overall prevelance was: cestodes (Taenia sp.) 14.28%, nematodes (Toxocara sp.) 33.3% and mixed infection 14.28% prevalent (Table IV). It was recorded that prevalence of endoparasites was greater in female lions (38.9%) as compared to male lions (28.5%) (Table V). Table V: Comparison of prevalence of endoparasites in male and female lions in Lahore Zoo and Lahore Safari Park Sr. No. Locality Total No. of Lions Prevalence of endoparasites in male lions Prevalence of endoparasites in female lions Total prevalence of endoparasites 1. Lahore Zoo 7 1 4 5 (14.28%) (57.1%) (71.4%) 4 4 8 (28.5%) (28.5%) (57.1%) 5 8 13 (23.8%) (38.09%) (61.9%) 2. 3. Lahore Safari Park 14 Total 21 DISCUSSION In Pakistan more than 100 African lions are present in the captivity. They are in Zoological gardens, in the wildlife sanctuaries and in the personal zoos but no wild lion have been reported in Pakistan. A group exercise led by WCS and the IUCN SSC Cat Specialist Group estimated that 42% of major Lion populations were declining (Bauer, 2008). The rate of decline is most unlikely to have been as high as 90%, as reported in a series of news reports in 2003 (Kirby 2003, Frank & Parker 2003). The present study was conducted to assess the prevalence of helminths (endoparasites) among lions. In general, endoparasites (i.e., parasitic species usually reproduce by transmitting free living infective stages that pass from one host to another host) aggregate across their host population. Most individuals harbour low number of parasites but a few individuals become victim to high parasitic infection (Shaw & Dobson, 1995). Such heterogeneity is developed due to the variation between the individuals in their exposure to infective stages and difference in their susceptibility (Wilson et al., 2002). Prevalence of endoparasites in female lions (38.9%) was found to be greater as compared to male lions (23.8%) which contradicted the findings of Ravindran et al. (2006) who stated that male and female lions equally suffered from the endoparasite infection but agreed with the study of Smith & KOK (2006) who reported highest number of parasites in female lions. Lions present in Lahore Zoo showed high prevalence of endoparasites as compared to Lahore Safari Park because in Lahore Safari Park, lions were kept in an environment closer to their natural habitat and thus may have developed resistance against endoparasites. The similar result was published by Atanaskova et al. (2011) which showed that prevalence of endoparasites in Skopje Zoological Gardens was fairly high during 20072009 that was 21.4%, 32.1% and 28.6% in the years 2007, 2008, 2009 respectively. In captivity, lions are less resistant to endoparasites than in their natural habitats because they are provided with less varied food (Goossens et al., 2005). Furthermore, lions were caged in close proximity to each other which increased the prevalence of endoparasites in Lahore Zoo. 216 A. Q. K. SULEHRIA ET AL All of the helminth parasites are found to be transmitted through environment, transplacemental transmission or through the feed given to the animals. In Lahore Zoo and Lahore Safari Park, lions are fed beef which can be intermediate host for many helminthic infections. The similar findings were made by Smith & KOK (2006) who described that helminths have the herbivore as intermediate host that may play important role in the transmission of parasites to lion. Likewise, Chakraborty & Goswami (2001) also concluded that high incidence of helminths in wild animals was due to the close association of these animals in captivity. Cubs present in Lahore Safari Park had less parasitic infection. Only 20% cubs were found positive for nematodes which might be due to the fact that more care and attention are given to cubs for better livability and growth which indirectly helps to prevent the invasion of infected stages of parasites. Modi et al. (1997) and Varadharajan & Subramanian (2003) reported similar findings. The old aged lions, both in the Lahore Zoo and Lahore Safari Park, had more parasitic burden. Smith & KOK (2006) opined that older male lions were infested with endoparasites because of their feeding habit. In the present study, it was found that both; in Lahore Zoo and Lahore Safari Park, only very few young lions (1-9 years) were carrying endoparasites. Smith & KOK (2006) reported similar findings in their study that the younger male lions had least number of eggs and parasitic infection. The resistance in young lions against endoparasites could be as a result of their heavy feeding, as observed by Smith & KOK (2006) that a younger male lion consumed the largest amount of feed that was 50 Kg. He kept eating for 4 hrs and 22 min, so he had physiological resources to resist against endoparasites. In captive lions prevalence of nematodes was (33.3%) that was quite high as compared to cestode infection. Among nematodes only Toxocara sp., was found in the faecal samples of lions at Lahore Zoo & Lahore Safari Park. Deshmukh et al., (2009) reported that prevalence of Toxocara sp., was 13.3% in wild animals in captivity. Varadharajan & Kandasamy (2000) reported that out of 3 lions 2 were found having Toxocara sp. The result is in BIOLOGIA (PAKISTAN) accordance with Ravindran et al., (2006) who mentioned that out of 17 lions 12 were carrying Toxocara sp., as an endoparasite. Hase et al., (2007) reported toxocara infection in an 18 years old lion belonging to Siddharth Municipal Council Zoological Garden which was suffering from dullness, depressed appetite, epiphora and loose faeces. In Safari Park a cub was found having loose faeces in which Toxocara sp., was observed and this cub died later on. Vincent & Francis (2007) reported a very high number of lions suffering from Toxocara canis and Toxocara cati. They described that 66.6% lions were infected from Toxocara sp. at animal orphanage in Kenya, Boomker et al., (1997) reported Toxocara cati and T. canis as most prevalent endoparasites of lions. Bjork et al. (2000) reported absence of Toxocara sp., from free ranging wild lions. Muller-Graf (1995) reported that the prevalence of Toxocara sp. in wild animals was very low (4.5%). He found that only 5 individuals out of 112 were carrying Toxocara sp. It was calculated that the total prevalence of cestode parasite in Lahore Zoo and Lahore Safari Park was 14.28% e.g., 3 out of 21 lions were positive for cestodes. Among cestodes only Taenia sp. was found. Cestodes are more prevalent endoparasites of wild animals but some reports have been found from captivity. Ogungbade & Ogunrinade (1984) reported taeniid (Taenia hydatigena) in Panthera leo in captivity. A large variety of Taenia sp., is highly prevalent among carnivores. All the Taenia sp., use ruminants as an intermediate host. When these ruminants are eaten by lions, this parasite is transmitted to lion (Boomker et al., 1997). Kashid et al. (2003) reported Taenia taeniaeformis in wild captive animals. Bjork et al. (2000) reported eggs of Taenia sp. from free ranging wild lions of Northern Tanzania and observed that Taenia infection was most prevalent among lions. 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