INTERNATIONAL JOURNAL OF SCIENTIFIC & TECHNOLOGY RESEARCH VOLUME 9, ISSUE 04, APRIL 2020 ISSN 2277-8616 Gastrointestinal Parasites In Fecal Samples Of Sumatran Laughingthrush ( bicolor) From Markets, Medan City, North Sumatra

Markus Mangantar Pardamean Sianturi, Adrian Hartanto, Adetia Arjuna Girsang

Abstract: Sumatran laughingthrush (Garrulax bicolor) is an endemic avifanual from North Sumatra. The species is heavily exploited and traded in bird markets in Medan city following the threats to its health due to prolonged captivity and poor bird housing by the vendors and distributors. This preliminary investigation aims to identify the gastrointestinal (GI) parasites infecting the G. bicolor through coproscopical analysis and microscopical observation. Total of 120 fecal samples were collected and examined in a weekly-basis for two months from July to August 2019. The results revealed the presence of seven GI parasites namely one coccidia (Eimeria), two cestodes (Choanotaenia, Raillietina), and four nematodes (Ascarida, Amidostomum, Capillaria, Heterakis) in 68 positive samples (56.6 %). Raillietina spp. are designated as the most prevalent GI parasites to G. bicolor, followed by Amidostomum (47.5 %), Eimeria (36.6 %), Choanotaenia (12.5 %), Capillaria (0.07 %), Heterakis (0.06 %), and Ascarida (0.03%). Severe infections are also obtained from Raillietina (75.0±22.6) with the relative density of 3.3/ind, followed with the remaining moderate infections by Ascarida (20.0±13.4), Eimeria (18.1±10.3), Choanotaenia (11.7±5.1), Heterakis (9.7±5.35), and Capillaria (6.1±3.6)..Our results may then reflect the importance of sanitary management by the keepers to decrease the health risk posed by these parasites as well as to prevent a possible zoonotic infection from captive .

Index Terms: Bird market, Fecal, Garrulax bicolor, Gastrointestinal parasite, Medan city, Railleitina, Sumatran laughingthrush ——————————  ——————————

1. INTRODUCTION The risk become greater with the possibility of finding North Sumatra has long been a part as an important zoonotic parasites which concern to the personal health of province in Indonesia which facilitate intense wildlife trade, the bird keeper or even to the community health [8]. The especially in avifauna through bird market activities. present study was undertaken to investigate the presence or Garrulax spp. are exotic avifaunal of gastrointestinal parasites through fecal or coprological species commonly kept and exploited from the wild, leading survey from G. bicolor sampled from representative bird to over-catchment and trade in North Sumatra [1]. Both the markets in Medan city, North Sumatra. In addition, native and non-native Garrulax species are commercially categorizations are given to reflect the importance of our available in bird markets with fluctuative inputs based on finding to the highlighted parasite. demands and natural supply for certain species [2], [3]. Sumatran Laughingthrush (Garrulax bicolor) is a native and endangered species from North Sumatra which is 2. MATERIALS AND METHOD commonly traded in wildlife and bird markets to bird enthusiasts and keepers [4], [5]. Past studies have revealed 2.1 Study Area a change of interest in which G. bicolor has been a The bird markets are located in Jalan Bintang, known as substitute to the White-crested Laughingthrush (G. the largest wildlife market in Medan city, North Sumatra, leucolophus) in market demands. Hence, the species is Indonesia. The area is characterized by the presence of reported to becoming unstable in the level of trade with the numerous wildlife species being reared and raised in risk of extinction in the future [6]. Infestation of parasites is captivity for trade purposes, including the Sumatran an important issue in captive birds, especially to the high- Laughingthrush or Garrulax bicolor. We chose four vendors density population with increasing risk of exposure of cross- as sampling sources by contacting a local middleman since infection and prolonged captivity to birds in cage [7]. there is a limited information and restricted permit given by Indication of poor management in bird markets, e.g sanitary the owner of the shops. and health care may pose a threat to the captive G. bicolor with the fatal issue of mortality [6]. 2.2 Collection and Processing of Fecal Samples A total of 120 fecal samples (20-30 g) from each individual ______G. bicolor at the selected sites (5 ind./site) were collected randomly and stored into a sterile sample cup. The fecal  Markus Mangantar Pardamean Sianturi, The Natural Resources samples directly from the cloaca or freshly dropped feces Conservation Agency in North Sumatra, Medan 20147, Indonesia. from the ground were separately sampled over a period Email: [email protected] from July to August 2019 on a weekly basis.  Adrian Hartanto, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Sumatera Utara, Medan 20155, Indonesia. 2.3 Coproscopical Analyses  Adetia Arjuna Girsang, Department of Biology, Faculty of Fecal samples were prepared following the modified Mathematics and Natural Sciences, Universitas Sumatera Utara, saturated salt flotation technique [9]. Fecal sample weighing Medan 20155, Indonesia. ± 10 g were diluted into saturated NaCl solution (1:10, w/v) in a flask. The flask was let to settle for 20 min for

2446 IJSTR©2020 www.ijstr.org INTERNATIONAL JOURNAL OF SCIENTIFIC & TECHNOLOGY RESEARCH VOLUME 9, ISSUE 04, APRIL 2020 ISSN 2277-8616 sedimentation. A drop of liquid was pipetted and spotted on TABLE 2 an object glass for microscope observation. INTENSITY AND RELATIVE DENSITY OF GASTROINTESTINAL The gastrointestinal (GI) parasites were visually identified PARASITE IN FECAL SAMPLES FROM GARRULAX BICOLOR for their resemblance morphologically to at least the genera INTENSITY RELATIVE level by using available literatures in Balai Veteriner Medan, PARASITES (Σ PARASITE/ IND.) CATEGORY DENSITY Medan city, North Sumatra [10], [11], [12]. MEAN S.D RANGE COCCIDIA 18.1 10.3 1–43 Moderate 2.4 Data Analysis EIMERIA 1.7 The data was presented in percentage (%) for prevalence and mean ± SD for intensity and frequency for relative CESTODA CHOANOTAENIA 11.7 5.1 5–20 Moderate 1.1 density [13]. The formulation for calculating parasitic RAILLIETINA 75.0 22.6 10–100 Severe 3.3 infestation is described as follows: NEMATODA AMIDOSTOMUM 13.3 5.9 1–33 Moderate 1.7

ASCARIDA 20.0 13.4 5–60 Moderate 0.6 CAPILLARIA 6.1 3.6 1–10 Moderate 0.4 HETERAKIS 9.7 5.35 2–20 Moderate 0.6

3. RESULTS AND DISCUSSION In total of 120 fecal samples examined, 68 (56.6 %) were detected positive to be infected by gastrointestinal

parasites. The prevalence of parasitic species found in fecal

samples of G. bicolor from bird markets is presented in The categorization on ecological parameters of parasites Table 1. Six helminths were recovered, which are classified was based on Williams and Williams [14] to assess the into two cestodes and four nematodes along with one status of infestation by gastrointestinal parasites to G. coccidian oocyst (Eimeria sp). Raillietina sp. was bicolor. categorized as the most frequent parasite detected (56.6

%) followed by Amidostomum (47.5 %), Eimeria (36.6 %), TABLE 1 Choanotaenia (12.5 %), Capillaria (0.07 %), Heterakis (0.06 PREVALENCE OF GASTROINTESTINAL PARASITE IN FECAL %), and Ascarida (0.03%). Scabies mites (Sarcoptes SAMPLES FROM GARRULAX BICOLOR scabiei: Sarcoptidae) are also present in the stool samples INFECTED/ PREVALENCE PARASITES CATEGORY although not considered in this study. The intensity and EXAMINED (%) relative density from each parasitic species is presented in COCCIDIA Table 2. Severe infection was shown by Raillietina EUCOCCIDIORIDA 44/120 36.67 COMMONLY EIMERIIDAE (75.0±22.6) with density of 3.3/ind, followed with the EIMERIA SP. remaining moderate infections by Ascarida (20.0±13.4), Eimeria (18.1±10.3), Choanotaenia (11.7±5.1), Heterakis CESTODA (9.7±5.35), and Capillaria (6.1±3.6). The range of infestation Cyclophyllidea found in one individual G. bicolor was the highest by Davaineidae Raillietina (10-100/ ind). Study on endoparasitic infection on Raillietina sp. 68/120 56.67 FREQUENT Dilepididae G. bicolor is still limited. A recent documentation on deadly Choanotaenia sp. 15/120 12.50 OFTEN coccidiosis was reported on G. chinensis which was caused

by the coccidian Isospora (Coccidia: Eimeriidae) through

NEMATODA the use of molecular identification [15]. In addition, our

Ascaridida finding on coccidian was only limited to Eimeria, which is

Ascaridiidae VERY classified as a common parasite with limited information on Ascarida sp. 4/120 .03 RARELY a peculiar disease to Garrulax spp. The health risks posed Heterakidae VERY Heterakis sp. 8/120 .06 by this protozoan to birds may extend from anorexia, fluffy RARELY feathers, excess diarrhea, gastrointestinal disorders, and

ENOPLIDA decreased physiological state leading to other epidemic

Capillariidae VERY diseases, e.g mycoplasmosis and colibacillosis [16], [17]. Capillaria sp. 9/120 .07 RARELY The helminths dominate in terms of prevalences, intensities Strongylida and relative densities. Although the studies on helminth Amidostomatidae parasites have been focused on commercial poultries, their Amidostomum sp. 57/120 47.50 COMMONLY presences in exotic species must also be evaluated to ensure the health risk on particular endangered species, especially the captive G. bicolor in markets. In our findings, the cestode Raillietina spp. and the nematode Amidostomum spp. are the most prevalent in G. bicolor fecal samples. Helminthes species are considered as secondary pathogen to birds which may cause anorexia, 2447 IJSTR©2020 www.ijstr.org INTERNATIONAL JOURNAL OF SCIENTIFIC & TECHNOLOGY RESEARCH VOLUME 9, ISSUE 04, APRIL 2020 ISSN 2277-8616 enteritis, ulceration and death [18]. In specific to members [8]. G. Boseret, “Zoonoses in pet birds: review and of Raillietina spp., these species are well documented in perspectives,” Vet. Res. vol. 44, no. 1, pp. 1-17, 2013 commercially-bred chickens which caused significantly low [9]. M.O. Ajala and S.O. Asaolu, “Efficiency of the salt performance in poultry industry in the tropical countries [19], flotation technique in the recovery of Ascaris [20], [21]. Until now, there is no documentation of lumbricoides eggs from the soil,” J. Helminthol, vol. parasitological disease on G. bicolor which lead into 69, no. 1, pp. 1-5, 1995. mortality. In fact, Busina et al [6] have reported the total [10]. S. Hidajati, “Atlas Parasitologi Kedokteran,” Jakarta: mortality of G. bicolor reaching 16% in bird markets with Penerbit Buku Kedokteran EGS, 2014. varying results among months. Although no direct evidence [11]. E.J. Soulsby, “Helmints, Arthopods, and Protozoa of on housing condition and health risk in the bird markets, the Domesticated .” London: The English documented endoparasites in our study may suggest the Language Book Society and Bailliere, 1986. lack or poor bird housing and care. [12]. Z.M. Anne and G.A. Conboy, “Veterinary Clinical Parasitology,” United States: John Wiley & Sons, 2012. 4. CONCLUSION [13]. L. Margolis, G.W. Esch, J.C. Holmes, A.M. Kuris, and Coproscopical analysis on Garrulax bicolor traded and G.A. Schad, “The use of ecological terms in reared in four representative bird markets in Medan city, parasitology (report of an ad hoc committee of the North Sumatra revealed the high prevalence of cestode American Society of Parasitologists),” J. Parasit. vol. Raillietina spp. (>50 %) with the discovery of one coccidia 68, pp. 131-133, 1982. (Eimeria) and six parasitic helminthes (Amidostomum, [14]. E.H. Williams and I.B. 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