COPROLOGICAL STUDY OF TREMATODE INFECTION IN REHABILITATED GREEN TURTLES AT THE TURTLE CONSERVATION AND EDUCATION CENTER BALI
Abstract
Trematode infection can affect population dynamics of C. mydas in the wild. Diversification and spatio-temporal dynamics of coastal and marine environments in Indonesia can lead to different trematode community compositions among various populations of C. mydas. This study aims to determine the types of trematodes in C. mydas that live in one feeding ground of the Indonesian waters. The research was conducted at the Turtle Conservation and Education Center (TCEC) Serangan, Bali. Nine juveniles C. mydas with the curved carapace lengths between 41 – 66 cm were observed. The turtles are confiscated by the police from a smuggling attempt to Bali, which was previously caught in the waters around Sapeken Island, East Java. Parasite examination was carried out using the Mini-Flotac® coprology technique in combination with Fill-Flotac®. Eggs were identified based on their morphological and morphometric characteristics and the number of eggs per gram (EPG) of feces was calculated according to available technical guidelines. Trematode eggs found were identical to Learedius learedi (Spirirorchiidae), Diaschistorchis pandus (Pronocephalidae), Octangium sagita (Pronocephalidae), and Enodiotrema megachondrus (Plagiorchiidae). The prevalence of L. learedi and D. pandus was 100%, while O. sagita and E. megachondrus were 77.7% and 66.6%. The highest EPG was found in L. learedi (104±57), followed by D. pandus (42±14), O. sagita (32±28), and E. megachondrus (23±19). Statistically, the mean EPG of L. learedi was significantly higher (P<0.05) from the other three types of parasites, while the EPG density of the three types of parasites other than L. learedi was not significantly different (P>0.05). The result provides an up-to-date baseline information on the type and prevalence of trematodes in C. mydas inhabited Sapeken waters of East Java. Similar studies involving turtle populations from other areas are needed to enhance the understanding of the host-parasite dynamics between turtle population stocks from various waters in Indonesia.
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References
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Adnyana IBW, Ladds PW, Blair D. 2020. Prevalence and clinico-pathological studies on trematodiasis in marine turtles in Indonesia. Int. J. Sci. Res. Pub. 10(8): 274-295.
Anderson RM, May RM. 1978. Regulation and stability of host - parasite population interactions. I. Regulatory processes. J. Anim. Ecol. 47(1): 219-247.
Barda B, Cajal P, Villagran E. 2014. Mini-FLOTAC, Kato-Katz and McMaster: three methods, one goal; highlights from north Argentina. Parasites Vectors. 7(271): 1-7.
Binoti E, Gomes MC, Junior A. De C, Werneck MR, Martin IVF, Boeloni JN. 2016. Helminth fauna of Chelonia mydas (Linnaeus, 1758) in the South of Espirito Santo State in Brasil. Helminthologia. 53(2):195-199.
Godber OF, Phythian CJ, Bosco A, Ianniello D, Coles G, Rinaldi L, Cringoli G. 2015. A comparison of the FECPAK and Mini-FLOTAC faecal egg counting techniques. Vet. Parasitol. 207(3-4): 342-345.
Catalano S, Symeou A, Marsh KJ. 2019. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasites Vectors. 12(439): 1-9.
Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, Rinaldi L. 2017. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protocols. 12(9): 1723–1732.
Dipineto L, Rinaldi L, Bosco A, Russo TP, Fioretti A, Cringoli G. 2013. Co-infection by Escherichia coli O157 and gastrointestinal strongyles in sheep. The Vet. J. 197(3): 884–885.
Esteban N, Mortimer JA, Stokes HJ. 2020. A global review of green turtle diet: sea surface temperature as a potential driver of omnivory levels. Mar. Biol. 167(183): 1-17.
Federica M, Rudi C, Nancy P, Cinzia T, Erica M. 2022. A comparative study of Mini-FLOTAC with traditional coprological techniques in the analysis of cetacean fecal samples. Front. Vet. Sci. 9: 1-7.
Flint M, Patterson-Kane JC, Limpus CJ, Mills PC. 2010. Health surveillance of stranded green turtles in Southern Queensland, Australia (2006-2009): an epidemiological analysis of causes of disease and mortality. Eco. Health. 7: 135-145.
Flint M, Patterson-Kane JC, Limpus CJ, Mills PC. 2015. Trends in marine turtle strandings along the east Queensland, Australia coast, between 1996 and 2013. J. Mar. Biol. 2015: 7.
Gordon AN, Kelly WR,Cribb TH. 1998. Lesions caused by cardiovascular flukes (Digenea: Spirorchidae) in stranded green turtles (Chelonia mydas). Vet. Pathol. 35: 21–30.
Greiner EC. 2013. Parasites of Marine Turtles. In: Wyneken J, Lohmann KJ, Musick JA, editors. The Biology of Sea Turtles. Volume III. CRC Press; Boca Raton, FL, USA, Pp. 249–284.
Hirth HF, Schaffer WM. 1974. Survival Rate of the green turtle, Chelonia mydas. Necessary to Maintain Stable Populations. 1974(2): 544-546.
Irvine RJ. 2006. Parasites and the dynamics of wild mammal populations. Anim. Sci. 82(06): 775-781.
Jacobson ER, Homer BL, Stacy BA, Greiner EC, Szabo NJ, Chrisman CL, Origgi F, Coberley S, Foley AM, Landsberg JH. 2006. Neurological disease in wild loggerhead sea turtles Caretta caretta. Dis. Aqua. Org. 70: 139–154.
Kołodziej-Sobocińska M. 2019. Factors affecting the spread of parasites in populations of wild European terrestrial mammals. Mammal Res. 64: 301–318.
Kripa V, Prema D, Varghese, Molly N, Rekha KS, Sobhana R, Vidya B, Vivekanand S, Uma. 2023 Book of Abstracts & Success Stories National Conference on Marine Debris COMAD 2018. Marine Biological Association of India, Kochi. http://eprints.cmfri.org.in/id/eprint/12700 .
Lee PL, Luschi P, Hays GC. 2007. Detecting female precise natal philopatry in green turtles using assignment methods. Mol. Ecol. 16(1): 61-74.
Lozano J, Almeida C, Victório AC, Melo P, Rodrigues JP, Rinaldi L, Cringoli G, Gomes L, Oliveira M, Paz-Silva A, Madeira de Carvalho L. 2021. Implementation of Mini-FLOTAC in routine diagnosis of coccidia and helminth infections in domestic and exotic birds. Vet. Sci. 8(8):1-12.
Mahony KE, Sian E, Sharon AL, Hugues B, Anouk G, Emily G, Nicolas S, Xavier M, Shelagh KM, Sarah CC. 2022. Drivers of growth in a keystone fished species along the European Atlantic coast: The common cockle Cerastoderma edule. J. Sea Res. 179: 1-9.
Marangi M, Carlino P, Profico C, Olivieri V, Totaro G, Furii G, Marzano G, Roberto AP. 2020. First multicenter coprological survey on helminth parasite communities of free-living loggerhead sea turtles Caretta caretta from the Adriatic Sea and Northern Ionian Sea. Int. J. Parasitol. Parasites and Wildlife. 11: 207-212.
Maulid D, Dwi S, Fidry RI, Kusuma D. 2018. Cause of the death sea turtle stranded in nesting beach (Paloh, West Kalimantan) period from February to April 2018. Paper presented Proc. of the 20th FAVA Congress & The 15th KIVNAS PDHI, Bali Nov 1-3, 2018.
MB da Silva, DF de Oliveira, FV Santos, CDS Aguiar, IS Prado, DA Brandão, AA Pereira, TS de Queiroz, L Tomazi, br Ricardo Evangelista Fraga.2022. Gastrointestinal parasites in wild and exotic animals from a zoo in the State of Bahia, Brazil - first record. Res. Soc. Develop. 11(13): 1-22.
Pace A, Rinaldi L, Ianniello D, Borrelli L, Cringoli G, Fioretti A, Hochscheid S, Dipineto L. 2019. Gastrointestinal investigation of parasites and Enterobacteriaceae in loggerhead sea turtles from Italian coasts. BMC Vet. Res. 15(370): 1-9.
Preston D, Johnson P. 2010. Ecological Consequences of Parasitism. Nat. Edu. Knowledge. 1(8): 39
Santoro M, Greiner E, Morales J, Rodriguez-Ortiz B. 2006. Digenetic Trematode Community in nesting green sea turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. J. Parasitol. 92(6): 1202-1206.
Santoro M, Morales JA, Rodriguez-Ortiz B. 2007a. Some digenetic trematodesof the olive ridley sea turtle, Lepidochelys olivacea (Testudines:Cheloniidae) in Costa Rica. Helminthologia. 44(1): 25 – 28.
Santoro M, Morales JA, Rodriguez-Ortiz B. 2007b. Spirorchiidiosis (Digenea: Spirorchiidae) and lesions associated with parasites in Caribbean green sea turtles (Chelonia mydas). Vet. Rec. 161(14): 482 – 486
Santoro M, Morales J, Bolaáos F, Chaves G, Stefano M. 2015. Helminths of hawksbill turtle (Eretmochelys imbricata) from the Pacific coast of Costa Rica. Helminthologia. 52(1): 67-70.
Santoro M, Iaccarino D, Bellisario B. 2020. Host biological factors and geographic locality influence predictors of parasite communities in sympatric sparid fishes off the southern Italian coast. Sci. Rep. 10(1): 13283.
Santos RG, Martins AS, Farias JN, Horta PA, Pinheiro HT, Torezani E, Baptistotte C, Seminoff JA, Balazz GH, Work TM. 2011. Coastal habitat degradation and green sea turtle diets in Southeastern Brazil. Marine Pollut. Bul. 62(6): 1297-1302.
Simon Kin-Fung Chan, I-Jiunn Cheng, Ting Zhou, Hua-Jie Wang, He-Xiang Gu, Xiao-Jun Song. 2007. A comprehensive overview of the population and conservation status of sea turtles in China. Chelonian Conserv. Biol. 6(2): 185–198.
Stacy BA, Foley AM, Greiner E, Herbst LH, Bolten A, Klein P, Manire CA, Jacobson ER. 2010. Spirorchiidiasis in stranded loggerhead Caretta caretta and green turtles Chelonia mydas in Florida (USA): Host pathology and significance. Dis. Aquat. Orgs. 89: 237–259.
Stubbs JL, Marn N, Vanderklift MA, Fossette S, Mitchell NJ. 2020. Simulated growth and reproduction of green turtles (Chelonia mydas) under climate change and marine heat wave scenarios. Ecol. Modelling. 431: 304-380.
Suastika P, Adnyana IBW, Suprapti D. 2012. Profil seks rasio tukik penyu hijau (Chelonia mydas) pada penetasan alami dan non-alami di pantai Sukamade Kabupaten Banyuwangi. Bul. Vet. Udayana. 4(2): 47-53.
Thompson AN, Kennedy AJ, Holmes J, Kearney G. 2010. Arrow leaf clover improves lamb growth rates in late spring and early summer compared with subterranean clover pastures in south-west Victoria. Anim. Prod. Sci. 50(8): 807-816.
Werneck M, Silva R. 2015. Helminth Parasites of Juvenile Green Turtles Chelonia mydas (Testudines: Cheloniidae) in Brazil. The J. Parasitol. 101(10): 160-780.
Wilcox CP, Melody S, Qamar T, Kathy H, Britta. 2018. A quantitative analysis linking sea turtle mortality and plastic debris ingestion. Sci. Rep. 8(12836): 1-11.
Work TM, Balazs GH, Summers TM, Hapdei JR, Tagarino AP. 2015. Causes of mortality in green turtles from Hawaii and the insular Pacific exclusive of fibropapillomatosis. Dis. Aquat. Org. 115: 103-110.
Zainudin IM, Pet-Soede L, Hitipeuw C, Adnyana IBW. 2007. Interaction of Sea Turtles with Indonesian Fisheries – Preliminary Finding. Indian Ocean Turtle Newsletter. 6: 1-10.
Adnyana W, Hitipeuw C. 2009. Panduan Melakukan Pemantauan Populasi Penyu di Pantai Peneluran di Indonesia. Diterbitkan oleh WWF-Indonesia, Jakarta. Pp. 1-31.
Adnyana W, Damriyasa IM, Trilaksana IGNB, Ratha IMJ, Hitipeuw C. 2010. Laporan Sigi Pemanfaatan dan Perdagangan Penyu di Bali dan Rekomendasi Pengentasannya. Fakultas Kedokteran Hewan Universitas Udayana dan WWF Indonesia, Pp. 1-10.
Adnyana IBW, Ladds PW, Blair D. 2020. Prevalence and clinico-pathological studies on trematodiasis in marine turtles in Indonesia. Int. J. Sci. Res. Pub. 10(8): 274-295.
Anderson RM, May RM. 1978. Regulation and stability of host - parasite population interactions. I. Regulatory processes. J. Anim. Ecol. 47(1): 219-247.
Barda B, Cajal P, Villagran E. 2014. Mini-FLOTAC, Kato-Katz and McMaster: three methods, one goal; highlights from north Argentina. Parasites Vectors. 7(271): 1-7.
Binoti E, Gomes MC, Junior A. De C, Werneck MR, Martin IVF, Boeloni JN. 2016. Helminth fauna of Chelonia mydas (Linnaeus, 1758) in the South of Espirito Santo State in Brasil. Helminthologia. 53(2):195-199.
Godber OF, Phythian CJ, Bosco A, Ianniello D, Coles G, Rinaldi L, Cringoli G. 2015. A comparison of the FECPAK and Mini-FLOTAC faecal egg counting techniques. Vet. Parasitol. 207(3-4): 342-345.
Catalano S, Symeou A, Marsh KJ. 2019. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasites Vectors. 12(439): 1-9.
Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, Rinaldi L. 2017. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protocols. 12(9): 1723–1732.
Dipineto L, Rinaldi L, Bosco A, Russo TP, Fioretti A, Cringoli G. 2013. Co-infection by Escherichia coli O157 and gastrointestinal strongyles in sheep. The Vet. J. 197(3): 884–885.
Esteban N, Mortimer JA, Stokes HJ. 2020. A global review of green turtle diet: sea surface temperature as a potential driver of omnivory levels. Mar. Biol. 167(183): 1-17.
Federica M, Rudi C, Nancy P, Cinzia T, Erica M. 2022. A comparative study of Mini-FLOTAC with traditional coprological techniques in the analysis of cetacean fecal samples. Front. Vet. Sci. 9: 1-7.
Flint M, Patterson-Kane JC, Limpus CJ, Mills PC. 2010. Health surveillance of stranded green turtles in Southern Queensland, Australia (2006-2009): an epidemiological analysis of causes of disease and mortality. Eco. Health. 7: 135-145.
Flint M, Patterson-Kane JC, Limpus CJ, Mills PC. 2015. Trends in marine turtle strandings along the east Queensland, Australia coast, between 1996 and 2013. J. Mar. Biol. 2015: 7.
Gordon AN, Kelly WR,Cribb TH. 1998. Lesions caused by cardiovascular flukes (Digenea: Spirorchidae) in stranded green turtles (Chelonia mydas). Vet. Pathol. 35: 21–30.
Greiner EC. 2013. Parasites of Marine Turtles. In: Wyneken J, Lohmann KJ, Musick JA, editors. The Biology of Sea Turtles. Volume III. CRC Press; Boca Raton, FL, USA, Pp. 249–284.
Hirth HF, Schaffer WM. 1974. Survival Rate of the green turtle, Chelonia mydas. Necessary to Maintain Stable Populations. 1974(2): 544-546.
Irvine RJ. 2006. Parasites and the dynamics of wild mammal populations. Anim. Sci. 82(06): 775-781.
Jacobson ER, Homer BL, Stacy BA, Greiner EC, Szabo NJ, Chrisman CL, Origgi F, Coberley S, Foley AM, Landsberg JH. 2006. Neurological disease in wild loggerhead sea turtles Caretta caretta. Dis. Aqua. Org. 70: 139–154.
Kołodziej-Sobocińska M. 2019. Factors affecting the spread of parasites in populations of wild European terrestrial mammals. Mammal Res. 64: 301–318.
Kripa V, Prema D, Varghese, Molly N, Rekha KS, Sobhana R, Vidya B, Vivekanand S, Uma. 2023 Book of Abstracts & Success Stories National Conference on Marine Debris COMAD 2018. Marine Biological Association of India, Kochi. http://eprints.cmfri.org.in/id/eprint/12700 .
Lee PL, Luschi P, Hays GC. 2007. Detecting female precise natal philopatry in green turtles using assignment methods. Mol. Ecol. 16(1): 61-74.
Lozano J, Almeida C, Victório AC, Melo P, Rodrigues JP, Rinaldi L, Cringoli G, Gomes L, Oliveira M, Paz-Silva A, Madeira de Carvalho L. 2021. Implementation of Mini-FLOTAC in routine diagnosis of coccidia and helminth infections in domestic and exotic birds. Vet. Sci. 8(8):1-12.
Mahony KE, Sian E, Sharon AL, Hugues B, Anouk G, Emily G, Nicolas S, Xavier M, Shelagh KM, Sarah CC. 2022. Drivers of growth in a keystone fished species along the European Atlantic coast: The common cockle Cerastoderma edule. J. Sea Res. 179: 1-9.
Marangi M, Carlino P, Profico C, Olivieri V, Totaro G, Furii G, Marzano G, Roberto AP. 2020. First multicenter coprological survey on helminth parasite communities of free-living loggerhead sea turtles Caretta caretta from the Adriatic Sea and Northern Ionian Sea. Int. J. Parasitol. Parasites and Wildlife. 11: 207-212.
Maulid D, Dwi S, Fidry RI, Kusuma D. 2018. Cause of the death sea turtle stranded in nesting beach (Paloh, West Kalimantan) period from February to April 2018. Paper presented Proc. of the 20th FAVA Congress & The 15th KIVNAS PDHI, Bali Nov 1-3, 2018.
MB da Silva, DF de Oliveira, FV Santos, CDS Aguiar, IS Prado, DA Brandão, AA Pereira, TS de Queiroz, L Tomazi, br Ricardo Evangelista Fraga.2022. Gastrointestinal parasites in wild and exotic animals from a zoo in the State of Bahia, Brazil - first record. Res. Soc. Develop. 11(13): 1-22.
Pace A, Rinaldi L, Ianniello D, Borrelli L, Cringoli G, Fioretti A, Hochscheid S, Dipineto L. 2019. Gastrointestinal investigation of parasites and Enterobacteriaceae in loggerhead sea turtles from Italian coasts. BMC Vet. Res. 15(370): 1-9.
Preston D, Johnson P. 2010. Ecological Consequences of Parasitism. Nat. Edu. Knowledge. 1(8): 39
Santoro M, Greiner E, Morales J, Rodriguez-Ortiz B. 2006. Digenetic Trematode Community in nesting green sea turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. J. Parasitol. 92(6): 1202-1206.
Santoro M, Morales JA, Rodriguez-Ortiz B. 2007a. Some digenetic trematodesof the olive ridley sea turtle, Lepidochelys olivacea (Testudines:Cheloniidae) in Costa Rica. Helminthologia. 44(1): 25 – 28.
Santoro M, Morales JA, Rodriguez-Ortiz B. 2007b. Spirorchiidiosis (Digenea: Spirorchiidae) and lesions associated with parasites in Caribbean green sea turtles (Chelonia mydas). Vet. Rec. 161(14): 482 – 486
Santoro M, Morales J, Bolaáos F, Chaves G, Stefano M. 2015. Helminths of hawksbill turtle (Eretmochelys imbricata) from the Pacific coast of Costa Rica. Helminthologia. 52(1): 67-70.
Santoro M, Iaccarino D, Bellisario B. 2020. Host biological factors and geographic locality influence predictors of parasite communities in sympatric sparid fishes off the southern Italian coast. Sci. Rep. 10(1): 13283.
Santos RG, Martins AS, Farias JN, Horta PA, Pinheiro HT, Torezani E, Baptistotte C, Seminoff JA, Balazz GH, Work TM. 2011. Coastal habitat degradation and green sea turtle diets in Southeastern Brazil. Marine Pollut. Bul. 62(6): 1297-1302.
Simon Kin-Fung Chan, I-Jiunn Cheng, Ting Zhou, Hua-Jie Wang, He-Xiang Gu, Xiao-Jun Song. 2007. A comprehensive overview of the population and conservation status of sea turtles in China. Chelonian Conserv. Biol. 6(2): 185–198.
Stacy BA, Foley AM, Greiner E, Herbst LH, Bolten A, Klein P, Manire CA, Jacobson ER. 2010. Spirorchiidiasis in stranded loggerhead Caretta caretta and green turtles Chelonia mydas in Florida (USA): Host pathology and significance. Dis. Aquat. Orgs. 89: 237–259.
Stubbs JL, Marn N, Vanderklift MA, Fossette S, Mitchell NJ. 2020. Simulated growth and reproduction of green turtles (Chelonia mydas) under climate change and marine heat wave scenarios. Ecol. Modelling. 431: 304-380.
Suastika P, Adnyana IBW, Suprapti D. 2012. Profil seks rasio tukik penyu hijau (Chelonia mydas) pada penetasan alami dan non-alami di pantai Sukamade Kabupaten Banyuwangi. Bul. Vet. Udayana. 4(2): 47-53.
Thompson AN, Kennedy AJ, Holmes J, Kearney G. 2010. Arrow leaf clover improves lamb growth rates in late spring and early summer compared with subterranean clover pastures in south-west Victoria. Anim. Prod. Sci. 50(8): 807-816.
Werneck M, Silva R. 2015. Helminth Parasites of Juvenile Green Turtles Chelonia mydas (Testudines: Cheloniidae) in Brazil. The J. Parasitol. 101(10): 160-780.
Wilcox CP, Melody S, Qamar T, Kathy H, Britta. 2018. A quantitative analysis linking sea turtle mortality and plastic debris ingestion. Sci. Rep. 8(12836): 1-11.
Work TM, Balazs GH, Summers TM, Hapdei JR, Tagarino AP. 2015. Causes of mortality in green turtles from Hawaii and the insular Pacific exclusive of fibropapillomatosis. Dis. Aquat. Org. 115: 103-110.
Zainudin IM, Pet-Soede L, Hitipeuw C, Adnyana IBW. 2007. Interaction of Sea Turtles with Indonesian Fisheries – Preliminary Finding. Indian Ocean Turtle Newsletter. 6: 1-10.
Published
2023-04-02
How to Cite
PERMADI, Aditia; ADNYANA, Ida Bagus Windia; SUARTINI, I Gusti Agung Ayu.
COPROLOGICAL STUDY OF TREMATODE INFECTION IN REHABILITATED GREEN TURTLES AT THE TURTLE CONSERVATION AND EDUCATION CENTER BALI.
Buletin Veteriner Udayana, [S.l.], p. 971-981, apr. 2023.
ISSN 2477-2712.
Available at: <https://ojs.unud.ac.id/index.php/buletinvet/article/view/99077>. Date accessed: 21 nov. 2024.
doi: https://doi.org/10.24843/bulvet.2023.v15.i05.p34.
Section
Articles
