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Population dynamics and diversity of trematode infections in Bithynia siamensis goniomphalos in an irrigated area in northeast Thailand

Published online by Cambridge University Press:  12 November 2021

Kulthida Y. Kopolrat
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand
Paiboon Sithithaworn*
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand
Nadda Kiatsopit
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand
Jutamas Namsanor
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand
Opal Pitaksakulrat
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Patiwat Yasaka
Affiliation:
Faculty of Management Technology, Rajamangala University of Technology Isan, Surin Campus, Surin, Thailand
Prasert Saichua
Affiliation:
Tropical Medicine Graduate Program, Academic Affairs, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand WHO Collaborating Centre for Research and Control of Opisthorchiasis (Southeast Asian Liver fluke Disease), Tropical Disease Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
Weerachai Saijuntha
Affiliation:
Walai Rukhavej Botanical Research Institute, Mahasarakham University, Maha Sarakham 44150, Thailand
Smarn Tesana
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Ross H. Andrews
Affiliation:
Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand Faculty of Medicine, Imperial College London, St Mary's Campus, South Wharf Street, London W2 1NY, UK
Trevor N. Petney
Affiliation:
Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand State Museum of Natural History Karlsruhe, Evolution and Paleontology, Erbprinzenstrasse 13, 76133 Karlsruhe, Germany
*
Author for correspondence: Paiboon Sithithaworn, E-mail: [email protected]

Abstract

Several trematodes including Opisthorchis viverrini utilize Bithynia siamensis goniomphalos as a snail intermediate host in their life cycles. In order to capture a comprehensive range of host–parasite interactions and their transmission dynamic patterns, B. s. goniomphalos were sampled monthly over 4 consecutive years in an irrigated paddy-field habitat in northeast Thailand. Using a standard cercarial shedding method, a high diversity of trematodes (17 types) was recovered. Virgulate xiphidiocercariae were the most prevalent (7.84%) followed by O. viverrini (0.71%). In addition to seasonal and environmental factors, the quantity of irrigation water for rice cultivation correlated with transmission dynamics of trematodes in B. s. goniomphalos. The peak prevalence of all trematode infections combined in the snails shifted from the cool-dry season in 2010–2012 to the hot-dry season in 2013 associated with an increasing quantity of water irrigation. A low frequency of mixed trematode infections was found, indicating that the emergence of virgulate cercariae, but not of O. viverrini, was negatively impacted by the presence of other trematodes in the same snail. Taken together, the observed results suggest that interactions between host and parasite, and hence transmission dynamics, depend on specific characteristics of the parasite and environmental factors including irrigated water for rice cultivation.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Adam, R, Arnold, H, Pipitgool, V, Sithithaworn, P, Hinz, E and Storch, V (1993) Studies on lophocercous cercariae from Bithynia siamensis goniomphalos (Prosobranchia: Bithyniidae). The Southeast Asian Journal of Tropical Medicine and Public Health 24, 697700.Google Scholar
Altizer, S, Dobson, A, Hosseini, P, Hudson, P, Pascual, M and Rohani, P (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467484.CrossRefGoogle ScholarPubMed
Anderson, RM and May, RM (1991) Infectious Diseases of Humans, Dynamics and Control. New York, USA: Oxford University Press.Google Scholar
Basch, PF, Lie, KJ and Heyneman, D (1969) Antagonistic interaction between strigeid and schistosome sporocysts within a snail host. Journal of Parasitology 55, 753758.CrossRefGoogle ScholarPubMed
Bayne, CJ and Loker, ES (1987) Survival within the host. In Rollinson, D and Simpson, AJG (eds), The Biology of Schistosomes from Genes to Latrines. London, UK: Academic Press, pp. 321346.Google Scholar
Brandt, RAM (1974) The non-marine aquatic mollusca of Thailand. Archiv für Molluskenkunde 105, 1423.Google Scholar
Brockelman, WY, Upatham, ES, Viyanant, V, Ardsungnoen, S and Chantanawat, R (1986) Field studies on the transmission of the human liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. International Journal for Parasitology 16, 545552.CrossRefGoogle ScholarPubMed
Cattadori, IM, Haydon, DT and Hudson, PJ (2005) Parasites and climate synchronize red grouse populations. Nature 433, 737741.CrossRefGoogle ScholarPubMed
Chitramvong, YP (1992) The Bithyniidae (Gastropoda: Prosobranchia) of Thailand: comparative external morphology. Malacological Review 25, 2138.Google Scholar
Chontananarth, T, Wongsawad, C and Chai, JY (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai Province, Thailand. Asian Pacific Journal of Tropical Biomedicine 3, 237243.CrossRefGoogle Scholar
Clausen, JH, Madsen, H, Murrell, KD, Phan Thi, V, Nguyen Manh, H, Viet, KN and Dalsgaard, A (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Neglected Tropical Diseases 6, e1945.CrossRefGoogle ScholarPubMed
Ditrich, O, Scholz, T and Giboda, M (1990) Occurrence of some medically important flukes (Trematoda: Opisthorchiidae and Heterophyidae) in Nam Ngum water reservoir, Laos. The Southeast Asian Journal of Tropical Medicine and Public Health 21, 482488.Google Scholar
Ditrich, O, Nasincova, V, Scholz, T and Giboda, M (1992) Larval stages of medically important flukes (Trematoda) from Vientiane Province, Laos. Part II. Cercariae. Annales de Parasitologie Humaine et Comparee 67, 7581.CrossRefGoogle ScholarPubMed
Ditrich, O, Schoiz, T, Aguiree-Macedo, L and Vargas-Vazquez, J (1997) Larval stages of trematodes from freshwater molluscs of the Yucatan Peninsula, Mexico. Folia Parasitlogica 44, 109127.Google Scholar
Esch, GW, Curtis, LA and Barger, MA (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123(suppl), S57S75.CrossRefGoogle ScholarPubMed
Fernandez, J and Esch, GW (1991a) Guild structure of larval trematodes in the snail Helisoma anceps: patterns and processes at the individual host level. Journal of Parasitology 77, 528539.CrossRefGoogle Scholar
Fernandez, J and Esch, GW (1991b) The component community structure of larval trematodes in the pulmonate snail Helisoma anceps. Journal of Parasitology 77, 540550.CrossRefGoogle Scholar
Frandsen, F (1987) Control of schistosomiasis by use of biological control of snail hosts with special reference to competition. Memorias do Instituto Oswaldo Cruz 82, 129133.CrossRefGoogle Scholar
Giboda, M, Ditrich, O, Scholz, T, Viengsay, T and Bouaphanh, S (1991) Human Opisthorchis and Haplorchis infections in Laos. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 538540.CrossRefGoogle ScholarPubMed
Haas, W (1994) Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109(suppl), S15S29.CrossRefGoogle ScholarPubMed
Hill, D (2005) Handbook of Biodiversity Methods : Survey, Evaluation and Monitoring. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Hillebrand, H (2008) Dominance. In Fath, SEJD (ed.), Encyclopedia of Ecology, Oxford, UK: Academic Press, pp. 938944.CrossRefGoogle Scholar
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: the great neglected tropical diseases. The Journal of Clinical Investigation 118, 13111321.CrossRefGoogle ScholarPubMed
Ito, J, Papasarathorn, T and Tongkoom, B (1962) Studies on cercariae from fresh water snails in Thailand. Japanese Journal of Medical Science and Biology 15, 249270.CrossRefGoogle Scholar
Jourdane, J and Theron, A (1987) Larval development: eggs to cercariae. In Rollinson, D and Simpson, AJG (eds), The Biology of Schistosomes from Genes to Latrines. London, UK: Academic Press, pp. 83106.Google Scholar
Keiser, J and Utzinger, J (2005) Emerging foodborne trematodiasis. Emerging Infectious Diseases 11, 15071514.CrossRefGoogle ScholarPubMed
Keiser, J and Utzinger, J (2009) Food-borne trematodiases. Clinical Microbiology Reviews 22, 466483.CrossRefGoogle ScholarPubMed
Kiatsopit, N, Sithithaworn, P, Saijuntha, W, Boonmars, T, Tesana, S, Sithithaworn, J, Petney, TN and Andrews, RH (2012) Exceptionally high prevalence of infection of Bithynia siamensis goniomphalos with Opisthorchis viverrini cercariae in different wetlands in Thailand and Lao PDR. American Journal of Tropical Medicine and Hygiene 86, 464469.CrossRefGoogle ScholarPubMed
Kiatsopit, N, Sithithaworn, P, Kopolrat, K, Namsanor, J, Andrews, RH and Petney, TN (2015) Trematode diversity in the freshwater snail Bithynia siamensis goniomphalos sensu lato from Thailand and Lao PDR. Journal of Helminthology 90, 312320. doi: 10.1017/S0022149X15000292CrossRefGoogle ScholarPubMed
Kim, K, Dobson, AP, Gulland, FMD and Harvell, CD (2005) Diseases and the conservation of marine biodiversity. In Norse, EA and Crowde, LB (eds), The Science of Maintaining the Sea's Biodiversity. Washington, DC: Island Press, pp. 149166.Google Scholar
Kopolrat, K, Sithithaworn, P, Kiatsopit, N, Namsanor, J, Laoprom, N, Tesana, S, Andrews, RH and Petney, TN (2020) Influence of water irrigation schemes and seasonality on transmission dynamics of Opisthorchis viverrini in the snail intermediate host, Bithynia siamensis goniomphalos in rice paddy fields in Northeast Thailand. American Journal of Tropical Medicine and Hygiene 103, 276286.CrossRefGoogle ScholarPubMed
Krailas, D, Namchote, S, Koonchornboon, T, Dechruksa, W and Boonmekam, D (2014) Trematodes obtained from the thiarid freshwater snail Melanoides tuberculata (Müller, 1774) as vector of human infections in Thailand. Zoosystematics and Evolution 90, 5786.CrossRefGoogle Scholar
Lafferty, KD, Sammond, DT and Kuris, AM (1994) Analysis of larval trematode communities. Ecology 75, 22752285.CrossRefGoogle Scholar
Lim, HK and Heyneman, D (1972) Intramolluscan inter-trematode antagonism: a review of factors influencing the host–parasite system and its possible role in biological control. Advances in Parasitology 10, 191268.CrossRefGoogle ScholarPubMed
Lohachit, C (2004–2005) Ecological studies of Bithynia siamensis goniomphalos, a snail intermediate host of Opisthorchis viverrini, in Khon Kaen Province, Northeast Thailand. Malacological Review 37/38, 126.Google Scholar
Loy, C and Haas, W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878882.Google Scholar
Machado, SM, Magalhaes, LA and de Artigas, PT, da Cordeiro, NS and de Carvalho, JF (1988) Verification of antagonism between larvae of Schistosoma mansoni and other Digenea in Biomphalaria tenagophila, a planorbid mollusc from a natural breeding in the region of Campinas, SP, Brazil. Revista de Saúde Pública 22, 484488.CrossRefGoogle ScholarPubMed
McCarthy, HO, Fitzpatrick, SM and Irwin, SW (2004) Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages. Parasitology 128, 714.CrossRefGoogle ScholarPubMed
Mohammed, NA, Madsen, H and Ahmed, AA (2016) Types of trematodes infecting freshwater snails found in irrigation canals in the East Nile locality, Khartoum, Sudan. Infectious Diseases of Poverty 5, 1626. doi: 10.1186/s40249-016-0108-yCrossRefGoogle ScholarPubMed
Moraes, J, Silva, MP, Ohlweiler, FP and Kawano, T (2009) Schistosoma mansoni and other larval trematodes in Biomphalaria tenagophila (Planorbidae) from Guarulhos, Sao Paulo State, Brazil. The Revista do Instituto de Medicina Tropical de São Paulo 51, 7782.CrossRefGoogle ScholarPubMed
Mouritsen, KN and Poulin, R (2002) Parasitism, climate oscillations and the structure of natural communities. Oikos 97, 462468.CrossRefGoogle Scholar
Namsanor, J, Sithithaworn, P, Kopolrat, K, Kiatsopit, N, Pitaksakulrat, O, Tesana, S, Andrews, RH and Petney, TN (2015) Seasonal transmission of Opisthorchis viverrini sensu lato and a lecithodendriid trematode species in Bithynia siamensis goniomphalos snails in Northeast Thailand. American Journal of Tropical Medicine and Hygiene 93, 8793. doi: 10.4269/ajtmh.14-0639CrossRefGoogle Scholar
Ngern-klun, R, Sukontason, KL, Tesana, S, Sripakdee, D, Irvine, KN and Sukontason, K (2006) Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 37, 662672.Google ScholarPubMed
Nithiuthai, S, Wiwanitkit, V, Suwansaksri, J and Chaengphukeaw, P (2002) A survey of trematode cercariae in Bithynia goniomphalos in northeast Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 33(suppl. 3), 106109.Google ScholarPubMed
Petney, TN (1997) Ecological implications of control strategies: arthropods of domestic and production animals. International Journal for Parasitology 27, 155165.CrossRefGoogle ScholarPubMed
Petney, TN, Sithithaworn, P, Andrews, R, Kiatsopit, N, Tesana, S, Grundy-Warr, C and Ziegler, A (2012) The ecology of the Bithynia first intermediate hosts of Opisthorchis viverrini. Parasitology International 61, 3845.CrossRefGoogle ScholarPubMed
Sandland, GJ and Minchella, DJ (2003) Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134, 479486.CrossRefGoogle ScholarPubMed
Schell, SC (1970) How to Know the Trematode. Dubuque, IA: WMC Brown Company Publishers.Google Scholar
Sorensen, RE and Minchella, DJ (2001) Snail–trematode life history interactions: past trends and future directions. Parasitology 123, S3S18.CrossRefGoogle ScholarPubMed
Sousa, WP (1990) Spatial scale and the processes structuring a guild of larval trematode parasites. In Esch, G, Bush, A and Aho, J (eds), Parasite Communities: Patterns and Processes. Chaman and Hall, London, UK: Springer Netherlands, pp. 4167.CrossRefGoogle Scholar
Sousa, WP (1992) Interspecific interactions among larval trematode parasites of freshwater and marine snails. American Zoologist 32, 583592.CrossRefGoogle Scholar
Sousa, WP (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103128.CrossRefGoogle Scholar
Spellerberg, IF and Fedor, PJ (2003) A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–Wiener’ index. Global Ecology and Biogeography 12, 177183.CrossRefGoogle Scholar
Sri-Aroon, P, Butraporn, P, Limsomboon, J, Kerdpuech, Y, Kaewpoolsri, M and Kiatsiri, S (2005) Freshwater mollusks of medical importance in Kalasin Province, northeast Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 36, 653657.Google ScholarPubMed
Sri-Aroon, P, Butraporn, P, Limsoomboon, J, Kaewpoolsri, M, Chusongsang, Y, Charoenjai, P, Chusongsang, P, Numnuan, S and Kiatsiri, S (2007) Freshwater mollusks at designated areas in eleven provinces of Thailand according to the water resource development projects. The Southeast Asian Journal of Tropical Medicine and Public Health 38, 294301.Google Scholar
Tabbabi, A, Ghrab, J, Aoun, K, Ready, PD and Bouratbine, A (2011) Habitats of the sandfly vectors of Leishmania tropica and L. major in a mixed focus of cutaneous leishmaniasis in southeast Tunisia. Acta Tropica 119, 131137.CrossRefGoogle Scholar
Tesana, S, Thapsripair, P, Suwannatrai, A, Harauy, S, Piratae, S, Khampoosa, P, Thammasiri, C, Prasopdee, S, Kulsantiwong, J, Chalorkpunrut, P and Jones, MK (2014) Parasite surveys and environmental management for prevention of parasitic infection in cultivated Barbonymus gonionotus (Cyprinidae) in fishponds, in an opisthorchiasis endemic area of northeast Thailand. Aquaculture 428-429, 5460.CrossRefGoogle Scholar
Ukong, S, Krailas, D, Dangprasert, T and Channgarm, P (2007) Studies on the morphology of cercariae obtained from freshwater snails at Erawan Waterfall, Erawan National Park, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 38, 302312.Google ScholarPubMed
Upatham, ES, Sornmani, S, Kitikoon, V, Lohachit, C and Bruch, JB (1983) Identification key for fresh-brackish water snails of Thailand. Malacological Review 16, 107132.Google Scholar
Wang, YC, Ho, RC, Feng, CC, Namsanor, J and Sithithaworn, P (2015) An ecological study of Bithynia snails, the first intermediate host of Opisthorchis viverrini in northeast Thailand. Acta Tropica 141, 244252.CrossRefGoogle ScholarPubMed
Williams, JA and Esch, GW (1991) Infra- and component community dynamics in the pulmonate snail Helisoma anceps, with special emphasis on the hemiurid trematode Halipegus occidualis. Journal of Parasitology 77, 246253.CrossRefGoogle Scholar
Wykoff, DE, Harinasuta, C, Juttijudata, P and Winn, MM (1965) Opisthorchis viverrini in Thailand – the life cycle and comparison with O. Felineus. Journal of Parasitology 51, 207214.CrossRefGoogle ScholarPubMed
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic trematodes of Vertebrates. Tokyo, Japan: Keiguku Publication Co.Google Scholar
Ziegler, AD, Petney, TN, Grundy-Warr, C, Andrews, RH, Baird, IG, Wasson, RJ and Sithithaworn, P (2013) Dams and disease triggers on the lower Mekong River. PLoS Neglected Tropical Diseases 7, e2166.CrossRefGoogle ScholarPubMed
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