Hostname: page-component-6bf8c574d5-r8w4l Total loading time: 0 Render date: 2025-03-11T17:12:50.290Z Has data issue: false hasContentIssue false

Aestivation and its impact on the survival of snail intermediate hosts and trematode transmission in rice paddies

Published online by Cambridge University Press:  10 March 2025

K. Chantima*
Affiliation:
Environmental Science and Technology Program, Faculty of Science and Technology, Chiang Rai Rajabhat University, Chiang Rai, Thailand
K. Suk-ueng
Affiliation:
Environmental Science and Technology Program, Faculty of Science and Technology, Chiang Rai Rajabhat University, Chiang Rai, Thailand
T. Tananoi
Affiliation:
Environmental Science and Technology Program, Faculty of Science and Technology, Chiang Rai Rajabhat University, Chiang Rai, Thailand
T. Prasertsin
Affiliation:
Biological Science Program, Faculty of Science and Technology, Chiang Rai Rajabhat University, Chiang Rai, Thailand
*
Corresponding author: K. Chantima; Email: [email protected]

Abstract

In this study, we investigated the diversity and survival of aestivating snails in dry-season rice paddies, focusing on their role as intermediate hosts for trematodes. A total of 1,159 snails from various families were collected and analysed, revealing nine species, primarily from the Bithyniidae family, with Bithynia siamensis siamensis being the most abundant. Of the nine species collected, the most common species, B. s. siamensis, exhibited a relatively high survival rate of 81.5% throughout the three-month dry period post-harvest, whereas the remaining eight species had survival rates below 24.0% (0–23.1%). Four snail species, B. s. siamensis, Filopaludina martensi martensi, F. sumatrensis polygramma, and F. doliaris, were found infected with larval trematodes, with an overall prevalence of 8.46% (57/674). The larval trematodes identified were categorized into four types: echinostome metacercaria, Thapariella anastomusa metacercaria, unidentified metacercaria, and unidentified rediae. These findings demonstrate that trematode infections can persist in aestivating snails despite the challenging conditions during the dry season, emphasizing the potential of aestivating snails to act as vectors for trematode transmission in agricultural settings. This underscores the need for effective management strategies to mitigate the risks associated with trematode transmission.

Type
Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agrawal, SM (1958) Further observations on Thapariella anstastomusa Srivastava, 1953 (Trematoda: Thapariellidae). Indian Journal of Helminthology 10, 4045.Google Scholar
Agrawal, N, Pandey, KC and Kiran, GB (2002) Record of metacercaria of Thapareilla anastomusa Srivastava, 1958, from Bellamya bengalensis (L.). Indian Journal of Helminthology 20, 3538.Google Scholar
Bachtel, RZ, Rittenhouse, M, Sandland, GJ and Koop, JAH (2019) Infection patterns of trematodes across size classes of an invasive snail species using field and laboratory studies. Parasitology 146(4), 438444.CrossRefGoogle ScholarPubMed
Badger, LI and Oyerinde, JPO (1996) Schistosoma mansoni: Effect of aestivation on the intra-molluscan stages and the survival rate of infected Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 90(6), 617620.CrossRefGoogle ScholarPubMed
Brandt, RAM (1974) The non-marine aquatic mollusca of Thailand. Archiv fur Molluskenkunde 105, 1423.Google Scholar
Brewer, R (1994) The Science of Ecology, 2nd edn. New York: Saunders College.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 of Parasitology 16(5), 545552.CrossRefGoogle ScholarPubMed
Burch, JB and Lohachit, C (1983) Snail of medical importance in Thailand. Walkerana Transactions of the POETS Society 1, 395398.Google Scholar
Chai, JY, Sohn, WM, Na, BK and De, NV (2011) Echinostoma revolutum: metacercariae in Filopaludina snails from Nam Dinh Province, Vietnam, and adults from experimental hamsters. Korean Journal of Parasitology 49(4), 449455.CrossRefGoogle Scholar
Chai, JY, Murrell, KD and Lymbery, AJ (2005) Fish-borne parasitic zoonoses: Status and issues. International Journal of Parasitology 35(11–12), 12331254.CrossRefGoogle ScholarPubMed
Chai, JY, Shin, EH, Lee, SH and Rim, HJ (2009) Food-borne intestinal flukes in Southeast Asia. Korean Journal of Parasitology 47(Suppl), 69102.CrossRefGoogle Scholar
Chaichana, R and Sumpan, T (2015) Environmental tolerance of invasive golden apple snails (Pomacea canaliculata (Lamarck, 1822)) and Thai native apple snails (Pila scutate (Mousson, 1848)). Tropical Ecology 56(3), 347355.Google Scholar
Chaiyasaeng, M, Pechdee, P, Sereewong, C, Suwannatrai, A, Laha, T and Tesana, S (2019) Effects of aestivation on survival of Bithynia siamensis goniomphalos snails and the infection of Opisthorchis viverrini in the irrigation area of wet- and dry-season rice paddy. Acta Tropica 192(Suppl. 4), 5560.CrossRefGoogle ScholarPubMed
Chandiwana, SK, Taylor, P, Chimbari, M, Ndhlovu, P, Makura, O, Bradley, M and Gondo, P (1998) Control of schistosomiasis transmission in newly established smallholder irrigation schemes. Transactions of The Royal Society of Tropical Medicine and Hygiene 82(6), 874880.CrossRefGoogle Scholar
Chantima, K and Rika, C (2020) Snail-borne zoonotic trematodes in edible viviparid snails obtained from wet markets in Northern Thailand. Journal of Helminthology 94, E198.CrossRefGoogle ScholarPubMed
Chantima, K, Chai, JY and Wongsawad, C (2013) Echinostoma revolutum: Freshwater snails as the second intermediate hosts in Chiang Mai, Thailand. Korean Journal of Parasitology 51(2), 183189.CrossRefGoogle Scholar
Chantima, K, Suk-ueng, K and Kampan, M (2018a) Freshwater snail diversity in Mae Lao agricultural basin (Chiang Rai, Thailand) with a focus on larval trematode infections. Korean Journal of Parasitology 56(3), 247257.CrossRefGoogle Scholar
Chantima, K, Phromkhong, K, Sonyod, N and Chaichana, N (2018b) Occurrence of larval trematode in freshwater snail from Pa Ko Dam Sub-district, Mae Lao District, Chiang Rai Province. In McCormick, K, Mungthaisong, S, Khittasangka, M, Chomchalow, N, Walsh, JC and Lisec, A (eds), ASIAN Community Knowledge Networks for the Economy, Society, Culture, and Environmental Stability. Chiang Rai: Chiang Rai Rajabhat University, 8488.Google Scholar
Chantima, K, Lekpet, S, Butboonchoo, P and Wongsawad, C (2020) Diversity and abundance of gastropods in relation to physio-chemical parameters in rice paddies, Chiang Rai Province, Thailand. Agricultural and Natural Resources 54(3), 295300.Google Scholar
Chanyapeth, CH and Achawakhom, T (1998) Golden apple snails. In Proceedings of a Seminar on the Golden Apple Snail. Bangkok: Entomology and Zoology Division, Department of Agriculture, and the Entomology and Zoology Association of Thailand. 3.13.15.Google Scholar
Clarke, KR and Warwick, RM (1994) Change in Marine Community: An Approach to Statistical Analysis and Interpretation. Plymouth: Plymouth Marine Laboratory.Google Scholar
Eastham, J, Mpelasoka, F, Mainuddin, M, Ticehurst, C, Dyce, P, Hodgson, G, Ali, R and Kirby, M (2008) Mekong River Basin Water Resources Assessment: Impacts of Climate Change. Australia: CSIRO: Water for a Healthy Country National Research Flagship.Google Scholar
Fenwick, A, Webster, JP, Bosque-Oliva, E, Blair, L, Fleming, F, Zhang, Y, Garba, A, Stothard, J, Gabrielli, AF and Clements, A (2009) The Schistosomiasis Control Initiative (SCI): Rationale, development and implementation from 2002-2008. Parasitology 136(13), 17191730.CrossRefGoogle ScholarPubMed
Geo-Informatics and Space Technology Development Agency (Public Organization) (GISTDA) (2011) L05_AdminBoundary_Province_2011_50k_FGDS_Beta [Shapefile]. Bangkok: Geo-Informatics and Space Technology Development Agency (Public Organization).Google Scholar
Github (2024) World_Countries [Shapefile]. Available at https://github.com/prasertcbs/thailand_gis/tree/main/world_map Accessed 16 April 2024.Google Scholar
Hill, D, Fasham, M, Tucker, G, Shewry, M and Shaw, P (2005) Handbook of Biodiversity Methods: Survey, Evaluation and Monitoring. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Hillebrand, H (2008) Dominance. In Jorgensen, SE and Fath, B (eds), Encyclopedia of Ecology. Oxford: Elsevier, 938944.CrossRefGoogle Scholar
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(1), 5786.CrossRefGoogle Scholar
Kuris, A and Lafferty, KD (1994) Community structure: Larval trematodes in snail hosts. Annual Review of Ecology, Evolution, and Systematics 25, 189217.CrossRefGoogle Scholar
Lively, CM (2001) Trematode infection and the distribution and dynamics of parthenogenetic snail populations. Parasitology 123(7), 1926.CrossRefGoogle Scholar
Mard-arhin, N, Prawang, T and Wongsawad, C (2001) Helminths of freshwater animals from five provinces in Northern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 32(Suppl. 2), 206214.Google ScholarPubMed
Madsen, H and Hung, NM (2014) An overview of freshwater snails in Asia with main focus on Vietnam. Acta Tropica 140(Pt B), 105117.CrossRefGoogle ScholarPubMed
Min, F, Wang, J, Liu, X, Yuan, Y, Guo, Y, Zhu, K, Chai, Z, Zhang, Y and Li, S (2020) Environmental factors affecting freshwater snail intermediate hosts in Shenzhen and adjacent region, South China. Tropical Medicine and Infectious Disease 7(12), 426.CrossRefGoogle Scholar
Ng, TH, Annate, S, Jeratthitikul, E, Sutcharit, C, Limpanont, Y and Panha, S (2020) Disappearing apple snails (Caenogastropoda: Ampullariidae) of Thailand: A comprehensive update of their taxonomic status and distribution. Journal of Molluscan Studies 86(4), 290305.CrossRefGoogle Scholar
Osborne, TR and Wright, JC (2018) Seeking refuge in subsurface microhabitats during aestivation aids avoidance of lethally high temperature and desiccation in the snail Helminthoglypta tudiculata (Binney, 1843) (Pulmonata: Helminthoglyptidae). Journal of Molluscan Studies 84(2), 132140.CrossRefGoogle Scholar
Phalee, W, Phalee, A and Wongsawad, C (2018) New record of Thapariella anastomusa (Trematoda: Thapariellidae) metacercariae in Northern Thailand. Korean Journal of Parasitology 56(1), 4952.CrossRefGoogle ScholarPubMed
Prudhoe, S (1957) Trematoda: Exploration du Parc National de l’Upemba. Institut des Parcs Nationaux du Congo Belge 48, 128.Google Scholar
Pratumchart, K, Suwannatrai, K, Sereewong, C, Thinkhamrop, K, Chaiyos, J, Boonmars, T and Suwannatrai, AT (2019) Ecological niche model based on maximum entropy for mapping distribution of Bithynia siamensis goniomphalos, first intermediate host snail of Opisthorchis viverrini in Thailand. Acta Tropica 193(5), 183191.CrossRefGoogle ScholarPubMed
Qiu, J, Li, R, Zhu, H, Xia, J, Xiao, Y, Huang, D and Wang, Y (2020) The effect of ecological environmental changes and mollusciciding on snail intermediate host of Schistosoma in Qianjiang city of China from 1985 to 2015. Parasites Vectors 13(1), 397.CrossRefGoogle ScholarPubMed
Rai, DN and Pande, BP (1967) On the metacercariae of Thapariella anastomusa Srivastava, 1955. Indian Journal of Helminthology 19, 6469.Google Scholar
Rubaba, O, Chimbari, MJ and Mukaratirwa, S (2016) The role of snail aestivation in transmission of schistosomiasis in changing climatic conditions. African Journal of Aquatic Science 41(2), 143150.CrossRefGoogle Scholar
Schell, SC (1962) Parasitology Laboratory Manual. New York: Wiley.Google Scholar
Sparks, DL, Page, AL, Helmke, PA, Loeppert, RH, Soltanpour, PN, Tabatabai, MA, Johnston, CT and Sumner, ME (1996) Methods of Soil Analysis. Part 3 - Chemical Methods. Washington, DC: American Society of Agronomy, Inc.CrossRefGoogle Scholar
Sri-Aroon, P (2011) Freshwater Snails of Medical Importance in Thailand. Thailand: Mollusk Museum, Applied Malacology Center, Department of Social and Environmental Medicine, Mahidol University, 68.Google Scholar
Srivastava, NN (1953) On the morphology and systematic position of a new avian trematode Thapariella anastomusa n.g., n.sp., with a suggestion on the creation of a new family Thapariellidae. Indian Journal of Helminthology 5, 101108.Google Scholar
Suwannatrai, A, Suwannatrai, K, Haruay, S, Piratae, S, Thammasiri, C, Khampoosa, P, Kulsantiwong, J, Prasopdee, S, Tarbsripair, P, Suwanwerakamtorn, R, Sukchan, S, Boonmars, T, Malone, JB, Kearney, MT and Tesana, S (2011) Effect of soil surface salt on the density and distribution of the snail Bithynia siamensis goniomphalos in northeast Thailand. Geospatial Health 5(2), 183190.CrossRefGoogle ScholarPubMed
Upatham, ES, Sornmani, S, Kitikoon, V, Lohachit, C and Burch, JB (1983) Identification key for fresh-and brackish-water snails of Thailand. Malacological Review 16, 107136.Google Scholar
U.S. Salinity Laboratory Staff (1954) Diagnosis and Improvement of Saline and Alkaline Soils (Agriculture Handbook No. 60). Washington, DC: United States Government Printing Office.Google Scholar
Wang, LD, Chen, HG, Guo, JG, Zeng, XJ, Hong, XL, Xiong, JJ, Wu, XH, Wang, XH, Wang, LY and Xia, G (2009) A strategy to control transmission of Schistosoma japonicum in China. The New England Journal of Medicine 360(2), 121128.CrossRefGoogle ScholarPubMed
Wang, YC, Feng, CC, Sithithaworn, P, Feng, Y and Petney, TN (2011) How do snails meet fish? Landscape perspective needed to study parasite prevalence. Ecohealth 8(3), 258260.CrossRefGoogle ScholarPubMed
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(Pt B), 244252.CrossRefGoogle ScholarPubMed
Washington, HG (1984) Diversity, biotic and similarity indices. Water Research 18, 653694.CrossRefGoogle Scholar
Woodruff, DS and Upatham, ES (1993) Snail transmitted diseases of medical and veterinary importance in Thailand and the Mekong valley. Journal of Medical and Applied Malacology 4, 112.Google Scholar
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates. Kyoto: Keigaku Publishing.Google Scholar