Skip to main content Accessibility help
×
Home
Hostname: page-component-5c569c448b-8lphq Total loading time: 0.297 Render date: 2022-07-03T15:09:06.538Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Article contents

High diversity of trematode metacercariae that parasitize freshwater gastropods in Bangkok, Thailand, and their infective situations, morphologies and phylogenetic relationships

Published online by Cambridge University Press:  10 March 2022

Pichit Wiroonpan
Affiliation:
Animal Systematics and Ecology Speciality Research Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
Thapana Chontananarth
Affiliation:
Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University, Bangkok, Thailand Center of Excellence in Animal, Plant and Parasitic Biotechnology, Srinakharinwirot University, Bangkok, Thailand
Jong-Yil Chai
Affiliation:
Institute of Parasitic Diseases, Korea Association of Health Promotion (KAHP), Seoul 07649, Korea
Watchariya Purivirojkul*
Affiliation:
Animal Systematics and Ecology Speciality Research Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
*
Author for correspondence: Watchariya Purivirojkul, E-mail: fsciwyp@ku.ac.th

Abstract

We investigated diversity, infective situations, morphological features and phylogenetic relationships of the metacercariae in freshwater snails from Bangkok between March 2018 and February 2020. Crushing and dissection techniques were performed to explore the metacercariae in the snail hosts. Polymerase chain reaction was implemented to amplify the internal transcribed spacer 1 (ITS1), 5.8S ribosomal DNA and ITS2 regions of metacercarial DNA. A total of 3173 of all 21 707 snails showed infections with metacercariae, representing a relatively high infective prevalence (14.62%) compared to earlier research. All infected snails belonged to 14 species/subspecies. A group of viviparid snails exhibited the highest metacercarial infections (26.10–82.18%). We found metacercariae with seven morphological groups. Five of them can be stated as new records of the metacercariae in Thailand, indicating a broader spectrum of larval trematode diversity. Our phylogenetic assessments established that five of the seven morphological groups can be molecularly classified into different taxonomic levels of digenean trematodes. Echinostome A metacercariae revealed the highest infective prevalence (7.15%), and their sequence data were conspecific with a sequence of Echinostoma mekongki, which is a human intestinal fluke; this finding denotes the distribution and suggests epidemiological surveillance of this medically important fluke in Bangkok and adjacent areas. However, two groups of Opisthorchiata-like and renicolid metacercariae remain unclear as to their narrow taxonomic status, although their molecular properties were considered. For more understanding about trematode transmissions in ecosystems, both physical and biological factors may be further analysed to consider the factors that relate to and contribute to trematode infections.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. 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

Abramoff, MD, Magalhaes, PJ and Ram, SJ (2004) Image processing with ImageJ. Biophotonics International 11, 3642.Google Scholar
Anucherngchai, S and Chontananarth, T (2016) The prevalence and morphological characteristic of trematodes infection in freshwater snails, Filopaludina in Khlong Toey market, Bangkok, Thailand. In The 4th Academic Science and Technology Conference 2016. Bangkok, Thailand: Thai traditional medicine college and faculty of agricultural technology, Rajamangala University of Technology Thanyaburi, pp. 92–97.Google Scholar
Apiraksena, K, Namchote, S, Komsuwan, J, Dechraksa, W, Tharapoom, K, Veeravechsukij, N, Glaubrecht, M and Krailas, D (2020) Survey of Stenomelania Fisher, 1885 (Cerithioidea, Thiaridae): the potential of trematode infections in a newly-recorded snail genus at the coast of Andaman Sea, South Thailand. Zoosystematics and Evolution 96, 807819.CrossRefGoogle Scholar
Besprozvannykh, VV, Tatonova, YV and Shumenko, PG (2019) Life cycle, morphology of developmental stages of Metorchis ussuriensis sp. nov. (Trematoda: Opisthorchiidae), and phylogenetic relationships with other opisthorchiids. Journal of Zoological Systematics and Evolutionary Research 57, 2440.CrossRefGoogle Scholar
Bouchet, P, Rocroi, J-P, Fryda, J, Hausdorf, B, Ponder, W, Valdes, A and Warén, A (2005) Classification and nomenclator of gastropod families. Malacologia 47, 1368.Google Scholar
Brandt, RAM (1974) The non-marine aquatic mollusca of Thailand. Archiv für Molluskenkunde 105, 1423.Google Scholar
Bray, R, Gibson, D and Jones, A (2008) Keys to the Trematoda, vol. 3. London, UK: CABI Publishing, Wallingford & The Natural History Museum.Google Scholar
Bunchom, N, Pilap, W, Suksavate, W, Vaisusuk, K, Suganuma, N, Agatsuma, T, Petney, TN and Saijuntha, W (2020) Trematode infection in freshwater snails from Maha Sarakham Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 51, 518527.Google Scholar
Butboonchoo, P, Wongsawad, C, Wongsawad, P and Chai, J-Y (2020) Morphology and molecular identification of Echinostoma revolutum and Echinostoma macrorchis in freshwater snails and experimental hamsters in upper northern Thailand. The Korean Journal of Parasitology 58, 499511.CrossRefGoogle ScholarPubMed
Caron, Y, Rondelaud, D and Losson, B (2008) The detection and quantification of a digenean infection in the snail host with special emphasis on Fasciola sp. Parasitology Research 103, 735.CrossRefGoogle ScholarPubMed
Catalano, S, Symeou, A, Marsh, KJ, Borlase, A, Léger, E, Fall, CB, Sène, M, Diouf, ND, Ianniello, D, Cringoli, G, Rinaldi, L, , K and Webster, JP (2019) Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasites & Vectors 12, 439.CrossRefGoogle ScholarPubMed
Chai, J-Y, Sohn, W-M, Na, B-K and Van De, N (2011) Echinostoma revolutum: Metacercariae in Filopaludina snails from Nam Dinh Province, Vietnam, and adults from experimental hamsters. The Korean Journal of Parasitology 49, 449455.CrossRefGoogle Scholar
Chai, J-Y, Cho, J, Chang, T, Jung, B-K and Sohn, W-M (2020) Taxonomy of Echinostoma revolutum and 37-collar-spined Echinostoma spp.: a historical review. The Korean Journal of Parasitology 58, 343371.CrossRefGoogle ScholarPubMed
Chai, J-Y, Sohn, W-M, Cho, J, Jung, B-K, Chang, T, Lee, KH, Khieu, V and Huy, R (2021) Echinostoma mekongi: discovery of its metacercarial stage in snails, Filopaludina martensi cambodjensis, in Pursat Province, Cambodia. The Korean Journal of Parasitology 59, 4753.CrossRefGoogle ScholarPubMed
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, J-Y and Wongsawad, C (2013) Echinostoma revolutum: freshwater snails as the second intermediate hosts in Chiang Mai, Thailand. The Korean Journal of Parasitology 51, 183189.CrossRefGoogle ScholarPubMed
Chantima, K, Suk-Ueng, K and Kampan, M (2018) Freshwater snail diversity in Mae Lao agricultural basin (Chiang Rai, Thailand) with a focus on larval trematode infections. The Korean Journal of Parasitology 56, 247257.CrossRefGoogle Scholar
Charoensuk, L, Ribas, A, Chedtabud, K and Prakobwong, S (2022) Infection rate of Opisthorchis viverrini metacercariae in cyprinoid fish from the markets and its association to human opisthorchiasis in the local community in the Northeast Thailand. Acta Tropica 225, 106216.CrossRefGoogle ScholarPubMed
Cheatum, EP (1934) Limnological investigations on respiration, annual migratory cycle, and other related phenomena in fresh-water pulmonate snails. Transactions of the American Microscopical Society 53, 348407.CrossRefGoogle Scholar
Chérnin, E (1967) Occurrence' of metacercariae within ehinostome rediae transplanted into Australorbis glabratus. Journal of Parasitology 53, 219.CrossRefGoogle Scholar
Cho, J, Jung, B-K, Chang, T, Sohn, W-M, Sinuon, M and Chai, J-Y (2020) Echinostoma mekongi n. sp. (Digenea: Echinostomatidae) from Riparian People along the Mekong River in Cambodia. The Korean Journal of Parasitology 58, 431443.CrossRefGoogle Scholar
Chomchoei, N, Wongsawad, C and Nantarat, N (2018) Investigation of cryptic diversity and occurrence of echinostome metacercariae infection in Anentome helena (von dem Busch, 1847). Asian Pacific Journal of Tropical Medicine 11, 590596.Google Scholar
Chontananarth, T and Wongsawad, C (2017) The pleurophocercous cercariae infection in snail Family Thiaridae Grey, 1847 Northern, Thailand. Asian Pacific Journal of Tropical Disease 7, 205210.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dawnay, N, Ogden, R, McEwing, R, Carvalho, GR and Thorpe, RS (2007) Validation of the barcoding gene COI for use in forensic genetic species identification. Forensic Science International 173, 16.CrossRefGoogle ScholarPubMed
Dechruksa, W, Krailas, D, Ukong, S, Inkapatanakul, W and Koonchornboon, T (2007) Trematode infections of the freshwater snail family Thiaridae in the Khek River, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 38, 10161028.Google ScholarPubMed
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611620.CrossRefGoogle ScholarPubMed
Devkota, R, Budha, P and Gupta, R (2011) Trematode cercariae infections in freshwater snails of Chitwan District, central Nepal. Himalayan Journal of Sciences 7, 914.CrossRefGoogle Scholar
Diaz, JI and Cremonte, F (2010) Development from metacercaria to adult of a new species of Maritrema (Digenea: Microphallidae) parasitic in the kelp gull, Larus dominicanus, from the Patagonian coast, Argentina. Journal of Parasitology 96, 740745.CrossRefGoogle ScholarPubMed
Duan, Y, Al-Jubury, A, Kania, PW and Buchmann, K (2021) Trematode diversity reflecting the community structure of Danish freshwater systems: molecular clues. Parasites & Vectors 14, 43.CrossRefGoogle ScholarPubMed
Duflot, M, Setbon, T, Midelet, G, Brauge, T and Gay, M (2021) A review of molecular identification tools for the opisthorchioidea. Journal of Microbiological Methods 187, 106258.CrossRefGoogle ScholarPubMed
Dzikowski, R, Levy, MG, Poore, MF, Flowers, JR and Paperna, I (2004) Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Diseases of Aquatic Organisms 59, 3541.CrossRefGoogle ScholarPubMed
Esch, GW and Fernandez, JC (1994) Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. The American Midland Naturalist 131, 209237.CrossRefGoogle Scholar
Esteban, J, Toledo, R, Sánchez, L and Muñoz-Antolí, C (1997) Life-cycle of Euparyphium albuferensis n. sp. (Trematoda: Echinostomatidae) from rats in Spain. Systematic Parasitology 38, 211219.CrossRefGoogle Scholar
Faltýnková, A, Našincová, V and Kablásková, L (2007) Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14, 3951.CrossRefGoogle ScholarPubMed
Faltýnková, A, Našincová, V and Kablásková, L (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Systematic Parasitology 69, 155178.CrossRefGoogle ScholarPubMed
Fretter, V and Graham, A (1962) British Prosobranch Molluscs: Their Functional Anatomy and Ecology. London: Ray Society.Google Scholar
Gilardoni, C, Etchegoin, J, Diaz, JI, Ituarte, C and Cremonte, F (2011) A survey of larval digeneans in the commonest intertidal snails from Northern Patagonian coast, Argentina. Acta Parasitologica 56, 163.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Haas, W, Beran, B and Loy, C (2008) Selection of the host's habitat by cercariae: from laboratory experiments to the field. Journal of Parasitology 94, 12331238.CrossRefGoogle ScholarPubMed
Hirano, T, Saito, T, Tsunamoto, Y, Koseki, J, Prozorova, L, Do, VT, Matsuoka, K, Nakai, K, Suyama, Y and Chiba, S (2019) Role of ancient lakes in genetic and phenotypic diversification of freshwater snails. Molecular Ecology 28, 50325051.CrossRefGoogle ScholarPubMed
Huang, X and Madan, A (1999) CAP3: a DNA sequence assembly program. Genome Research 9, 868877.CrossRefGoogle ScholarPubMed
Jones, A, Bray, R and Gibson, D (2005) Keys to the Trematoda, vol. 2. London, UK: CABI Publishing, Wallingford & The Natural History Museum.CrossRefGoogle Scholar
Jousson, O, Bartoli, P and Pawlowski, J (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology 29, 18531858.CrossRefGoogle Scholar
Keane, RM and Crawley, MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164170.CrossRefGoogle Scholar
Kostadinova, A and Gibson, DI (2002) Isthmiophora Lühe, 1909 and Euparyphium Dietz, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Systematic Parasitology 52, 205217.CrossRefGoogle ScholarPubMed
Kostadinova, A, Herniou, EA, Barrett, J and Littlewood, DT (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology 54, 159176.CrossRefGoogle ScholarPubMed
Krailas, D, Janecharat, T, Ukong, S, Junhom, W, Klamkhlai, S, Notesiri, N and Ratanathai, P (2004) Trematode infection rates of fish from a wastewater treatment factory polishing pond and a canal in Phuket, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 35, 291295.Google 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, 5786.CrossRefGoogle Scholar
Krailas, D, Veeravechsukij, N, Chuanprasit, C, Boonmekam, D and Namchote, S (2016) Prevalence of fish-borne trematodes of the family Heterophyidae at Pasak Cholasid Reservoir, Thailand. Acta Tropica 156, 7986.CrossRefGoogle ScholarPubMed
Kudlai, O, Kostadinova, A, Pulis, EE and Tkach, VV (2015) A new species of Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae) from the double-crested cormorant Phalacrocorax auritus (Lesson) (Aves: Phalacrocoracidae) in North America. Systematic Parasitology 90, 221230.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Kumchoo, K, Wongsawad, C, Chai, JY, Vanittanakom, P and Rojanapaibul, A (2005) High prevalence of Haplorchis taichui metacercariae in cyprinoid fish from Chiang Mai Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 36, 451455.Google Scholar
Loy, C, Motzel, W and Haas, W (2001) Photo- and geo-orientation by echinostome cercariae results in habitat selection. Journal of Parasitology 87, 505509.CrossRefGoogle ScholarPubMed
Mard-arhin, N, Prawang, T and Wongsawad, C (2001) Helminths of freshwater animals from five provinces in northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 32(Suppl. 2), 206209.Google ScholarPubMed
Mekong River Commission (2006) Identification of Freshwater Invertebrates of the Mekong River and its Tributaries. Vientiane: Mekong River Commission.Google Scholar
Miller, TL, Downie, AJ and Cribb, TH (2009) Morphological disparity despite genetic similarity; new species of Lobosorchis Miller & Cribb, 2005 (Digenea: Cryptogonimidae) from the Great Barrier Reef and the Maldives. Zootaxa 1992, 3752.CrossRefGoogle Scholar
Miller, TL, Adlard, RD, Bray, RA, Justine, J-L and Cribb, TH (2010) Cryptic species of Euryakaina n. g. (Digenea: Cryptogonimidae) from sympatric lutjanids in the Indo-West Pacific. Systematic Parasitology 77, 185204.CrossRefGoogle Scholar
Morgan, JAT and Blair, D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111, 609615.CrossRefGoogle ScholarPubMed
Namsanor, J, Kiatsopit, N, Laha, T, Andrews, RH, Petney, TN and Sithithaworn, P (2020) Infection dynamics of Opisthorchis viverrini metacercariae in cyprinid fishes from two endemic areas in Thailand and Lao PDR. The American Journal of Tropical Medicine and Hygiene 102, 110116.CrossRefGoogle ScholarPubMed
Nasir, P (1962) Further observations on the life cycle of Echinostoma nudicaudatum Nasir, 1960 (Echinostomatidae: Trematoda). Proceedings of the Helminthological Society of Washington 29, 115127.Google Scholar
Ng, TH, Limpanont, Y, Chusongsang, Y, Chusongsang, P and Panha, S (2018) Correcting misidentifications and first confirmation of the globally-invasive Physa acuta Draparnaud, 1805 (Gastropoda: Physidae) in Thailand and Laos. BioInvasions Records 7, 1519.CrossRefGoogle Scholar
Nithiuthai, S, Suwansaksri, J, Wiwanitkit, V and Chaengphukeaw, P (2002) A survey of metacercariae in cyprinoid fish in Nakhon Ratchasima, northeast Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 33(Suppl. 3), 103105.Google ScholarPubMed
Noikong, W and Wongsawad, C (2014) Epidemiology and molecular genotyping of echinostome metacercariae in Filopaludina snails in Lamphun Province, Thailand. Asian Pacific Journal of Tropical Medicine 7, 2629.CrossRefGoogle ScholarPubMed
Noikong, W, Wongsawad, C, Chai, J-Y, Saenphet, S and Trudgett, A (2014) Molecular analysis of echinostome metacercariae from their second intermediate host found in a localised geographic region reveals genetic heterogeneity and possible cryptic speciation. PLOS Neglected Tropical Diseases 8, e2778.CrossRefGoogle Scholar
Olivier, L and Schneiderman, M (1956) A method for estimating the density of aquatic snail populations. Experimental Parasitology 5, 109117.CrossRefGoogle ScholarPubMed
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle Scholar
Patarwut, L, Chontananarth, T, Chai, J-Y and Purivirojkul, W (2020) Infections of digenetic trematode metacercariae in Wrestling Halfbeak, Dermogenys pusilla from Bangkok Metropolitan Region in Thailand. The Korean Journal of Parasitology 58, 2735.CrossRefGoogle ScholarPubMed
Phalee, W, Phalee, A and Wongsawad, C (2018) New record of Thapariella anastomusa (Trematoda: Thapariellidae) Metacercariae in Northern Thailand. The Korean Journal of Parasitology 56, 4952.CrossRefGoogle ScholarPubMed
Pinlaor, S, Onsurathum, S, Boonmars, T, Pinlaor, P, Hongsrichan, N, Chaidee, A, Haonon, O, Limviroj, W, Tesana, S, Kaewkes, S and Sithithaworn, P (2013) Distribution and abundance of Opisthorchis viverrini metacercariae in cyprinid fish in Northeastern Thailand. The Korean Journal of Parasitology 51, 703710.CrossRefGoogle ScholarPubMed
Pinto, HA and De Melo, AL (2011) A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa 2799, 1528.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Schell, SC (1970) How to Know the Trematodes. Dubuque, IA: Wm. C. Brown Company.Google Scholar
Sewell, RB (1922) Cercariae indica. The Indian Journal of Medical Research 10, 1370.Google Scholar
Sohn, W-M and Na, B-K (2017) Echinostoma macrorchis (Digenea: Echinostomatidae): Metacercariae in Cipangopaludina chinensis malleata snails and adults from experimental rats in Korea. The Korean Journal of Parasitology 55, 541548.CrossRefGoogle ScholarPubMed
Sohn, W-M, Chai, J-Y, Na, B-K, Yong, T-S, Eom, KS, Park, H, Min, D-Y and Rim, H-J (2013) Echinostoma macrorchis in Lao PDR: Metacercariae in Cipangopaludina snails and adults from experimentally infected animals. The Korean Journal of Parasitology 51, 191196.CrossRefGoogle ScholarPubMed
Sohn, W-M, Yong, T-S, Eom, KS, Sinuon, M, Jeoung, H-G and Chai, J-Y (2017) Artyfechinostomum malayanum: Metacercariae encysted in Pila sp. snails purchased from Phnom Penh, Cambodia. The Korean Journal of Parasitology 55, 341345.CrossRefGoogle ScholarPubMed
Sohn, W-M, Na, B-K, Lee, D, Eom, KS, Yong, T-S, Chai, J-Y and Min, D-Y (2019) Echinostoma macrorchis metacercariae in Cipangopaludina chinensis malleata from Xiengkhuang Province, Lao PDR and morphologies of adults from experimental animals. The Korean Journal of Parasitology 57, 657664.CrossRefGoogle ScholarPubMed
Sokolov, SG, Atopkin, DM and Urabe, M (2019) Redescription and supplementary molecular characteristics of Aspidogaster ijimai Kawamura, 1915 (Trematoda, Aspidogastrea, Aspidogastridae), a parasite of Cyprinus carpio Linnaeus, 1758 s. lato (Actinopterygii) and freshwater bivalves in East Asia. Parasitology International 71, 167176.CrossRefGoogle ScholarPubMed
Sorensen, RE, Curtis, J and Minchella, DJ (1998) Intraspecific variation in the rDNA its loci of 37-collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. Journal of Parasitology 84, 992997.CrossRefGoogle ScholarPubMed
Suanyuk, N, Mankhakhet, S, Soliman, H, Saleh, M and El-Matbouli, M (2013) Euclinostomum heterostomum infection in guppies Poecilia reticulata cultured in southern Thailand. Diseases of Aquatic Organisms 104, 121127.CrossRefGoogle ScholarPubMed
Tatonova, YV, Besprozvannykh, VV, Katugina, LO, Solodovnik, DA and Nguyen, HM (2020 a) Morphological and molecular data for highly pathogenic avian parasite Erschoviorchis anuiensis sp. n. and phylogenetic relationships within the Opisthorchiidae (Trematoda). Parasitology International 75, 102055.CrossRefGoogle Scholar
Tatonova, YV, Izrailskaia, AV and Besprozvannykh, VV (2020 b) Stephanoprora amurensis sp. nov., Echinochasmus milvi Yamaguti, 1939 and E. suifunensis Besprozvannykh, 1991 from the Russian southern Far East and their phylogenetic relationships within the Echinochasmidae Odhner 1910. Parasitology 147, 14691479.CrossRefGoogle Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle ScholarPubMed
Toledo, R, Muñoz-Antoli, C and Esteban, J (1999) Encystment sites of metacercariae of Hypoderaeum conoideum (Trematoda: Echinostomatidae) in freshwater gastropods. Folia Parasitologica 46, 5758.Google Scholar
Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ and Kuris, AM (2003) Introduced species and their missing parasites. Nature 421, 628630.CrossRefGoogle ScholarPubMed
Upatham, E, Sormani, S, Kitikoon, V, Lohachit, C and Burch, J (1983) Identification key for the fresh and brackish-water snails of Thailand. Malacological Review 16, 107132.Google Scholar
Upatham, S, Kruatrachue, M, Chitramwong, Y and Chantateme, S (1995) Malacology. Bangkok: Sukdisopakarnpim.Google Scholar
VanAcker, MC, Lambert, MR, Schmitz, OJ and Skelly, DK (2019) Suburbanization increases echinostome infection in green frogs and snails. EcoHealth 16, 235247.CrossRefGoogle ScholarPubMed
Veeravechsukij, N, Namchote, S, Neiber, MT, Glaubrecht, M and Krailas, D (2018) Exploring the evolutionary potential of parasites: Larval stages of pathogen digenic trematodes in their thiarid snail host Tarebia granifera in Thailand. Zoosystematics and Evolution 94, 425460.CrossRefGoogle Scholar
Wetzel, EJ and Shreve, EW (2003) The influence of habitat on the distribution and abundance of metacercariae of Macravestibulum obtusicaudum (Pronocephalidae) in a small Indiana stream. Journal of Parasitology 89, 10881090.CrossRefGoogle Scholar
Wiroonpan, P and Purivirojkul, W (2018) Trematode infection of the edible pond snail (Filopaludina martensi) from Kasetsart University, Thailand. In The 18th Agricultural Conference. Faculty of Agriculture, Khon Kaen University, vol. 46, pp. 267–272.Google Scholar
Wiroonpan, P and Purivirojkul, W (2021) A survey of Thapariella anastomusa (Trematoda: Thapariellidae) metacercariae in edible viviparid snails from Bangkok, Thailand. In Proceedings of the 59th Kasetsart University Annual Conference. Bangkok: Kasetsart University Research and Development Institute, Kasetsart University, pp. 525–535.Google Scholar
Wiroonpan, P, Chontananarth, T and Purivirojkul, W (2021) Cercarial trematodes in freshwater snails from Bangkok, Thailand: prevalence, morphological and molecular studies and human parasite perspective. Parasitology 148, 366383.CrossRefGoogle ScholarPubMed
Wongsawad, C, Rojanapaibul, A, Mhad-arehin, N, Pachanawan, A, Marayong, T, Suwattanacoupt, S, Rojtinnakorn, J, Wongsawad, P, Kumchoo, K and Nichapu, A (2000) Metacercaria from freshwater fishes of Mae Sa stream, Chiang Mai, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 31(Suppl. 1), 5457.Google ScholarPubMed
Wongsawad, C, Intamong, J and Chantima, K (2017) Surface morphology of Echinostoma revolutum (Digenea: Echinostomatidae): Excysted metacercariae. Microscopy and Microanalysis Research 30, 2427.Google Scholar
Yoder, HR and Coggins, JR (1998) Larval trematode assemblages in the snail Lymnaea stagnalis from southeastern Wisconsin. The Journal of Parasitology 84, 259268.CrossRefGoogle ScholarPubMed
Yurlova, NI, Vodyanitskaya, SN, Serbina, EA, Biserkov, VY, Georgiev, BB and Chipev, NH (2006) Temporal variation in prevalence and abundance of metacercariae in the pulmonate snail lymnaea stagnalis in Chany Lake, West Siberia, Russia: Long-term patterns and environmental covariates. Journal of Parasitology 92, 249259.CrossRefGoogle ScholarPubMed

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

High diversity of trematode metacercariae that parasitize freshwater gastropods in Bangkok, Thailand, and their infective situations, morphologies and phylogenetic relationships
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

High diversity of trematode metacercariae that parasitize freshwater gastropods in Bangkok, Thailand, and their infective situations, morphologies and phylogenetic relationships
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

High diversity of trematode metacercariae that parasitize freshwater gastropods in Bangkok, Thailand, and their infective situations, morphologies and phylogenetic relationships
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *