Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Morphological and molecular characteristics of Paralecithodendrium longiforme (Digenea: Lecithodendriidae) adults and cercariae from Chinese pipistrelle bats and viviparid snails in Thailand

  • Thitichai Arttra (Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Pheravut Wongsawad (Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Chalobol Wongsawad (Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Nattawadee Nantarat (Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Preeyaporn Butboonchoo (Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Jong-Yil Chai (Department of Tropical Medicine and Parasitology, Seoul National University College of Medicine)
  • Received : 2023.10.27
  • Accepted : 2023.12.28
  • Published : 2024.02.29
Download PDF
⟨ Previous Next ⟩

Abstract

This study aimed to describe the morphological and molecular characteristics of Paralecithodendrium longiforme (Digenea: Lecithodendriidae) adults and cercariae isolated in Thailand. Adult flukes were isolated from the Chinese pipistrelle bat (Hypsugo sp.), and cercariae were detected in the viviparid snail (Filopaludina martensi martensi) from Chiang Mai province. The morphological characteristics were observed and described using conventional methods, and the molecular characteristics with internal transcribed spacer 2 (ITS2) and 28S rDNA gene sequences. The adult flukes were fusiform, 0.84-0.98 mm in length, and 0.37-0.49 mm in width, and were distinguishable from other species by the presence of longitudinal uterine coils. The cercariae were nonvirgulate xiphidiocercariae, with the oral sucker bigger than the acetabulum, the tail without fin fold, a body size of 117.5-138.3×48.3-52.2 ㎛, and a tail size of 100.7-103.7×15.0-18.9 ㎛. Molecular studies revealed that the adults and cercariae shared 99.3% (ITS2) and 99.6% (28S rDNA) homology with each other. They were phylogenetically close to P. longiforme with an identity of 94.5% for ITS2 and 98.7% for 28S rDNA. This study provides new information on the natural definitive host and first intermediate host of P. longiforme in Thailand. The discovery of its cercarial stage in Filopaludina snails highlights the importance of monitoring the associated second intermediate host and prevention and control of this potentially zoonotic trematode.

Keywords

Acknowledgement

This research was supported by Chiang Mai University. The authors acknowledge the Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University for their facilities and laboratory processing.

References

  1. Lotz JM, Font WF. Family lecithodendriidae luhe. In Bray RA, Jones A, Gibson DI eds. Keys to the Trematoda Volume 3. CAB International, London, UK. 2008. pp 527-536.
  2. Manning GS, Lertprasert P. Studies on the life cycle of Phaneropsolus bonnei and Prosthodendrium molenkampi in thailand. Ann Trop Med Parasit 1973;67(3):361-365. https://doi.org/10.1080/00034983.1973.11686899
  3. Vasuteprungson M, Kliks M. The helminth fauna of north thailand. II. Parasites of aves and chiroptera. J Assoc Med Sci 2016;6(3):161. https://he01.tcithaijo.org/index.php/bulletinAMS/article/view/60769
  4. Chai JY. Lecithodendriid-like flukes. In Chai JY ed. Human Intestinal Flukes: From Discovery to Treatment and Control. Springer Nature, Dordrecht, The Netherlands. 2019. pp 443-461.
  5. Bhalerao GD. The intestinal parasites of the bat (Nyctinomus plicatus) with a list of the trematodes hitherto recorded from Burma. J Burma Res Soc 1926;15:181-195.
  6. Lotz JM, Palmieri JR. Lecithodendriidae (Trematoda) from Taphozous melanopogon (Chiroptera) in Perlis, Malaysia. Proc Helminthol Soc Wash 1985;52(1):21-29. https://api.semanticscholar.org/CorpusID:88832522
  7. Tkach V, Pawlowski J, Mariaux J. Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 2000;30(1):83-93. https://doi.org/10.1016/S0020-7519(99)00163-0
  8. Horvat Z, Cabrilo B, Paunovic M, Karapandza B, Jovanovic J, et al. Gastrointestinal digeneans (Platyhelminthes: Trematoda) of horseshoe and vesper bats (Chiroptera: Rhinolophidae and Vespertilionidae) in Serbia. Helminthologia 2017;54(1):17-25. https://doi.org/10.1515/helm-2017-0009
  9. Eduardo SL. First report of Plagiorchis vespertilionis (Muller, 1780), a known zoonotic fluke, with notes on two species of Paralecithodendrium (Platyhelminthes: Trematoda) from Myotis sp. and Miniopterus sp. (Mammalia: Chiroptera) in the Philippines. Philip J Vet Med 2021;58:70-77. https://ovcre.uplb.edu.ph/journals-uplb/index.php/PJVM/article/view/598
  10. Azim MA. On the life history of Lecithodendrium pyramidum looss, 1896 and its development from a xiphiodiocercaria, C. pyramidum sp. nov. from Melania tuberculata. Ann Trop Med Parasitol 1936;30:351-328. https://doi.org/10.1080/00034983.1936.11684943
  11. Knight RA, Pratt I. The life-histories of Allassogonoporus vespertilionis Macy and Acanthatrium oregonense Macy (Trematoda: Lecithodendriidae). J Parasitol 1955;41(3):248-255. https://doi.org/10.2307/3274199
  12. Etges FJ. On the life history of Prosthodendrium (Acanthatrium) anaplocami n. sp. (Trematoda: Lecithodendriidae). J Parasitol 1960;46:235-240. https://doi.org/10.2307/3275180
  13. Besprozvannykh VV. Life cycle of Prosthodendrium dollfusi sp. n. and Acanthatrium ovatum (Tematoda: Lecithodendriidae) in the south of the far east of the USSR. Parazitologiya 1990;24:431-439.
  14. Wongsawad C, Nantarat N, Wongsawad P. Phylogenetic analysis reveals cryptic species diversity within minute intestinal fluke, Stellantchasmus falcatus onji and nishio, 1916 (Trematoda, Heterophyidae). Asian Pac J Trop Med 2017;10(2):165-170. https://doi.org/10.1016/j.apjtm.2017.01.016
  15. Butboonchoo P, Wongsawad C, Wongsawad P, Chai JY. Morphology and molecular identification of Echinostoma revolutum and Echinostoma macrorchis in freshwater snails and experimental hamsters in upper northern Thailand. Parasites Hosts Dis 2020;58(5):499-511. https://doi.org/10.3347/kjp.2020.58.5.499
  16. Kudlai O, Stunzenas V, Tkach V. The taxonomic identity and phylogenetic relationships of Cercaria pugnax and C. helvetica XII (Digenea: Lecitho-dendriidae) based on morphological and molecular data. Folia Parasitol (Praha) 2015;62. http://doi.org/10.14411/fp.2015.003
  17. Enabulele EE, Lawton SP, Walker AJ, Kirk RS. Molecular and morphological characterization of the cercariae of Lecithodendrium linstowi (Dollfus, 1931), a tremaatode of bats, and incrimination of the first intermediate snail host, Radix balthica. Parasitology 2018;145(3):307-312. http://doi.org/10.1017/S0031182017001640
  18. Dunghungzin C, Chontananarth T. Prevalence of cercarial infections in freshwater snails and morphological and molecular identification and phylogenetic trends of trematodes. Asian Pac J Trop Med 2020;13(10):439-447. http://doi.org/10.4103/1995-7645.291037
  19. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: margolis et al. revisited. J Parasitol 1997;83(4):575-583. https://doi.org/10.2307/3284227
  20. Noikong W, Wongsawad C, Chai JY, Saenphet S, Trudgett A. Molecular analysis of echinostome metacercariae from their second intermediate host found in a localised geographic region reveals genetic heterogeneity and possible cryptic speciation. PLoS Negl Trop Dis 2014;8(4):e2778. https://doi.org/10.1371/journal.pntd.0002778
  21. Bowles J, Blair D, McManus DP. A molecular phylogeny of the human schistosomes. Mol Phylogenet Evol 1995;4(2):103-109. https://doi.org/10.1006/mpev.1995.1011
  22. Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DT. Phylogeny and classification of the digenea (Platyhelminthes: Trematoda). Int J Parasitol 2003;33(7):733-755. https://doi.org/10.1016/S0020-7519(03)00049-3
  23. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018;35(6):1547-1549. https://doi.org/10.1093/molbev/msy096
  24. Morrison DA. Phylogenetic analyses of parasites in the new millennium. Adv Parasitol 2006;63:1-124. https://doi.org/10.1016/S0065-308X(06)63001-7
  25. San Mauro D, Agorreta A. Molecular systematics: a synthesis of the common methods and the state of knowledge. Cell Mol Biol Lett 2010;15(2):311-341. https://doi.org/10.2478/s11658-010-0010-8
  26. Saoud MF, Ramadan MM. Studies on digenetic trematodes of the genus Prosthodendrium dollfus, 1931 from some egyptian bats. 2. Trematodes of the subgenus Paralecithodendrium Odhner, 1911. Folia Parasitol (Praha) 1977;24(4):317-321.
  27. Matskasi I. The systematico-faunistical survey of the trematode fauna of hungarian bats I. Ann Hist-Nat Mus Natn Hung 1967;59:217-238.
  28. Pande BP. Contribution to the digenetic trematodes of the microchiroptera of northern India. Part 2. Studies on the genus Lecithodendrium Looss, 1896. Proc Acad Sci 1935;5:86-98.
  29. Dubois G. Les Trematodes de Chiropteres de la collection villy aellen. Etude suivie d'une revision du sousgenre Prosthodendrium Dollfus 1937 (Lecithodendriinae Luhe). Rev Suisse Zool 1955;62:469-506. https://doi.org/10.5962/bhl.part.75442
  30. Luhe M. Die Susswasserfauna deutschlands. Eine Exkursionsfauna. In Brauer A ed, 17 Parasitische Plattwurmer (1: Trematodes). Gustav Fischer. Jena, Germany. 1909.
  31. Kruidenier FJ. The formation and function of mucoids in virgulate cercariae, including a study of the virgula organ. Am Midl Nat 1951;46(3):660-683. https://doi.org/10.2307/2421810
  32. Lopes AS, Pulido-Murillo EA, Lopez-Hernandez D, Melo ALd, Pinto HA. First report of Melanoides tuberculata (Mollusca: Thiaridae) harboring a xiphidiocercaria in Brazil: a new parasite introduced in the americas? Parasitol Int 2021;82:102284. https://doi.org/10.1016/j.parint.2021.102284
  33. Tkach VV, Littlewood DT, Olson PD, Kinsella JM, Swiderski Z. Molecular phylogenetic analysis of the microphalloidea ward, 1901 (Trematoda: Digenea). Syst Parasitol 2003;56(1):1-15. https://doi.org/10.1023/A:1025546001611