Abstract
The diversity of fish parasites from freshwater fishes collected from the Nong Han wetland (Udon Thani Province, Thailand) was studied by visually examining 22 freshwater fish species (253 samples) from 19 genera for external and internal parasites. A majority of fishes in the Nong Han wetland were infected by parasites (75.89%). Twenty fish species (75.89%) were infected with a total of 29 species of parasites. These included 9 species of monogeneans, 5 crustaceans, 5 acanthocephalans, 4 nematodes, 3 digeneans, and 3 species of cestodes. Cyclocheilichthys apogon had the most diverse parasite community (8 species). Seasons affected the prevalence and mean intensity of parasitic infection; the prevalence was highest during the rainy (85.54%) and winter (84.75%) seasons, and lower during the summer (63.96%) season. Fish diversity and parasite diversity exhibited a positive correlation relationship. In the light of declining fish populations in the Nong Han wetland, this study may provide critical information for the sustainable management of this wetland. Furthermore, some of the identified fish parasites can be harmful to humans if fish is eaten raw or improperly cooked, as is the tradition in northeastern Thailand, so our findings may bear relevance for public health workers as well.
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References
Abro MM, Birmani NA, Bhutto MB (2019) Incidence of helminth parasites in freshwater fishes of the River Indus at Jamshoro, Sindh, Pakistan. Biol Forum 11:113–116
Acosta AA, Smit NJ, Silva RJ (2020) Diversity of helminth parasites of eight siluriform fishes from the Aguapeí River, upper Paraná basin, São Paulo state, Brazil. Int J Parasitol Parasites Wildl 11:120–128. https://doi.org/10.1016/j.ijppaw.2020.01.003
Alves MT, Taylor NGH (2020) Models suggest pathogen risks to wild fish can be mitigated by acquired immunity in freshwater aquaculture systems. Sci. Rep. 10:7513. https://doi.org/10.1038/s41598-020-64023-2
Atalabi TE, Awharitoma AO, Akinluyi FO (2018) Prevalence, intensity, and exposed variables of infection with Acanthocephala parasites of the gastrointestinal tract of Coptodon zillii (Gervais, 1848) [Perciformes: Cichlidae] in Zobe Dam, Dutsin-Ma Local Government Area, Katsina State, Nigeria. J Basic Appl Zool 79:1–7. https://doi.org/10.1186/s41936-018-0042-6
Bichi AH, Bawaki SA (2010) Survey of ectoparasites on the gill, skin, and fins of Oreochromis niloticus at Bagauda Fish Farm, Kano. Nigeria. J. pure appl. sci. technol. 3:83–86. https://doi.org/10.4314/bajopas.v3i1.58720
Boonchot K, Wongsawad C (2005) A survey of helminths in cyprinoid fish from the Mae Ngad Somboonchon reservoir, Chiang Mai province, Thailand. Southeast Asian J Trop Med Public Health. 36(1):103–107
Boonmekam D, Namchote S, Nak-ai W, Glaubrecht M, Krailas D (2016) The prevalence of human intestinal fluke infections, Haplorchis taichui, in thiarid snails and cyprinid fish in Bo Kluea District and Pua District, Nan Province, Thailand. Silpakorn U Science & Tech J 10: 29-37. https://doi.org/10.14456/sustj.2016.3
Braga MP, Araújo SBL, Boeger WA (2014) Patterns of interaction between neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitol. Res. 113:481–490. https://doi.org/10.1007/s00436-013-3677-8
Bush OA, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 83(4): 575-583. https://doi.org/10.7939/R3J38KV04
Carrassón M, Dallarés S, Cartes JE, Constenla M, Pérez-del-Olmo A, Zucca L, Kostadinova A (2019) Drivers of parasite community structure in fishes of the continental shelf of the Western Mediterranean: the importance of host phylogeny and autecological traits. Int J Parasitol 49:669–683. https://doi.org/10.1016/j.ijpara.2019.04.004
Chai JY, Sohn WM, Na BK, Yong TS, Eom KS, Yoon CH, Hoang EH, Jeoung HG, Socheat D (2014) Zoonotic trematode metacercariae in fish from Phnom Penh and Pursat. Cambodia. Korean J. Parasitol. 52:35–40. https://doi.org/10.3347/kjp.2014.52.1.35
Chawchai S, Chabangborn A, Kylander M, Löwemark L, Mörth CM, Blaauw M, Klubseang W, Reimer PJ, Fritz SC, Wohlfarth B (2013) Lake Kumphawapi—an archive of Holocene palaeoenvirontal and palaeoclimatic changes in northeast Thailand. Quat. Sci. Rev. 68:59–75. https://doi.org/10.1016/j.quascirev.2013.01.030
Dash G, Majumder D, Ramudu KR (2015) Seasonal distribution of parasites in freshwater exotic carps of West Bengal. India. Indian J. Anim. Res. 49:95–102. https://doi.org/10.5958/0976-0555.2015.00020.5
Donthaisong C, Arunsan P, Suwannatrai K, Prasopdee S, Kulsantiwong J, Wongmaneeprateep S, Suwannatrai A, Tesana S (2015) Reprint of ‘Experimental infection of Opisthorchis viverrini cercariae to the cyprinid fish, Barbonymus gonionotus’. Acta Trop 141:253–257
El-Seify MA, Zaki MS, Desouky ARY, Abbas HH, Abdel Hady OK, Abou Zaid AA (2018) Seasonal variations and prevalence of some external parasites affecting freshwater fishes reared at upper Egypt. IIn: Kumar V., Kumar M., Prasad R. (eds) Phytobiont and Ecosystem Restitution. Springer, Singapore. pp 175-183. https://doi.org/10.1007/978-981-13-1187-1_9
Ferreira-Sobrinho A, Tavares-Dias M (2016) A study on monogenean parasites from the gills of some cichlids (Pisces: Cichlidae) from the Brazilian Amazon. Rev Mex Biodivers 87:1002–1009. https://doi.org/10.1016/j.rmb.2016.06.010
Golzio JESA, Falkenberg JM, Praxedes RCG, Coutinho AS, Laurindo MK, Pessanha A, Madi RR, Patrício J, Vendel AL, Souza GTR, Melo CM, Lacerda ACF (2017) Gill parasites of fish from two estuaries in Northeastern Brazil: new hosts and geographical records. An. Acad. Bras. Cienc. 89:2281–2291. https://doi.org/10.1590/0001-3765201720160883
Hoffman GL (1967) Parasites of North American freshwater fishes. University of California Press, Los Angeles
Hoffman GL (1999) Parasites of North American freshwater fishes. A division of Cornell University Press, London
Iyaji FO, Eyo JE (2008) Parasites and their freshwater fish host. Bio-Research 6:328–338. https://doi.org/10.4314/br.v6i1.28660
Kabata Z (1985) Parasites and diseases of fish cultured in the trophics. Taylor and Francis, London and Philadelphia
Kaewsang W (2017) Sustainable conservation guidelines for management and utilization of Nong Han Kumphawapi wetland. Dissertation, Silpakorn University. Khalil MI, El-Shahawy IS, Abdelkader HS (2014) Studies on some fish parasites of public health importance in the southern area of Saudi Arabia. Rev Bras Parasitol Vet 23:435–442. https://doi.org/10.1590/s1984-29612014082
Kim CS, Echaubard P, Suwannatrai A, Kaewkes S, Wilcox BA, Sripa B (2016) Seasonal and spatial environmental influence on Opisthorchis viverrini intermediate hosts, abundance, and distribution: insights on transmission dynamics and sustainable control. PLoS Negl. Trop. Dis. 10:1–25. https://doi.org/10.1371/journal.pntd.0005121
Kim CS, Smith JF, Suwannatrai A, Echaubard P, Wilcox B, Kaewkes S, Sithithaworn P, Sripa B (2017) Role of socio-cultural and economic factors in cyprinid fish distribution networks and consumption in Lawa Lake region, Northeast Thailand: novel perspectives on Opisthorchis viverrini transmission dynamics. Acta Trop 170:85–94
Khanum H, Begum S, Begum A (2011) Seasonal prevalence, intensity and organal distribution of helminth parasites in Macrognathus aculeatus. Dhaka Univ. J. Biol. Sci. 20:117–122
Kulabtong S (2012) Biology and culture techniques of bocourti catfish, Pangasius bocourti Sauvage, 1880 in Thailand. Veridian E-J. sci. technol. Silpakorn Univ. 5:412–419
Kumari A, Sahay D (2019) Seasonal variation in prevalence of trematode parasites in freshwater fish Channa punctatus of Chapra, Bihar. IJRAR 6:826–828
Kumnerdphol A (2010) Parasites of some cyprinid fishes from Bang Pra Reservoir, Chon Buri Province. Dissertation, Kasetsart University.
Labbunruang N, Kulsantiwong J (2019) Investigation of trematode metacercariae in fermented fish from Udon Thani and Kalasin Provinces, Thailand. Phranakhon Rajabhat Research Journal: Science and Technology. 14:36–46
Lerssutthichawal T (1999) Monogeneans of the freshwater Siluriform fishes of Thailand. Dissertation, University of Malaya.
Lerssutthichawal T, Supamattaya K (2005) Diversity and distribution of parasites from potentially cultured freshwater fish in Nakhon Si Thammarat. Songklanakarin J. Sci. Technol. 27(Suppl. 1):333–345 ((in Thai))
Levy E, Canel D, Rossin MA, Hernández-Orts JS, González-Castro M, Timi JT (2019) Parasites as indicators of fish population structure at two different geographical scales in contrasting coastal environments of the south-western Atlantic. Estuar. Coast. Shelf Sci. 229:106400. https://doi.org/10.1016/j.ecss.2019.106400
Maceda-Veiga A, Nally RM, Green AJ, Poulin R, de Sostoa A (2019) Major determinants of the occurrence of a globally invasive parasite in riverine fish over large-scale environmental gradients. Int. J. Parasitol. 49:625–634. https://doi.org/10.1016/j.ijpara.2019.03.002
Madyod S (2014) Identification on monogenean parasite in Nile tilapia, Oreochromis niloticus from cage culture in Thapi river, Nakorn Si Thammarat Province. RMUTSB Acad. J. 2(2):97–108 ((in Thai))
Maheboob SI (2020) Seasonal study of parasitic infection in fresh water fishes from Siddheshwar dam Hingoli District (M.S). India. J Emerg Technol Innov Res 7:821–824
Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124(suppl 7):S83-99. https://doi.org/10.1017/s003118200200149x
Mard-arhin N, Prawang T, Wongsawad C (2001) Helminths of freshwater animals from five provinces in Northern Thailand. Southeast Asian J Trop Med Public Health 32(suppl 2):206–9
Miah MdF, Deb M, Ali H, Quddus MMA, Ahmed K (2013) Comparative surveillance of parasitic infestation in Channa punctatus (Osteichthys: Channidae) collected from open and closed water in Sylhet, Bangladesh. Adv. Zool. Bot. 1: 17-23. https://doi.org/10.13189/AZB.2013.010103
Nelson JS (2006) Fishes of the world. John Wiley and Sons Inc., New Jersey
Noikong W, Wongsawad C, Phalee A (2011) Seasonal variation of metacercariae in cyprinoid fish from Kwae Noi Bamroongdan Dam, Phitsanulok province, Northern Thailand. Southeast Asian J Trop Med Public Health 42:58–62
Phalee A (2018) Prevalence of helminthes infection in fishes from Nong Yat Reservoir, Mueang District. Nakhon Phanom Province. Burapha Science Journal. 23(3):1757–1769 ((in Thai))
Purivirojkul W (2013) Parasitology of aquatic animals. Kasetsart University Press, Bangkok ((in Thai))
Purivirojkul W, Sirikanchana P (2006) Two species of Prosorhynchoides Dollfus, 1929 (Bucephalidae: Bucephalinae) from Mekong giant catfish (Pangasianodon Gigas Chevey) from Mekong River. Chiangrai Province. Songklanakarin J. Sci. Technol. 28:745–751
Purivirojkul W, Areechon N (2008) Parasitic diversity of siluriform fishes in Mekong River, Chiang Rai Province. Kasetsart J. (Nat. Sci.). 42: 34-39.
Rabone M, Wiethase JH, Allan F, Gouvras AN, Pennance T, Hamidou AA, Webster BL, Labbo R, Emery AM, Garba AD, Rollinson D (2019) Freshwater snails of biomedical importance in the Niger River Valley: evidence of temporal and spatial patterns in abundance, distribution and infection with Schistosoma spp. Parasit Vectors 12:498. https://doi.org/10.1186/s13071-019-3745-8
Reiczigel J, Marozzi M, Fábián I, Rózsa L (2019) Biostatistics for parasitologists—a primer to quantitative parasitology. Trends Parasitol 35(4):277–281. https://doi.org/10.1016/j.pt.2019.01.003
Rim HJ, Sohn WM, Yong TS, Eom KS, Chai JY, Min DY, Lee SH, Hoang EH, Phommasack B, Insisengmay S (2008) Fishborne trematoda metacercariae detected in freshwater fish from Vientiane Municipality and Savannakhet Province, Lao PDR. Korean J Parasitol 46:253–260. https://doi.org/10.3347/kjp.2008.46.4.253
Rushton-Mellor SK (1993) The genus Argulus (Crustacea: Branchiura) in Africa: identification keys. Syst Parasitol 28:51–63
Saenjundaeng P (2014) Encyclopedia of fresh water fish of Thailand. KlungnanaVitthaya Press, Khonkaen ((in Thai))
Sanchez-Ramirez C, Vidal-Martinez VM, Aguirre-Macedo ML, Rodriguez-Canul RP, Gold-Bouchot G, Sures B (2007) Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinae) and its host, the Nile tilapia (Oreochromis niloticus), as bioindicators of chemical pollution. J. Parasitol. 93:1097–1106. https://doi.org/10.1645/ge-1162r.1
Senasri N, Tesana S, Yuangsoi B, Wongmaneeprateep S (2019) Effects of vitamin C supplementation on infectivity of Opisthorchis viverrini metacercaria in silver barb (Barbonymus gonionotus). Biosci. Res. 16:2204–2216
Schade FM, Raupach MJ, Wegner KM (2016) Seasonal variation in parasite infection patterns of marine fish species from the Northern Wadden Sea in relation to interannual temperature fluctuations. J. Sea Res. 113:73–84. https://doi.org/10.1016/j.seares.2015.09.002
Schmidt GD (1970) How to know the tapeworms. C. Brown Company Publishers, lowa, W.M
Shamsi S, Suthar J (2016) A revised method of examining fish for infection with zoonotic nematode larvae. Int. J. Food Microbiol 227:13–16. https://doi.org/10.1016/j.ijfoodmicro.2016.03.023
Shamsi S, Turner A, Wassens S (2018) Description and genetic characterization of a new Contracaecum larval type (Nematoda: Anisakidae) from Australia. J. Helminthol. 92:216–222. https://doi.org/10.1017/S0022149X17000360
Smith HM (1945) The fresh-water fishes of Siam or Thailand. Smithsonian Institution United States National Museum. Bull. 188. T. F. H. Publications, Inc., New Jersey.
Sriwongpuk S (2013) Parasites of knife fish (Notopterus notopterus, Pallas) from the Huajarake Mark Reservior in Buriram province. Khon Kaen Agr. J. 41(Suppl. 1):446–452 ((in Thai))
Suntaravitun P, Dokmaikaw A (2014) Prevalence of trematode metacercariae in cyprinoid fish from Rim Kok Subdistrict, Mueang Chiang Rai District, Chiang Rai Province. J. Mahanakorn Vet. Med. 9(2):113–120
Tesana S, Kaewkes S, Srisawangwonk T, Phinlaor S (1985) The distribution and density of Opisthorchis viverrini metacercariae in cyprinoid fish in Khon Kaen Province. J. Parasitol. Trop. Med. Assoc. 8:36–39
Ullah I, Khan MF, Khan MS, Khan SU, Hussain S, Javid M (2018) Copepod ecto-parasites of Labeo rohita from Dera Ismail Khan, Khyber Pakhtunkhwa Pakistan. J Entomol Zool Stud 6:1075–1076
Vankara AP, Mani G, Vijayalakshmi C (2011) A report on various digenetic metacercariae from the freshwater fishes of River Godavari. Rajahmundry. J. Parasit. Dis. 35:177–85. https://doi.org/10.1007/s12639-011-0041-8
Wali A, Balkhi MH, Maqbool R, Darzi MM, Shah FA, Bhat FA, Bhat BA (2016) Distribution of helminth parasites in intestines and their seasonal rate of infestation in three freshwater fishes of Kashmir. J Parasitol Res 1:1–16. https://doi.org/10.1155/2016/8901518
Willis MS (2001) Population Biology of Allocreadium lobatum Wallin, 1909 (Digenea: Allocreadiidae) in the Creek Chub, Semotilus atromaculatus, Mitchill (Osteichthyes: Cyprinadae), in a Nebraska Creek, USA. Mem Inst Oswaldo Cruz, Rio de Janeiro 96:331–338. https://doi.org/10.1590/S0074-02762001000300008
Wiriya B, Clausen JH, Inpankaew T, Thaenkham U, Jittapalapong S, Satapornvanit K, Dalsgaard A (2013) Fish-borne trematodes in cultured Nile tilapia (Oreochromis niloticus) and wild-caught fish from Thailand. Vet. Parasitol. 198:230–234. https://doi.org/10.1016/j.vetpar.2013.08.008
Zhu X, Barton DP, Wassens S, Shamsi S (2020) Morphological and genetic characterisation of the introduced copepod Lernaea cyprinacea Linnaeus (Cyclopoida: Lernaeidae) occurring in the Murrumbidgee catchment. Australia. Mar. Freshw. Res 72(6):876–886. https://doi.org/10.1071/MF20145
Acknowledgements
We thank Dr. Sumate Chomphutawach for assistance with data extraction from host-parasite checklists and helping with sample collection. We are very grateful to Khon Kaen University, Department of Fisheries, Thailand for funding this study.
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This study was supported by the National Research Council of Thailand (No. 600096), the earmarked fund for the Fundament Research Funds for the Khon Kaen University (958-4-34566-1).
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The authors’ responsibilities were as follows: PW and WP conceptualized the study; PW, JJ, and SW conducted research; PW and SW provided the materials; JJ and WP collected the data; WP and JJ analyzed the data; and JJ and WP wrote the manuscript. All authors took part in the study design, read the final manuscript, and provided comments and suggestions for improvements.
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Juntaban, J., Prisingkorn, W., Wongmaneeprateep, S. et al. A survey of parasites in freshwater fishes from Nong Han wetland, Udon Thani Province, Thailand. Parasitol Res 120, 3693–3708 (2021). https://doi.org/10.1007/s00436-021-07310-9
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DOI: https://doi.org/10.1007/s00436-021-07310-9