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Introducing the land snail Bradybaena pellucida increased infection risk of the avian parasite Postharmostomum commutatum in the Kanto region of Japan

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Abstract

The trematode Postharmostomum commutatum is a parasite of the chicken Gallus gallus domesticus. Its heavy infection can cause inflammation and hemorrhage in the cecum of host birds. We found a severe infection of metacercariae of P. commutatum, which was identified based on DNA barcodes with morphology, in the introduced land snail Bradybaena pellucida and its related species in the Kanto region of Japan. Our field survey revealed that metacercariae were detected in 14 of 69 sampling locations in this region. B. pellucida was thought to be the major second intermediate host of metacercariae of the trematode because this snail was most frequently found in the study area and the prevalence and infection intensity were higher than those of the other snail species. The observed increase in metacercariae in introduced populations of B. pellucida can enhance the infection risk of chickens and wild host birds, probably owing to the spillback effect. Our seasonal field study showed that the prevalence and infection intensity of metacercaria seemed to be high in populations of B. pellucida during the summer and early autumn. Therefore, chickens should not be bred outdoors during these seasons to prevent severe infection. Our molecular analysis, based on cytochrome c oxidase subunit I sequences, showed a significantly negative value for Tajima’s D in P. commutatum, suggesting an increase in its population size. Thus, P. commutatum distributed in the Kanto region may have increased its population size with the introduction of the host snail.

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Data availability

The sequence datasets analyzed during the current study are available in the Genbank repository, LC760655-LC760662. The other datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Alicata JE (1940) The life cycle of Postharmostomum gallinum, the cecal fluke of poultry. J Parasitol 26(2):135–143. https://doi.org/10.2307/3272380

    Article  Google Scholar 

  • Alicata JE (1964) Parasitic infections of man and animals in Hawaii. Tech Bull Hawaii Agric Exp Sta 6:11–139. (http://hdl.handle.net/10125/16564)

    Google Scholar 

  • Amato SB, Bezerra JCB (1992) Concurrent infection of Postharmostomum gallinum (Digenea, Brachylaimidae) and Eurytrema coelomaticum (Digenea, Dicrocoeliidae) in Bradybaena similaris (Stylommatophora, Xanthonichidae). Memórias do Instituto Oswaldo Cruz 87:309–311. (https://www.scielo.br/j/mioc/a/JcLr3DT7Rq56MmZwtFyx35z/?format=pdf&lang=en)

    Article  Google Scholar 

  • Asada J (1928) Harmostomum horisawai using domestic chickens as definitive hosts in Japan. Tokyo Med J 2589:1963–1968 [In Japanese]

    Google Scholar 

  • Asada J, Miyata I (1939) Studies of cercariae infecting terrestrial mollusks, especially Bradybaena similaris and Acusta despecta sieboldiana. Tokyo Med J 3123:492–497 [In Japanese]

    Google Scholar 

  • Asami T, Yamashita H, Park J, Ishikawa H (1997) Geographical distribution of the land snail Bradybaena pellucida (Pulmonata: Bradybaenidae). The Yuriyagai 5(1–2):31–42

    Google Scholar 

  • Azuma M (1995) Colored illustrations of the land snails of Japan, Enlarged and Revised Edition, Hoikusya, Osaka. [In Japanese]

  • Baker GM (2002) Molluscs as Crop Pests. CABI publishing, Oxon and New York

    Book  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Dawes B (1968) The Trematoda with special reference to British and other European forms. Cambridge University Press, London

    Google Scholar 

  • Duarte MJF (1980) The life cycle of Postharmostomum gallinum Witenberg, 1923, in Rio de Janeiro state, Brazil. Rev Bras Biol 40:793–809

    Google Scholar 

  • Fukuda Y (1999) Bradybaena pellucida in Hiratsuka City, Kanagawa Prefecture, Central Japan. Chiribotan 30:18–22 [In Japanese]

    Google Scholar 

  • Furuse N (2014) Science of the domestic chicken. Asakura Publishing Co., Ltd., Tokyo

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Heinze G, Ploner M, Dunkler D, Southworth H, Heinze MG (2022) Package ‘logistf’. http://mirrors.nic.cz/R/web/packages/logistf/logistf.pdf

  • Horisawa J (1915) On a trematode obtained from the caecum of the fowl. Nippon Byori Gakukaishi 3:377–380 [In Japanese]

    Google Scholar 

  • Ibaraki Prefecture (2022) Ibaraki Prefectural Government. https://www.pref.ibaraki.jp/index.html. Accessed 7 December 2022

  • Ikezawa H (2012) Distribution expansion and crop damage of the land snail Bradybaena pellucida in Ibaraki Prefecture Japan. A Museum 73:5

    Google Scholar 

  • Ishii N (1932) Studies on avian trematodes (Report I). Jikken Igaku Zasshi 16(1):1205–1233

    Google Scholar 

  • Japan Meteorological Agency (2023) Historical weather data retrieval. Japan Meteorological Agency. https://www.data.jma.go.jp/obd/stats/etrn/. Accessed 15 Jan 2023

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecol 90(8):2047–2056. https://doi.org/10.1890/08-1085.1

    Article  CAS  Google Scholar 

  • Kifune T, Kugi G (1978) Two trematode parasites of copper and green pheasants from Kyushu, Japan. Jap J Parasitol 27:225–230. (http://jsp.tm.nagasaki-u.ac.jp/archive/pdf/1978_27_3_07.pdf)

    Google Scholar 

  • Komai R (2008) Brand Name Chickens and Jidori Chickens. Anim Husb 62:657–664 [In Japanese]

    Google Scholar 

  • Kugi G (1987) Studies on the helminth fauna of vertebrates in Oita Prefecture. Part 2. Avian helminths.

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuris Y (1932) Studies on trematodes of chicken in Japan. J Kumamoto Med Soc 8(4):283–298

    Google Scholar 

  • Kurisu Y (1930) Study of trematode infecting terrestrial mollusks in Japan, especially infection of cercariae. J Kumamoto Med Soc 6:1318–1331 [In Japanese]

    Google Scholar 

  • Miao YW, Peng MS, Wu GS, Ouyang YN, Yang ZY, Yu N, Liang J-P, Pianchou G, Beja-Pereira A, Mitra B, Palanichamy MG, Baig M, Chaudhuri TK, Shen Y-Y, Kong Q-P, Murphy RW, Yao Y-G, Zhang YP (2013) Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity 110(3):277–282. https://doi.org/10.1038/hdy.2012.83

    Article  CAS  PubMed  Google Scholar 

  • Minamiya Y (2020) First record of domestic introduced species, Bradybaena pellucida (Pulmonata; Bradybaenidae) in Tochigi Prefecture, and their current distribution. Bull Tochigi Pref Mus 37:5–10

    Google Scholar 

  • Nakao M, Waki T, Sasaki M, Anders JL, Koga D, Asakawa M (2017) Brachylaima ezohelicis sp. nov. (Trematoda: Brachylaimidae) found from the land snail Ezohelix gainesi, with a note of an unidentified Brachylaima species in Hokkaido Japan. Parasitol Int 66:240–249. https://doi.org/10.1016/j.parint.2017.01.015

    Article  PubMed  Google Scholar 

  • Nakao M, Sasaki M, Waki T, Anders JL, Katahira H (2018) Brachylaima asakawai sp. Nov. (Trematoda: Brachylaimidae), a rodent intestinal fluke in Hokkaido, Japan, with a finding of the first and second intermediate hosts. Parasitol Int 67(5):565–574. https://doi.org/10.1016/j.parint.2018.04.010

    Article  PubMed  Google Scholar 

  • Nakao M, Sasaki M, Waki T (2020) Brachylaima succini sp. Nov. (Trematoda: Brachylaimidae) from Succinea lauta, an amber snail in Hokkaido Japan. Parasitol Int 77:102104. https://doi.org/10.1016/j.parint.2020.102104

    Article  CAS  PubMed  Google Scholar 

  • Nyumura N, Asami T (2015) Synchronous and non-synchronous semelparity in sibling species of pulmonates. Zool Sci 32(4):372–377. https://doi.org/10.2108/zs150020

    Article  Google Scholar 

  • Okamoto M (1992) Bradybaena pellucida from Tateyama, Chiba Prefecture. Chiribotan 23:13–18 [In Japanese]

    Google Scholar 

  • Ozaki Y (1925) On Harmonostomum horisawa1 and its life history. Tokyo Iji-Shinshi 2434:12–15 [In Japanese]

    Google Scholar 

  • Pence DB (1994) Postharmostomiasis in wild turkeys in New Mexico. J Wildl Dis 30:285–286. https://doi.org/10.7589/0090-3558-30.2.285

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 15 Desember 2022

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  • Seki K, Inoue S, Asami T (2002) Geographical distributions of sibling species of land snails Bradybaena pellucida and B. similaris in the Boso peninsula. Venus 61(1–2):41–48. https://doi.org/10.18941/venus.61.1-2_41

  • Sugiyama K (1982) Development mechanism of entrepreneur type of laying hen farming –a case study of the Aikeien Poltry Farms, Co. J Fac Appl Biol Sci Hiroshima Univ 21:75–89

    Google Scholar 

  • Takahashi S (1928) Six cercariae and their regia. Med Bull Fukuoka Univ 21(3):49–53

    Google Scholar 

  • Taylor MA, Coop RL, Wall RL (2016) Veterinary parasitology, 4th edn. John Wiley and Sons Inc, England

    Google Scholar 

  • The Nature Conservation Society of Japan (2004) Nature Study 2004 "Let's look for land snails”. https://www.nacsj.or.jp/shirabe/2004/07/1796/. Accessed 30 January 2023 [In Japanese]

  • Uechi T, Nishiyama A, Abe S, Okoba T (2020) New records of Bradybaena pellucida Kuroda & Habe in Habe, 1953 from Osaka Prefecture. Chiribotan 50(1):149–154 [In Japanese]

    Google Scholar 

  • Ueta M, Ikeno S (2021) Report of the Bird Monitoring Survey of Breeding Distribution in Ibaraki Prefecture, Japan, 2016–2021. Bird Research, Tokyo [In Japanese]

  • Umeya K, Okada T (2003) Agricultural Insect Pests in Japan. Zenkoku Noson Kyoiku Kyokai, Tokyo. [In Japanese]

  • Valadão MC, Silva B, López-Hernández D, Araújo JV, Locke SA, Pinto HA (2018) A molecular phylogenetic study of the caecal fluke of poultry, Postharmostomum commutatum (= P. gallinum)(Trematoda: Brachylaimidae). Parasitol Res 117(12):3927–3934. https://doi.org/10.1007/s00436-018-6102-5

    Article  PubMed  Google Scholar 

  • Waki T, Nakao M, Hayashi K, Ikezawa H, Tsutumi N (2018) Molecular and morphological discrimination of dicrocoeliid larvae (Trematoda: Digenea) from terrestrial mollusks in Japan. J Parasitol 104(6):660–670. https://doi.org/10.1645/18-24

    Article  CAS  Google Scholar 

  • Waki T, Sasaki M, Mashino K, Iwaki T, Nakao M (2020) Brachylaima lignieuhadrae n. sp. (Trematoda: Brachylaimidae) from land snails of the genus Euhadra in Japan. Parasitol Int 74:1–8. https://doi.org/10.1016/j.parint.2019.101992

    Article  CAS  Google Scholar 

  • Waki T, Nakao M, Sasaki M, Ikezawa H, Inoue K, Ohari Y, Kameda Y, Asada M, Furusawa H, Miyazaki S (2022) Brachylaima phaedusae n. sp. (Trematoda: Brachylaimidae) from door snails in Japan. Parasitol Int 86:102469. https://doi.org/10.1016/j.parint.2021.102469

    Article  CAS  PubMed  Google Scholar 

  • Waki T, Nakao M, Sasaki M, Takano T, Ikezawa H, Miyazaki S (2022) Report of unidentified metacercariae of the genus Brachylaima (Trematoda, Brachylaimidae) in Japan, with records of new localities and new hosts of two known species. TAXA 52:37–47. https://doi.org/10.19004/taxa.52.0_37

    Article  Google Scholar 

  • Yamaguti S (1933) Studies on the helminth fauna of Japan. Part I. Trematodes of birds, reptiles and mammals. Jap J Zool 5(i):1–134

    Google Scholar 

  • Yamaguti S (1975) Synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms. Keigaku Publishing Co, Tokyo

    Google Scholar 

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Acknowledgements

We greatly appreciate Minako Adachi, Yusuke Goto, and Kyoko Uehara for helping our research. We also greatly appreciate Shoichi Inose’s permission to survey farmland sites.

Funding

This work was supported by a Nakatsuji Foresight Foundation Research Grant.

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Authors and Affiliations

  1. Faculty of Science, Toho University, 2-2-1 Miyama, Funabashi, Chiba, 274-8510, Japan

    Haruki Furusawa & Tsukasa Waki

  2. Ibaraki Nature Museum, 700, Osaki, Bando, Ibaraki, 306-0622, Japan

    Hiromi Ikezawa

  3. Centre for Climate Change Adaptation, National Institute for Environmental Studies, Tsukuba, 305-8506, Japan

    Shohei G. Tsujimoto

  4. Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, 020-8550, Japan

    Madoka Ichikawa-Seki

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  1. Haruki Furusawa
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  4. Madoka Ichikawa-Seki
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  5. Tsukasa Waki
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Contributions

Haruki Furusawa, Madoka Ichikawa-Seki, and Tsukasa Waki wrote the main manuscript text. Haruki Furusawa, Hiromi Ikezawa, and Tsukasa Waki sampled host snails. Haruki Furusawa and Tsukasa Waki identified worms. Shohei G Tsujimoto analyzed the datasets. Haruki Furusawa prepared figures, tables, and online resources. All authors reviewed the manuscript.

Corresponding author

Correspondence to Tsukasa Waki.

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The authors declare no competing interests.

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Furusawa, H., Ikezawa, H., Tsujimoto, S.G. et al. Introducing the land snail Bradybaena pellucida increased infection risk of the avian parasite Postharmostomum commutatum in the Kanto region of Japan. Parasitol Res 122, 2207–2216 (2023). https://doi.org/10.1007/s00436-023-07921-4

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