Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-28T04:36:43.686Z Has data issue: false hasContentIssue false
  • English
  • Français

The Asian fish tapeworm (Schyzocotyle acheilognathi) discovered in Western Australia may pose a threat to the health of endemic native fishes

Published online by Cambridge University Press:  13 October 2021

C.J. Palermo Open the ORCID record for C.J. Palermo [Opens in a new window] ,
D.L. Morgan Open the ORCID record for D.L. Morgan [Opens in a new window] ,
S.J. Beatty Open the ORCID record for S.J. Beatty [Opens in a new window] ,
A. Elliot  and
T.L. Greay Open the ORCID record for T.L. Greay [Opens in a new window]
C.J. Palermo*
Affiliation:
College of Science, Health, Engineering and Education, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia Western Australian State Agricultural Biotechnology Centre, Murdoch University, Murdoch, 90 South Street, Murdoch, WA 6150, Australia
D.L. Morgan
Affiliation:
Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia
S.J. Beatty
Affiliation:
Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia
A. Elliot
Affiliation:
College of Science, Health, Engineering and Education, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia
T.L. Greay
Affiliation:
College of Science, Health, Engineering and Education, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia Western Australian State Agricultural Biotechnology Centre, Murdoch University, Murdoch, 90 South Street, Murdoch, WA 6150, Australia Executive Consultant, EpiSeq, PO Box 357, Kwinana, WA 6966, Australia
*
Author for correspondence: C.J. Palermo, E-mail: cindypalermo@outlook.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The Asian fish tapeworm (Schyzocotyle acheilognathi) is an important fish parasite with a wide host range that infects over 300 species of fish worldwide. Schyzocotyle acheilognathi has been reported from eastern coastal areas of Australia, but has not been previously reported in Western Australia (WA). During a control program for invasive freshwater fishes in south-western WA, a region with a unique and highly endangered freshwater fish fauna, tapeworms identified as S. acheilognathi from their distinctive scolex morphology were found at a prevalence of 3.3% in goldfish (Carassius auratus), 37.0% in koi carp (Cyprinus carpio haematopterus) and 65.0% in eastern gambusia (Gambusia holbrooki) in a small suburban lake to the north of Perth. For molecular confirmation, the 18S ribosomal RNA gene was targeted at hypervariable V4 region. Koi carp isolates were 100% identical to S. acheilognathi isolated from varying hosts, including the red shiner (Cyprinella lutrensis) and a human sample. Sequences obtained from two eastern gambusia were identified as S. acheilognathi, but formed a discrete cluster and may represent a novel genotype. Isolates from two other eastern gambusia and two goldfish formed a distinct clade with only 91.9% similarity to previously sequenced isolates of S. acheilognathi. This emphasizes the importance of molecular identification methods in addition to morphological identification. The presence and potential for transmission of these parasites in south-western WA may threaten the health of native fishes, which are immunologically naïve to this introduced parasite. Immediate control or containment measures should be implemented to halt the spread of these parasites.

Keywords

Invasive freshwater fishco-invading parasitemodified wetlandphylogeneticWestern Australia
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e60
Copyright
Copyright © The Author(s), 2021. 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

Bauer, O, Musselius, V and Strelkov, Y (1969) Diseases of pond fish. 220 pp. Israel Program for Scientific Translations, Cornell University Press, USSR.Google Scholar
Bean, MG (2008) Occurrence and impact of the Asian fish tapeworm Bothriocephalus acheilognathi in the Rio Grande (Rio Bravo Del Norte). Dissertation, Texas State University. Available at https://digital.library.txstate.edu/handle/10877/3123 (accessed 28 July 2020).Google Scholar
Bean, MG and Bonner, TH (2010) Spatial and temporal distribution of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in the Río Grande (Río Bravo del Norte). Journal of Aquatic Animal Health 22(3), 182–189.CrossRefGoogle Scholar
Bean, MG, Škeříková, A, Bonner, TH, Scholz, T and Huffman, DG (2007) First record of Bothriocephalus acheilognathi in the Rio Grande with comparative analysis of ITS2 and V4-18S rRNA Gene Sequences. Journal of Aquatic Animal Health 19(2), 71–76.Google Scholar
Beatty, SJ and Morgan, DL (2013) Introduced freshwater fishes in a global endemic hotspot and implications of habitat and climatic change. Biological Invasions Records 2(1), 1–9.Google Scholar
Boonthai, T, Herbst, SJ, Whelan, GE, Van Deuren, MG, Loch, TP and Faisal, M (2017) The Asian fish tapeworm Schyzocotyle acheilognathi is widespread in baitfish retail stores in Michigan, USA. Parasites & Vectors 10, 618.CrossRefGoogle ScholarPubMed
Brabec, J, Kuchta, R, Scholz, T and Littlewood, DTJ (2016) Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data. International Journal of Parasitology 46(9), 555–562.Google ScholarPubMed
Brouder, MJ (1999) Relationship between length of roundtail chub and infection intensity of Asian fish tapeworm Bothriocephalus acheilognathi. Journal of Aquatic Animal Health 11(3), 302–304.2.0.CO;2>CrossRefGoogle Scholar
Brouder, MJ and Hoffnagle, TL (1997) Distribution and prevalence of the Asian fish tapeworm, Bothriocephalus acheilognathi, in the Colorado River and tributaries, Grand Canyon, Arizona, including two new host records. Proceedings of the Helminthological Society of Washington 64(2), 219–226.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4), 575–583.Google Scholar
Chapman, A, Hobbs, R, Morgan, D and Gill, H (2006) Helminth parasitism of Galaxias maculatus (Jenyns 1842) in southwestern Australia. Ecology of Freshwater Fish 15(4), 559–564.Google Scholar
Choudhury, A and Cole, R (2012) Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). pp. 385–400 in Francis, RA (Ed) A handbook of global freshwater invasive species. London, Earthscan.Google Scholar
Choudhury, A, Hoffnagle, TL and Cole, RA (2004) Parasites of native and nonnative fishes of the Little Colorado River, Grand Canyon, Arizona. Journal of Parasitology 90(5), 1042–1053.CrossRefGoogle ScholarPubMed
Choudhury, A, Charipar, E, Nelson, P, Hodgson, JR, Bonar, S and Cole, RA (2006) Update on the distribution of the invasive Asian fish tapeworm, Bothriocephalus acheilognathi, in the US and Canada. Comparative Parasitology 73(2), 269–273.CrossRefGoogle Scholar
Choudhury, A, Zheng, S, de León, GP-P, Martínez-Aquino, A, Brosseau, C and Gale, E (2013) The invasive Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in the Chagres River/Panama Canal drainage, Panama. Bioinvasion Records 2(2), 99–104.CrossRefGoogle Scholar
Cole, RA and Choudhury, A (2016) Invasive species compendium: Bothriocephalus acheilognathi. Available at http://www.cabi.org/isc/datasheet/91669 (accessed 2 July 2021).Google Scholar
Davydov, O (1978) Effect of Bothriocephalus gowkongensis on the morphological characters and physiological statistics of the carp. Hydrobiology Journal 14, 50–54.Google Scholar
de León, GP-P, Lagunas-Calvo, O, García-Prieto, L, Briosio-Aguilar, R and Aguilar-Aguilar, R (2018) Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico. Journal of Helminthology 92(3), 279–290.Google Scholar
Dove, A and Fletcher, A (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. Journal of Helminthology 74(2), 121–127.CrossRefGoogle ScholarPubMed
Dove, A, Cribb, T, Mockler, S and Lintermans, M (1997) The Asian fish tapeworm, Bothriocephalus acheilognathi, in Australian freshwater fishes. Marine and Freshwater Research 48(2), 181–183.CrossRefGoogle Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5), 1792–1797.CrossRefGoogle ScholarPubMed
Edwards, DJ and Hine, P (1974) Introduction, preliminary handling, and diseases of grass carp in New Zealand. Journal of Marine and Freshwater Research 8(3), 441–454.CrossRefGoogle Scholar
García-Prieto, L and Osorio-Sarabia, D (1991) Distribución actual de Bothriocephalus acheilognathi en México. In: Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico. Serie Zoologia 62, 523–526.Google Scholar
Guindon, S, Dufayard, J-F, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59(3), 307–321.CrossRefGoogle ScholarPubMed
Güven, A and Öztürk, T (2018) Metazoan parasite faunas of three Gobiid species (Actinopterygii: Gobiidae) inhabiting the lower Kızılırmak Delta in Samsun: a comparative study. Turkiye Parazitoloji Dergisi 42(1), 33–38.CrossRefGoogle ScholarPubMed
Hadziavdic, K, Lekang, K, Lanzen, A, Jonassen, I, Thompson, EM and Troedsson, C (2014) Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS One 9, e87624.CrossRefGoogle ScholarPubMed
Hansen, SP, Choudhury, A, Heisey, D, Ahumada, J, Hoffnagle, T and Cole, R (2006) Experimental infection of the endangered bonytail chub (Gila elegans) with the Asian fish tapeworm (Bothriocephalus acheilognathi): impacts on survival, growth, and condition. Canadian Journal of Zoology 84(10), 1383–1394.CrossRefGoogle Scholar
Han, JE, Shin, SP, Kim, JH, Choresca, CH Jr, Jun, JW, Gomez, DK, et al. (2010) Mortality of cultured koi Cyprinus carpio in Korea caused by Bothriocephalus acheilognathi. African Journal of Microbiology Research 4(7), 543–546.Google Scholar
Hassan, M, Beatty, S, Morgan, D, Doupé, R and Lymbery, A (2008) An introduced parasite, Lernaea cyprinacea L., found on native freshwater fishes in the south west of Western Australia. Journal of the Royal Society of Western Australia 91(2), 149–153.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8), 754–755.CrossRefGoogle ScholarPubMed
İnnal, D, Aydogdu, A and Guclu, SS (2016) Invasion of Bothriocephalus acheilognathi (Cestoda: Pseudophyllidea) in Turkey. Acta Biologica Turcica 29(1), 20–25.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, et al. (2012) Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647–1649.CrossRefGoogle ScholarPubMed
Kilian, JV, Klauda, RJ, Widman, S, Kashiwagi, M, Bourquin, R, Weglein, S, et al. (2012) An assessment of a bait industry and angler behavior as a vector of invasive species. Biological Invasions 14(7), 1469–1481.CrossRefGoogle Scholar
Košuthová, L, Šmiga, Ľ, Oros, M, Barčák, D and Košuth, P (2015) The pathogenic Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in the Red discus (Symphysodon discus). Helminthologia 52(3), 52287–52292.CrossRefGoogle Scholar
Kuchta, R, Choudhury, A and Scholz, T (2018) Asian fish tapeworm: the most successful invasive parasite in freshwaters. Trends in Parasitolology 34(6), 511–523.CrossRefGoogle ScholarPubMed
Liao, HH and Shih, LCh (1956) Contribution to the biology and control of Bothriocephalus gowkongensis Yeh, a tapeworm parasitic in the young grass carp (Ctenopharyngodon idellus). Acta Hydrobiologica Sinica 7(1), 182–185.Google Scholar
Luo, H, Nie, P, Zhang, Y, Wang, G and Yao, W (2002) Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Systematic Parasitology 52(3), 159–166.CrossRefGoogle ScholarPubMed
Lymbery, AJ, Morine, M, Kanani, HG, Beatty, SJ and Morgan, DL (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 392, 171–177.Google Scholar
Lymbery, AJ, Lymbery, SJ and Beatty, SJ (2020) Fish out of water: aquatic parasites in a drying world. International Journal for Parasitology: Parasites and Wildlife 12, 300–307.Google Scholar
Matey, VE, Ervin, EL and Hovey, TE (2015) Asian fish tapeworm (Bothriocephalus acheilognathi) infecting a wild population of convict cichlid (Archocentrus nigrofasciatus) in Southwestern California. Bulletin of the Southern California Academy of Sciences 114(2), 89–97.Google Scholar
McAllister, CT, Bursey, CR, Robison, HW, Connior, MB and Trauth, SE (2017) New records of helminth parasites (Trematoda, Cestoda, Nematoda) from fishes in the Arkansas and Red River Drainages, Oklahoma. Proceedings of the Oklahoma Academy of Science 96, 2017.Google Scholar
Morgan, DL (2003) Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda). Environmental Biology of Fishes 66, 155–167.CrossRefGoogle Scholar
Morgan, L and Buttemer, W (1996) Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentata tadpoles. Australian Journal of Zoology 30(2), 143–149.CrossRefGoogle Scholar
Morgan, DL, Unmack, PJ, Beatty, SJ, Ebner, BC, Allen, MG, Keleher, J, et al. (2014) An overview of the ‘freshwater fishes’ of Western Australia. Journal of the Royal Society of Western Australia 97, 263–278.Google Scholar
Mulokozi, DP, Mmanda, FP, Onyango, P, Lundh, T, Tamatamah, R and Berg, H (2020) Rural culture: assessment of its contribution to household income and farmers’ perception in selected districts, Tanzania. Tanzania Aquacultural Economic Management 24(4), 387–405.CrossRefGoogle Scholar
Myers, N, Mittermeier, RA, Mittermeier, CG, Da Fonseca, GA and Kent, J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772), 853–858.CrossRefGoogle ScholarPubMed
Nickrent, DL and Sargent, ML (1991) An overview of the secondary structure of the V4 region of eukaryotic small-subunit ribosomal RNA. Nucleic Acids Research 19(2), 227–235.CrossRefGoogle ScholarPubMed
Olden, JD, Kennard, MJ and Pusey, BJ (2008) Species invasions and the changing biogeography of Australian freshwater fishes. Global Ecology and Biogeography 17(1), 25–37.Google Scholar
Olsen, RL and Hasan, MR (2012) A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends in Food Science & Technology 27(2), 120–128.CrossRefGoogle Scholar
Oros, M, Barčák, D, Bazsalovicsová, E and Hanzelová, V (2015) Asian fish tapeworm, Khawia japonensis (Yamaguti, 1934), has expanded its European invasive range. Parasitology Research 114(5), 2035–2039.CrossRefGoogle Scholar
Ozturk, M, Aydogdu, A and Dogan, I (2002) The occurrence of helminth fauna in sand goby (Gobius fluviatilis, Pallas, 1811) from lake Uluabat, Turkey. Acta Veterinaria 52(5–6), 381–391.Google Scholar
Pool, D, Ryder, K and Andrews, C (1984) The control of Bothriocephalus acheilognathi in grass carp, Ctenopharyngodon idella, using praziquantel. Aquaculture Research 15(1), 31–33.CrossRefGoogle Scholar
Prigli, M (1975) The role of aquatic birds in spreading Bothriocephalus gowkongensis Yeh, 1955 (Cestoda). Parasitology Hungary 8, 61–62.Google Scholar
Rahaman, S, Sabbir, W, Sarder, L, Biswas, S and Ghosh, A (2012) Induced breeding, embryonic and larval development of Koi carp (Cyprinus carpio) in Khulna, Bangladesh. Mesopotamian Journal of Marine Science 27(1), 1–14.Google Scholar
Reiczigel, J, Marozzi, M, Fábián, I and Rózsa, L (2019) Biostatistics for parasitologists–a primer to quantitative parasitology. Trends in Parasitology 35(4), 277–281.Google ScholarPubMed
Reynolds, SJ (2009) Impact of the introduced poeciliid Gambusia holbrooki on amphibians in southwestern Australia. Copeia 2009(2), 296–302.CrossRefGoogle Scholar
Rochat, E, Blasco-Costa, I, Scholz, T and Unmack, P (2020) High diversity of metazoan parasites in carp gudgeons (Eleotridae: Hypseleotris spp.) from Eastern Australia. Journal of Helminthology 94, e146.CrossRefGoogle ScholarPubMed
Salgado-Maldonado, G and Pineda-López, RF (2003) The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions 5(3), 261–268.CrossRefGoogle Scholar
Salgado-Maldonado, G, Matamoros, WA, Kreiser, BR, Caspeta-Mandujano, JM and Mendoza-Franco, EF (2015) First record of the invasive Asian fish tapeworm Bothriocephalus acheilognathi in Honduras, Central America. Parasite 22(5), 1–6.CrossRefGoogle ScholarPubMed
Sara, B, Barour, C, Sameh, A, Boualleg, C and Mourad, B (2016) Environmental parameters and parasitism in common carp (Cyprinus carpio Linnaeus, 1758) caught from Oubeira Lake (north-east of Algeria). Research Journal of Fisheries and Hydrobiology 11, 1816–9112.Google Scholar
Schäperclaus, W, Kulow, H and Schreckenbach, K (1991) Fish diseases. New Delhi, Amerind Publishing Company Pvt. Ltd.Google Scholar
Scholz, T (1997) A revision of the species of Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) parasitic in American freshwater fishes. Systematic Parasitology 36(2), 85–107.CrossRefGoogle Scholar
Scholz, T (1999) Parasites in cultured and feral fish. Veterinary Parasitology 84(3–4), 317–335.CrossRefGoogle ScholarPubMed
Scholz, T, Škeříková, A, Hanzelová, V, Koubková, B and Baruš, V (2003) Resurrection of Proteocephalus sagittus (Grimm, 1872) (Cestoda: Proteocephalidea) based on morphological and molecular data. Systematic Parasitology 56(3), 173–181.CrossRefGoogle ScholarPubMed
Scott, AL and Grizzle, JM (1979) Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yea, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases 2(1), 69–73.CrossRefGoogle Scholar
Shelton, WL and Rothbard, S (2006) Exotic species in global aquaculture-A review. Israeli Journal of Aquaculture – Bamidgeh 58(1), 3–28.Google Scholar
Škerıková, A, Hypša, V and Scholz, T (2004) A paraphyly of the genus Bothriocephalus Blanchard, 1852 (Cestoda: Pseudophyllidea) inferred from ITS2 and partial 18S rDNA sequences. Journal of Parasitology 90, 612–617.Google Scholar
Tacon, AG and Metian, M (2013) Fish matters: importance of aquatic foods in human nutrition and global food supply. Reviews in Fisheries Science 21(1), 22–38.CrossRefGoogle Scholar
Xi, B, Li, W, Wang, G, Nie, P and Xie, J (2016) Cryptic genetic diversity and host specificity of Bothriocephalus acheilognathi Yamaguti, 1934 (Eucestoda: Bothriocephalidea). 动物分类学报 41(2), 140–148.Google Scholar
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Applied Entomology and Zoology 6(1), 1–112.Google Scholar
Yang, R, Murphy, C, Yong, S, Ng-Hublin, J, Estscourt, A, Hijjawi, N, et al. (2013) Specific and quantitative detection and identification of Cryptosporidium hominis and C. parvum in clinical and environmental samples. Experimental Parasitology 135(1), 142–147.CrossRefGoogle Scholar
Yera, H, Kuchta, R, Brabec, J, Peyron, F and Dupouy-Camet, J (2013) First identification of eggs of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in human stool. Parasitology International 62(3), 268–271.CrossRefGoogle Scholar
Zhokhov, A, Pugacheva, M, Molodozhnikova, N and Berechikidze, I (2019) Alien parasite Species of the fish in the Volga River Basin: a review of data on the species number and distribution. Russian Journal of Biological Invasions 10(2), 136–152.CrossRefGoogle Scholar
Supplementary material: File

Palermo et al. supplementary material

Appendix

Download Palermo et al. supplementary material(File)
File 26 KB