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Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico

Published online by Cambridge University Press:  22 May 2017

G. Pérez-Ponce de León*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, A. P. 70-153, C.P. 04510, México D.F., México
O. Lagunas-Calvo
Affiliation:
Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México
L. García-Prieto
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, A. P. 70-153, C.P. 04510, México D.F., México
R. Briosio-Aguilar
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, A. P. 70-153, C.P. 04510, México D.F., México Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México
R. Aguilar-Aguilar
Affiliation:
Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México
*

Abstract

The Asian fish tapeworm, Schyzocotyle acheilognathi (syn. Bothriocephalus acheilognathi) represents a threat to freshwater fish, mainly cyprinids, across the globe. This tapeworm possesses an extraordinary ability to adapt to different environmental conditions and, because of that, from its natural geographical origin in mainland Asia, it has colonized every continent except Antarctica. It is thought that this pathogenic tapeworm was first co-introduced into Mexico in 1965 from China, with the grass carp Ctenopharyngodon idella, although the first formal record of its presence was published in 1981. Over the past 35 years, the Asian fish tapeworm has invaded about 22% of the freshwater fish in Mexico. Because fish communities in Mexico are characterized by high species richness and levels of endemism, S. acheilognathi is considered as a co-introduced and co-invasive species. In this review, we update the geographic distribution and host spectrum of the Asian fish tapeworm in Mexico. Up until December 2016, the tapeworm had been recorded in 110 freshwater fish species (96 native and 14 introduced), included in 51 genera, 11 families and 4 orders; it was also widely distributed in all types of aquatic environments, and has been found in 214 localities. We present novel data from a survey aimed at establishing the distribution pattern of the tapeworm in native freshwater fishes of two rivers in north-central Mexico, and the genetic variation among individuals of this co-invasive species collected from different host species and localities. We discuss briefly the factors that have determined the remarkable invasive success of this parasite in freshwater systems in Mexico.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Bowles, J., Blair, D. & McManus, D.P. (1992) Genetic variants within the genus Echinococcus identified by mitochondrial sequencing. Molecular and Biochemical Parasitology 54, 165217.Google Scholar
Brabec, J., Waeschenbach, A., Scholz, T., Littlewood, D.T.J. & Kuchta, R. (2015) Molecular phylogeny of the Bothriocephalidea (Cestoda): molecular data challenge morphological classification. International Journal for Parasitology 45, 761771.CrossRefGoogle ScholarPubMed
Brabec, J., Kuchta, R., Scholz, T. & Littlewood, D.T.J. (2016) Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data. International Journal for Parasitology 46, 555562.CrossRefGoogle ScholarPubMed
Bunkley-Williams, L. & Williams, E.H. (1994) Parasites of Puerto Rican freshwater sport fishes. 164 pp. San Juan and Mayaguez, Puerto Rico, Department of Natural and Environmental Resources and Department of Marine Sciences, University of Puerto Rico.Google Scholar
Choudhury, A. & Cole, R.A. (2012) Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). pp. 385400 in Francis, R.A. (Ed.) A handbook of global freshwater invasive species. London, UK, Earthscan.Google Scholar
Choudhury, A., Hoffnagle, T.L. & Cole, R.A. (2004) Parasites of native and non-native fishes in the Little Colorado River, Grand Canyon, Ariizona. Journal of Parasitology 90, 10421052.Google Scholar
Choudhury, A., Charipar, E., Nelson, P., Hodgson, J. R., Bonar, S. & Cole, R. A. (2006) Update on the distribution of the invasive Asian fish tapeworm, Bothriocephalus acheilognathi, in the US and Canada. Comparative Parasitology 73, 269273.Google Scholar
Choudhury, A., Zheng, S., Perez-Ponce de León, G., Martínez-Aquino, A., Brosseau, C. & Gale, E. (2013) The invasive Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in the Chagres River/Panama Canal drainage, Panama. Bioinvasions Records 2, 99104.Google Scholar
Choudhury, A., García-Varela, M. & Pérez-Ponce de León, G. (2017) Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far? Journal of Helminthology 91, 174196.CrossRefGoogle ScholarPubMed
Cole, R.A. & Choudhury, A. (2016) Invasive species compendium: Bothriocephalus acheilognathi. Available at http://www.cabi.org/isc/datasheet/91669 (accessed 10 January 2017).Google Scholar
Dove, A.D.M. & Fletcher, A.S. (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. Journal of Helminthology 74, 121127.Google Scholar
Dunn, A.M. (2009) Parasites and biological invasions. Advances in Parasitology 68, 161184.CrossRefGoogle ScholarPubMed
Espinosa-Pérez, H. (2014) Biodiversidad de peces en México. Revista Mexicana de Biodiversidad 85, S450S459.CrossRefGoogle Scholar
Font, W.F. (1997) Distribution of helminth parasites of native and introduced stream fishes in Hawaii. Bishop Museum Occasional Papers 49, 5662.Google Scholar
Font, W.F. (1998) Parasites in paradise: patterns of helminth distribution in Hawaiian stream fish. Journal of Helminthology 72, 307311.Google Scholar
Font, W.F. & Tate, D.F. (1994) Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. Journal of Parasitology 80, 682688.Google Scholar
García-Prieto, L. & Osorio-Sarabia, D. (1991) Distribución actual de Bothriocephalus acheilognathi en México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 62, 523526.Google Scholar
Gillis, N.K., Walters, L.J., Fernandes, F.C. & Hoffman, E.A. (2009) Higher genetic diversity in introduced than in native populations of the mussel Mytella charruana: evidence of population admixture at introduction sites. Diversity and Distributions 15, 784795.CrossRefGoogle Scholar
Hillis, D.M., Mable, B.K. & Moritz, C. (1996) Nucleic acids IV: Sequencing and cloning. pp. 321383 in Hillis, D.H., Moritz, C. & Mable, B.K. (Eds) Molecular systematics. Sunderland, Massachusetts, Sinauer.Google Scholar
Hoffman, G.L. (1999) Parasites of North American freshwater fishes. 2nd edn. 539 pp. Ithaca, New Constock Publishing Associates, Cornell University Press.Google Scholar
Kuchta, R. & Scholz, T. (2007) Diversity and distribution of fish tapeworms of the ‘Bothriocephalidea’ (Eucestoda). Parassitologia 49, 2138.Google Scholar
Lira-Guerrero, G., García-Prieto, L. & Pérez-Ponce de León, G. (2008) Helminth parasites of atherinopsid freshwater fishes (Osteichthyes: Atheriniformes) from central Mexico. Revista Mexicana de Biodiversidad 79, 325331.Google Scholar
López-Jiménez, S. (1981) Céstodos de peces I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae). Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 51, 6984.Google Scholar
Luo, H.Y., Nie, P., Zhang, Y.A., Wang, G.T. & Yao, W.J. (2002) Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Systematic Parasitology 52, 159166.CrossRefGoogle ScholarPubMed
Luton, K., Walker, D. & Blair, D. (1992) Comparison of ribosomal internal transcribed spacer from two congeneric species of flukes (Plathyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323328.Google Scholar
Lymbery, A.J., Morine, M., Kanani, H.G., Beatty, S.J. & Morgan, D.L. (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology. Parasites Wildlife 3, 171177.CrossRefGoogle ScholarPubMed
Marcogliese, D.J., Gendron, A.D., Forest, J.H., Li, W., Boyce, K., El-Shehabi, F., Drake, D.A., Mandrak, N.E., Sherry, J. & McLaughlin, J.D. (2016) Range expansion and molecular confirmation of the Asian fish tapeworm in the lower Great Lakes and St. Lawrence River with notes on infections in baitfish. Journal of Great Lakes Research 42, 819828.Google Scholar
Martínez-Aquino, A., Mendoza-Palmero, C., Aguilar-Aguilar, R. & Pérez-Ponce de León, G. (2014) Checklist of helminth parasites of Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae), an endemic subfamily of freshwater fishes from Mexico. Zootaxa 3856, 151191.Google Scholar
Martínez-Meyer, E., Sosa-Escalante, J. & Álvarez, F. (2014) El estudio de la biodiversidad en México: ¿una ruta con dirección?. Revista Mexicana de Biodiversidad Suppl. 85, S1S9.CrossRefGoogle Scholar
McAllister, C.T., Bursey, C.R., Fayton, T.J., Connior, M.B. & Robison, H.W. (2016) First report of the Asian fish tapeworm, Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea:Bothriocephalidae) from Oklahoma with new host records in non hatchery fishes in Arkansas. Proceedings of the Oklahoma Academy of Sciences 95, 3541.Google Scholar
Miller, R.R., Mincley, W.L. & Norris, S.M. (2005) Freshwater fishes of México. 652 pp. Chicago, The University of Chicago Press.Google Scholar
Pérez-Ponce de León, G. & Choudhury, A. (2010) Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country. Journal of Parasitology 96, 236244.CrossRefGoogle Scholar
Pérez-Ponce de León, G., Rosas-Valdez, R., Mendoza-Garfias, B., Aguilar-Aguilar, R., Falcón-Ordaz, J., Garrido-Olvera, L. & Pérez-Rodríguez, R. (2009) Survey of the endohelminth parasites of freshwater fish in the upper Mezquital River Basin, Durango State, Mexico. Zootaxa 2164, 120.Google Scholar
Pérez-Ponce de León, G., Rosas-Valdez, R., Aguilar-Aguilar, R., Mendoza-Garfias, B., Mendoza-Palmero, C., García-Prieto, L., Rojas-Sánchez, A., Briosio-Aguilar, R., Pérez-Rodríguez, R. & Domínguez-Domínguez, O. (2010) Helminth parasites of freshwater fishes in the Nazas River Basin, Northern Mexico. CheckList 6, 2635.CrossRefGoogle Scholar
Pérez-Ponce de León, G., García-Prieto, L. & Mendoza-Garfias, B. (2011) Describing parasite biodiversity: the case of the helminth fauna of wildlife vertebrates in Mexico. pp. 3354 in Grillo, O. & Venora, G. (Eds) Changing diversity in changing environment. Croacia, InTech.Google Scholar
Pérez-Ponce de León, G., Mendoza-Garfias, B., Rosas-Valdez, R. & Choudhury, A. (2013) New host and locality records of freshwater fish helminth parasites in river basins north of the Transmexican Volcanic Belt: another look at biogeographical patterns. Revista Mexicana de Biodiversidad 84, 556562.Google Scholar
Pinacho-Pinacho, C.D., García-Varela, M., Hernández-Orts, J., Mendoza-Palmero, C., Sereno-Uribe, A., Martínez-Ramírez, E., Andrade-Gómez, L., López-Jiménez, A., Hernéndez-Cruz, E. & Pérez-Ponce de León, G. (2015) Checklist of the helminth parasites of the genus Profundulus Hubbs, 1924 (Cyprinodontiformes, Profundulidae), an endemic family of freshwater fishes in Middle-America. Zookeys 523, 130.Google Scholar
Rojas-Sánchez, A. & García-Prieto, L. (2008) Distribución actual del céstodo Bothriocephalus acheilognathi en México. Memorias XXV Simposio sobre Fauna Silvestre. pp. 8993. México, Universidad Nacional Autónoma de México.Google Scholar
Rosas-Valdez, R. & Pérez-Ponce de León, G. (2008) Composición taxonómica de los helmintos parásitos de ictalúridos y heptaptéridos (Osteychthyes: Siluriformes) de México, con una hipótesis de homología biogeográfica primaria. Revista Mexicana de Biodiversidad 79, 473499.Google Scholar
Salgado-Maldonado, G. & Pineda-López, R. (2003) The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions 5, 261268.Google Scholar
Salgado-Maldonado, G. & Rubio-Godoy, M. (2014) Helmintos parásitos de peces de agua dulce introducidos. pp. 269285 in Mendoza, R. & Koleff, P. (Eds) Especies acuáticas invasoras en México. Mexico City, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.Google Scholar
Salgado-Maldonado, G., Matamoros, W.A., Kreiser, B.R., Caspeta-Mandujano, J.M. & Mendoza-Franco, E.F. (2015) First record of the invasive Asian fish tapeworm Bothriocephalus acheilognathi in Honduras, Central America. Parasite 22, 5.Google Scholar
Scholz, T. (1997) A revision of the species of Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) parasitic in American freshwater fishes. Systematic Parasitology 36, 85107.Google Scholar
Scholz, T., Vargas-Vazquez, J. & Moravec, F. (1996) Bothriocepahlus pearsei n. sp. from cenote fishes of the Yucatan Peninsula, Mexico. Journal of Parasitology 82, 801805.CrossRefGoogle Scholar
Scholz, T., Kuchta, R. & Williams, C. (2012) Bothriocephalus acheilognathi. pp. 282297 in Woo, P.T. & Buchmann, K. (Eds) Fish parasites: pathobiology and protection. Wallingford, UK, CABI.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology Evolution 30, 27252729.Google Scholar
Vidal-Martínez, V., Aguirre-Macedo, L., Scholz, T., González-Solís, D. & Mendoza-Franco, E. (2001) Atlas of helminth parasites of cichlid fishes of Mexico. 165 pp. Prague, Academia (Academy of Sciences of the Czech Republic).Google Scholar
Vincent, A.G. & Font, W. (2003) Host specificity and population structure of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi, parasitizing exotic fishes in Waianu stream, O'Ahu, Hawai'i. Journal of Parasitology 89, 540544.Google Scholar
Waicheim, A., Blasetti, G., Cordero, P., Rauque, C. & Viozzi, G. (2014) Macroparasites of the invasive fish, Cyprinus carpio, in Patagonia, Argentina. Comparative Parasitology 81, 270275.CrossRefGoogle Scholar
Whitney, K.D. & Gabler, C.A. (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions 14, 569580.Google Scholar
Yamaguti, S. (1934) Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Zoology 6, 112.Google Scholar
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