Use of Acanthobothrium spp. (batoid parasites) as a possible bioindicators of contamination in México

Authors

  • Erick Rodríguez-Ibarra Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo
  • Pablo Octavio-Aguilar Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo
  • Scott Monks Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo
  • Juan Violante-González Unidad Académica de Ecología Marina, Universidad Autónoma de Guerrero,
  • Griselda Pulido-Flores Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo,

DOI:

https://doi.org/10.47808/revistabioagro.v12i1.556

Keywords:

loss of biodiversity, prevalence, cestoda, principal coordinate analysis

Abstract

Parasites are a component of biodiversity, which are also affected by changes in the environment or their hosts. Therefore, it is considered that Acanthobothrium spp. can be a bioindicator of some threats in the coasts of Mexico. These cestodes have indirect life cycles, and are intestinal parasites of elasmobranchs. Data from 21 years of collection of Acanthobothrium spp. parasites of some batoid species in different localities and dates along the coast of Mexico were analyzed. Prevalence was calculated, and a principal coordinates analysis was performed, considering a non-linear multimetric distance (seasonality of collections (rainy and dry seasons), localities and years of collections) to evaluate a probable correlation between the absence or presence of Acanthobothrium spp. During the period evaluated, there was a decrease in the biodiversity of Acanthobothrium in the Gulf of Mexico, with low values of prevalence of the populations of these parasites. This is interpreted as an effect of the sensitivity of Acanthobothrium spp. to environmental changes. The life cycles of Acanthobothrium spp. can be affected directly or indirectly by contaminants, either in free-living larvae, or in parasitic larvae and/or adults of intermediate or definitive hosts.  Therefore, it is concluded that increased pollution in the Gulf of Mexico affects the prevalence values of Acanthobothrium spp. This highlights the importance of the use of parasites as bioindicators of environmental quality.

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References

Anantaraman, S., 1963. Larval cestodes in marine invertebrates and fishes with a discussion of the life cycles of the Tetraphyllidea and the Trypanorhyncha. Parasitology Research 23, pp. 309–314. https://doi.org/10.1007/BF00331227 DOI: https://doi.org/10.1007/BF00331227

Bautista-Hernández, C. E., S. Monks, G. Pulido-Flores y A. E. Rodríguez-Ibarra, 2015. Revisión bibliográfica de algunos términos ecológicos usados en parasitología, y su aplicación en estudios de caso. Estudios en biodiversidad, 1(1), 11-19.

Benitez, J. A., R. M. Cerón-Bretón, J. G. Cerón-Bretón y J. Rendón-Von-Osten, 2014. The environmental impact of human activities on the Mexican coast of the Gulf of Mexico: review of status and trends. WIT Transactions on Ecology and the Environment 181, pp. 37–50. https://doi.org/10.2495/EID140041 DOI: https://doi.org/10.2495/EID140041

Bennett, J., F. Jorge, R. Poulin y H. S. Randhawa, 2019. Revealing trophic transmission pathways of marine tapeworms. Parasitology Research 118(1), pp. 1435–1444. https://doi.org/10.1007/s00436-019-06264-3 DOI: https://doi.org/10.1007/s00436-019-06264-3

Burger, J., 2006. Bioindicators: types, development, and use in ecological assessment and research. Environmental Bioindicators 1 (1), pp. 22-39. https://doi.org/10.1080/15555270590966483 DOI: https://doi.org/10.1080/15555270590966483

Caira, J. N., 2011. Synergy advances parasite taxonomy and systematics: an example from elasmobranch tapeworms. Parasitology 138, pp. 1675–1687. https://doi.org/10.1017/S0031182011000643 DOI: https://doi.org/10.1017/S0031182011000643

Caira, J. N., K. Jensen y V. A. Ivanov, 2017. Onchoproteocephalidea II. In: J.N. Caira, Ed. Planetary biodiversity inventory (2008–2017): Tapeworms from vertebrate bowels of the earth. University of Kansas, Natural History Museum, Special Publication No. 25. Lawrence, Kansas, USA, pp. 290–315.

Cake, E. W. K., 1977. Larval Cestode Parasites of Edible Mollusks of the Northeastern Gulf of Mexico. Gulf Research Reports 6 (1): 1-8. DOI: https://doi.org/10.18785/grr.0601.01 DOI: https://doi.org/10.18785/grr.0601.01

Campbell, R. A., 1969. New Species of Acanthobothrium (Cestoda: Tetraphyllidea) from Chesapeake Bay, Virginia. The Journal of Parasitology. 55(3): 559-570. https://doi.org/10.2307/3277298 DOI: https://doi.org/10.2307/3277298

Campbell R. A., 1970. Notes on tetraphyllidean cestodes from the Atlantic Coast of North America, with descriptions of two new species. Journal of Parasitology 56: 498–508. https://doi.org/10.2307/3277613 DOI: https://doi.org/10.2307/3277613

Chambers, C. B., T. H. Cribb y M. K. Jones, 2000. Tetraphyllidea metacestodes of teleosts of the Great Barrier Reef, and the use of in vitro cultivation to identify them. Folia Parasitologica 47 (4), pp. 285-292. https://doi.org/10.14411/fp.2000.050 DOI: https://doi.org/10.14411/fp.2000.050

Cone, D. K., D. J. Marcogliese y W. D. Watt, 1993. Metazoan parasite communities of yellow eels (Anguilla rostrata) in acidic and limed rivers of Nova Scotia. Canadian Journal of Zoology, 71(1), pp. 177-184. https://doi.org/10.1139/z93-024 DOI: https://doi.org/10.1139/z93-024

Dulvy, N. K., S. L. Fowler, J. A. Musick, R. D. Cavanagh, P. M. Kyne, L. R. Harrison, et al. y W. T. White, 2014. Extinction risk and conservation of the world’s sharks and rays. eLIFE, 3, e00590. https://doi.org/10.7554/eLife.00590 DOI: https://doi.org/10.7554/eLife.00590

Dulvy, N. K., N. Pacoureau, C. L. Rigby, R. A. Pollom, R. W. Jabado, D. A. Ebert, et al. y C. A. Simpfendorfer, 2021. Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology, 31(21), pp. 4773-4787. https://doi.org/10.1016/j.cub.2021.08.062 DOI: https://doi.org/10.1016/j.cub.2021.08.062

Franzese, S. y V. A. Ivanov, 2018. Hyperapolytic species of Acanthobothrium (Cestoda: Onchoproteocephalidea) from batoids off Argentina. Parasitology International 67(4), pp. 431–443. https://doi.org/10.1016/j.parint.2018.04.001 DOI: https://doi.org/10.1016/j.parint.2018.04.001

Godínez-Campos, O. 2012. Metales pesados en Neritina reclivata Say, 1822 (Mollusca: Gastropoda) en la Laguna de Tampamachoco, Tesis de Maestría. Facultad de Ciencias Biológicas y Agropecuarias Universidad Veracruzana. Veracruz, México 66 pp.

Goldstein, R. J., 1964. Species of Acanthobothrium (Cestoda: Tetraphyllidea) from the Gulf of Mexico. The Journal of Parasitology. 50(5): 656. https://doi.org/10.2307/3276123 DOI: https://doi.org/10.2307/3276123

Goldstein, R. J., R. N. Henson y F. G. Schlicht, 1968. Acanthobothrium lintoni sp. n. (Cestoda: Tetraphyllidea) from the electric ray, Narcine brasiliensis (Olfers) in the Gulf of Mexico. Zoologischer Anzeiger, 181, 435–438.

Hammer, Ø., D. A. T. Harper y P. D. Ryan, 2001. PAST v. 2.17c. Palaeontologia Electronica 4 (1), pp. 1–229.

Halpern, B. S., M. Frazier, J. Afflerbach, J. S. Lowndes, F. Micheli, C. O’Hara, C. Scarborough y K. A. Selkoe, 2019. Recent pace of change in human impact on the world’s ocean. Scientific reports, 9(1), pp. 1-8. https://doi.org/10.1038/s41598-019-47201-9. DOI: https://doi.org/10.1038/s41598-019-47201-9

Heink, U. y I. Kowarik, 2010. What are indicators? On the definition of indicators in ecology and environmental planning. Ecological Indicators 10 (3), 584–593. https://doi.org/10.1016/j.ecolind.2009.09.009 DOI: https://doi.org/10.1016/j.ecolind.2009.09.009

Hyman, L. H., 1951. The Invertebrates: Acanthocephala, Aschelminthes, and Entoprocta; the pseudocode-mate bilateria. Vol. III, Mc-Graw-Hill Book Company, Inc., New York, USA. Pp. 572.

Holland, N. D., T. G. Campbell, J. R. Garey, L. Z. Holland y N. G. Wilson, 2009. The Florida amphioxus (Cephalochordata) hosts larvae of the tapeworm Acanthobothrium brevissime: natural history, anatomy and taxonomic identification of the parasite. Acta Zoologica 90 (1), pp. 75–86. https://doi.org/10.1111/j.1463-6395.2008.00343.x DOI: https://doi.org/10.1111/j.1463-6395.2008.00343.x

Holland, N. D. y N. G. Wilson, 2009. Molecular identification of larvae of a tetraphyllidean tapeworm (Platyhelminthes: Eucestoda) in a razor clam as an alternative intermediate host in the life cycle of Acanthobothrium brevissime. The Journal of Parasitology 95 (5), pp. 1215–1217. https://doi.org/10.1645/ge-1946.1 DOI: https://doi.org/10.1645/GE-1946.1

Jefferson, T., M. J. Costello, Q. Zhao y C. J. Lundquist, 2021. Conserving threatened marine species and biodiversity requires 40% ocean protection. Biological Conservation, 264, 109368. https://doi.org/10.1016/j.biocon.2021.109368 DOI: https://doi.org/10.1016/j.biocon.2021.109368

Linton, E., 1908. IX. Helminth fauna of the Dry Tortugas. I. Cestodes. Papers from the Tortugas Laboratory of the Carnegie Institution of Washington. Publication No. 102, 1: 157–190.

Lozada-Flores, O. 2015. Presencia de metales pesados en Isognomon alatus (Gmelin, 1791) de la Laguna Tampamachoco, Veracruz. Tesis de Maestría. Facultad de Ciencias Biológicas y Agropecuarias, Universidad Veracruzana. Veracruz, México, 104 pp.

Mackenzie, K., 1999. Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38 (11), pp. 955–959. https://doi.org/10.1016/s0025-326x(99)00100-9 DOI: https://doi.org/10.1016/S0025-326X(99)00100-9

MacKenzie, K., 2002. Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124 (07), pp. 153–163. https://doi.org/10.1017/S0031182002001518 DOI: https://doi.org/10.1017/S0031182002001518

MacNeil, M. A., D. D. Chapman, M. Heupel et al. (2020). Global status and conservation potential of reef sharks. Nature 583, pp. 801–806. https://doi.org/10.1038/s41586-020-2519-y DOI: https://doi.org/10.1038/s41586-020-2519-y

Marcogliese, D. J., 2004. Parasites: small players with crucial Roles in the ecological theater. EcoHealth 1 (2), pp. 151–164. https://doi.org/10.1007/s10393-004-0028-3 DOI: https://doi.org/10.1007/s10393-004-0028-3

Monks, S., G. Pulido-Flores, C. E. Bautista-Hernández, B. Alemán-García, J. Falcón-Ordaz y J. C. Gaytán-Oyarzún, 2013. El uso de helmintos parásitos como bioindicadores en la evaluación de la calidad del agua: Lago de Tecocomulco vs. Laguna de Metztitlán, Hidalgo, México. In: G. Pulido-Flores and S. Monks, eds. Estudios científicos en el estado de Hidalgo y zonas aledañas Vol. II. Zea Books, Lincoln, Nebraska, USA, pp. 25–34.

Monks S., G. Pulido-Flores, M. Lara-Sánchez, 2015. Distribution extension of Acanthobothrium cartagenensis Brooks & Mayes, 1980 (Tetraphyllidea: Onchobothriidae) in Urobatis jamaicensis (Cuvier, 1816) (Myliobatiformes: Urotrygonidae) from Quintana Roo, México. Check List 11(4): 1707. https://doi.org/10.15560/11.4.1707 DOI: https://doi.org/10.15560/11.4.1707

Oliver, S., M. Braccini, S. J. Newman y E. S. Harvey, 2015. Global patterns in the bycatch of sharks and rays. Marine Policy, 54, pp. 86-97. DOI: https://doi.org/10.1016/j.marpol.2014.12.017

Overstreet, R. M., 1997. Parasitological data as monitors of environmental health. Parassitologia 39 (3), pp. 169–175.

Pietrock, M. y D. J. Marcogliese, 2003. Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19(7), pp. 293–299. https://doi.org/10.1016/s1471-4922(03)00117-x DOI: https://doi.org/10.1016/S1471-4922(03)00117-X

Poulin, R., 1992. Toxic pollution and parasitism in freshwater fish. Parasitology Today 8 (2), pp. 58-61. https://doi.org/10.1016/0169-4758(92)90090-o DOI: https://doi.org/10.1016/0169-4758(92)90090-O

Pulido-Flores, G., S. Monks y A. J. Gordillo-Martínez, 2005. Monitoreo de bajo costo en la evaluación de la calidad ambiental. Revista Internacional de Ciencias Ambientales, 21(Suppl. 1), 578-583.

Rodríguez-Ibarra, A. E., 2011. Helmintos intestinales de algunos batoideos de Tamiahua y Tuxpan, Veracruz, México. Tesis de Maestría. Instituto de Ciencias Básicas e Ingeniarias, Universidad Autónoma del Estado de Hidalgo. Hidalgo, México, 114 pp.

Rodríguez-Ibarra, E., G. Pulido-Flores, J. Violante-González y S. Monks, 2018. A new species of Acanthobothrium (Eucestoda: Onchobothriidae) in Aetobatus cf. narinari (Myliobatidae) from Campeche, México. Revista Brasileira de Parasitologia Veterinária 27 (1), pp. 66-73. https://doi.org/10.1590/s1984-29612018009 DOI: https://doi.org/10.1590/s1984-29612018009

Rodríguez-Ibarra E, J. Violante-González, S. Monks, 2023. Two new species of Acanthobothrium Blanchard, 1848 (Cestoda, Onchoproteocephalidea) from Urobatis jamaicensis (Cuvier, 1816) (Elasmobranchii, Batoidea, Myliobatiformes) of the Mexican Caribbean. Zookeys, 1169:175-201. doi: 10.3897/zookeys.1169.101968. DOI: https://doi.org/10.3897/zookeys.1169.101968

Rosenthal, H., 1967. Parasites in larvae of the herring (Clupea harengus L.) fed with wild plankton. Marine Biology 1(1), 10-15. https://doi.org/10.1007/BF00346689 DOI: https://doi.org/10.1007/BF00346689

Southwell, T., 1930. Cestoda (Vol. 1). The Fauna of British India including Ceylon and Burma. Taylor and Francis, London, U.K. 391 pp.

StatSoft., 2011. STATISTICA (data analysis software system), version 10. http://www.statsoft.com. 30/08/2021

Vardo-Zalik, A. M. y R. A. Campbell, 2011. Five new species of Acanthobothrium van Beneden, 1849 (Cestoda: Tetraphyllidea) in elasmobranchs from the northwest Atlantic and Gulf of Mexico with first records from smooth-hound sharks and guitarfish. Zootaxa. 2838: 41–64. DOI: https://doi.org/10.11646/zootaxa.2838.1.3

Wardle, W. J., 1974. A survey of the occurrence, distribution and incidence of infection of helminth parasites of marine and estuarine Mollusca from Galveston, Texas. Ph.D. Thesis. Texas A & M University, College Station, Texas, USA, 303 pp.

Williams, H. H., K. MacKenzie y A. M. McCarthy, 1992. Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries 2(2), 144-176. https://doi.org/10.1007/BF00042882 DOI: https://doi.org/10.1007/BF00042882

Yamaguti, S., 1959. Systema helminthum. Vol. II. The cestodes of vertebrates. New York & London Interscience Publications, Inc, New York, USA, 860 pp.

Zaragoza-Tapia, F., G. Pulido-Flores, S. L. Gardner y S. Monks, 2020. Host relationships and geographic distribution of species of Acanthobothrium Blanchard, 1848 DOI: https://doi.org/10.3897/zookeys.940.46352.figure2

(Onchoproteocephalidea, Onchobothriidae) in elasmobranchs: a metadata analysis. ZooKeys 940, 1-49. https://doi.org/10.3897/zookeys.940.46352 DOI: https://doi.org/10.3897/zookeys.940.46352

Published

2024-06-01

How to Cite

Rodríguez-Ibarra , E., Octavio-Aguilar , P., Monks , S., Violante-González , J., & Pulido-Flores , G. (2024). Use of Acanthobothrium spp. (batoid parasites) as a possible bioindicators of contamination in México. Revista Biológico Agropecuaria Tuxpan, 12(1), 179–194. https://doi.org/10.47808/revistabioagro.v12i1.556

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Original Research Papers