Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-23T11:29:22.050Z Has data issue: false hasContentIssue false

Diversity of helminth parasites in aquatic invertebrate hosts in Latin America: how much do we know?

Published online by Cambridge University Press:  09 August 2016

M.L. Aguirre-Macedo*
Affiliation:
Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, C.P. 97310, México
A.L. May-Tec
Affiliation:
Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, C.P. 97310, México
A. Martínez-Aquino
Affiliation:
Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, C.P. 97310, México
F. Cremonte
Affiliation:
Instituto de Investigaciones de Organismos Marinos (CENPAT-CONICET), Bvd. Brown 2915, U9120ACF, Puerto Madryn, Chubut, Argentina
S.R. Martorelli
Affiliation:
CONICET – CCT, La Plata, Centro de Estudios Parasitológicos y Vectores (CEPAVE), Boulevard 120 S/N e/61 y 62 (B1902CHX) La Plata, Buenos Aires, Argentina

Abstract

Helminths in aquatic invertebrate hosts have been overlooked in comparison with vertebrate hosts. Therefore, the known diversity, ecology and distribution of these host–parasite systems are very limited in terms of their taxonomic diversity, habitat and geographic regions. In this study we examined the published literature on helminth parasites of aquatic invertebrates from Latin America and the Caribbean (LAC) to identify the state of the knowledge in the region and to identify patterns of helminth diversity. Results showed that 67% of the literature is from Argentina, Mexico and Brazil. We found records for 772 host–parasite associations. Most records relate to medically or economically important hosts. Molluscs were the most studied host group with 377 helminth records (80% trematodes). The lymnaeids and planorbids were the most studied molluscs across LAC. Arthropods were the second most studied host group with 78 helminth records (trematodes 38%, cestodes 24% and nematodes 20%), with shrimps and crabs being the most studied hosts. Host species with the largest number of helminth taxa were those with a larger sampling effort through time, usually in a small country region. No large geographical-scale studies were identified. In general, the knowledge is still too scarce to allow any zoogeographical or helminth diversity generalization, as most hosts have been studied locally and the studies on invertebrate hosts in LAC are substantially uneven among countries.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

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

Aguirre-Macedo, M.L., Simá-Álvarez, R., Román-Magaña, M.K. & Güemez-Ricalde, J.I. (2007) Parasite survey of the eastern oyster Crassostrea virginica in coastal lagoons of the Southern Gulf of Mexico. Journal of Aquatic Animal Health 19, 270279.Google Scholar
Alda, P., Bonel, N., Panei, C., Cazzaniga, N.J. & Martorelli, S.R. (2015) First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis . Acta Parasitologica 60, 791795.CrossRefGoogle ScholarPubMed
Balian, E.V., Segers, H., Lévéque, C. & Martens, K. (2008) The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595, 627637.CrossRefGoogle Scholar
Bargues, M.D. & Mas-Coma, S. (2005) Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. Journal of Helminthology 79, 257267.Google Scholar
Bower, S.M., McGladdery, S.E. & Price, I.M. (1994) Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases 4, 1199.CrossRefGoogle Scholar
Britton, J.R. & Andreou, D. (2016) Parasitism as a driver of trophic niche specialisation. Trends in Parasitology 32, 437445.Google Scholar
Bush, A.O. & Aho, J.M. (1990) Concluding remarks. pp. 321325 in Esch, G.W., Bush, A.O. & Aho, J.M. (Eds) Parasite communities: Patterns and Processes. London, Chapman & Hall.Google Scholar
Bush, A.O., Heard, R.W. & Overstreet, R.M. (1993) Intermediate hosts as source communities. Canadian Journal of Zoology – Revue Canadienne De Zoologie 71, 13581363.CrossRefGoogle Scholar
Chávez-Sánchez, M.C., Hernández-Martínez, M., Abad-Rosales, S., Fajer-Ávila, E., Montoya-Rodríguez, L. & Álvarez-Torres, P. (2002) A survey of infectious diseases and parasites of penaeid shrimp from the Gulf of Mexico. Journal of the World Aquaculture Society 33, 316329.Google Scholar
Ching, H. (1991) Lists of larval worms from marine-invertebrates of the Pacific coast of North America. Journal of the Helminthological Society of Washington 58, 5768.Google Scholar
Chubb, J.C., Ball, M.A. & Parker, G.A. (2010) Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends in Parasitology 26, 93102.Google Scholar
Combes, C. (2005) The art of being a parasite. 1st edn. 291 pp. Chicago, University of Chicago Press.Google Scholar
Correa, A.C., Escobar, J.S., Noyac, O., Velásquez, L.E., González-Ramírez, C., Hurtrez-Boussès, S. & Pointier, J. (2011) Morphological and molecular characterization of Neotropic Lymnaeidae (Gastropoda: Lymnaeoidea), vectors of fasciolosis. Infection, Genetics and Evolution 11, 19781988.Google Scholar
Cremonte, F. (2011) Enfermedades de moluscos bivalvos de interés comercial causadas por metazoos. pp. 333396 in Figueras, A. & Novoa, B. (Eds). Enfermedades de moluscos bivalvos de interés en acuicultura. Madrid, España, Fundación Observatorio Español de Acuicultura, Consejo Superior de Investigaciones Científicas, Ministerio de Medio Ambiente y Medio Rural y Marino.Google Scholar
Cremonte, F., Gilardoni, C., Pina, S., Rodrigues, P. & Ituarte, C. (2015) Revision of the family Gymnophallidae Odhner, 1905 (Digenea) based on morphological and molecular data. Parasitology International 64, 202210.Google Scholar
Cribb, T.H. (2016) Editorial: The biodiversity of trematodes of fishes. Systematic Parasitology 93, 219221.CrossRefGoogle ScholarPubMed
Cruz-Mendoza, I., Velarde, I.F.; Naranjo-García, E., Quintero-Martínez, Ma.T. & Lecumberri-López, J. (2002) Identificación taxonómica, estacionalidad y grado de infección con Fasciola hepatica de moluscos huéspedes y no huéspedes intermediarios del trematodo en el rancho. Veterinaria México 33, 189200.Google Scholar
Davies, D., Davies, C., Lauthier, J.J., Hamann, M. & Ostrowski de Núñez, M. (2015) Morphological and ITS2 molecular characterization of Ribeiroia Cercariae (Digenea: Psilostomidae) from Biomphalaria spp. (Gastropoda: Planorbidae) in Northern Argentina. Journal of Parasitology 101, 549555.CrossRefGoogle Scholar
Dunne, J.A., Lafferty, K.D., Dobson, A.P., Hechinger, R.F., Kuris, A.M., Martinez, N.D., McLaughlin, J.P., Mouritsen, K.N., Poulin, R., Reise, K., Stouffer, D.B., Thieltges, D.W., Williams, R.J. & Zander, C.D. (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biology 11, e1001579.Google Scholar
Faltýnková, A., Sures, B. & Kostadinova, A. (2016) Biodiversity of trematodes in their intermediate mollusc and fish hosts in the freshwater ecosystems of Europe. Systematic Parasitology 93, 283293.CrossRefGoogle ScholarPubMed
FAO (2014) Estado mundial de la pesca y agricultura. Oportunidades y desafíos. 253 pp. Rome, Food and Agriculture Organization.Google Scholar
Feigenbaum, D.L. (1975) Parasites of the commercial shrimp Penaeus vannamei Boone and Penaeus brasiliensis Latreille. Bulletin of Marine Science 25, 491514.Google Scholar
Flores-Barroeta, L. & Castaneyra-Olea, R. (1962) Investigaciones sobre dermatitis esquistosómica en el Lago Pátzcuaro, Michoacan, México. III. Cercaria brevicaeca, n. sp. Revista del Instituto de Salubridad y Enfermedades Tropicales 22, 7990.Google Scholar
Goater, C.P. (1993) Population biology of Meiogymnophallus minutus (Trematoda: Gymnophallidae) in cockles Cerastoderma edule from the Exe estuary, England. Journal of the Marine Biological Association of the United Kingdom 73, 163177.Google Scholar
Goater, C.P., Goss-Custard, J.D. & Kennedy, C.R. (1995). Population dynamics of two species of intestinal helminth in oystercatchers (Haematopius ostralegus). Canadian Journal of Zoology 73, 296300.Google Scholar
Goater, T.M., Goater, C.P. & Esch, G.W. (2014) Parasitisms: the diversity and ecology of animal. 2nd edn. 497 pp. Cambridge, Cambridge University Press.Google Scholar
Guillén-Hernández, S., García-Varela, M. & Pérez-Ponce De León, G. (2008) First record of Hexaglandula corynosoma (Travassos, 1915) Petrochenko, 1958 (Acanthocephala: Polymorphidae) in intermediate and definitive hosts in Mexico. Zootaxa 1873, 6168.Google Scholar
Hijmans, R.J., Guarino, L. & Mathur, P. (2012) DIVA-GIS version 7.5 manual. California, USA, University of California Davis. Manual available at http://www.diva-gis.org (accessed April 2016).Google Scholar
Hudson, P.J., Dobson, A.P. & Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381385.Google Scholar
Hugot, J.-P., Baujard, P. & Morand, S. (2001) Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3, 199208.Google Scholar
Iwagami, M., Monroy, C., Rosas, M.A., Agatsuma, Y. & Agatsuma, T. (2003) A molecular phylogeographic study based on DNA sequences from individual metacercariae of Paragonimus mexicanus from Guatemala and Ecuador. Journal of Helminthology 77, 3338.Google Scholar
Jensen, K. (2009) Cestoda (Platyhelminthes) of the Gulf of Mexico. pp. 487522 in Tunnell, J.W. Jr, Felder, D.L. & Earle, S.A. (Eds) Gulf of Mexico origin, waters and biota, volume 1, Biodiversity. College Station, Texas, Texas A&M University Press.Google Scholar
Jörger, K.M. & Schördl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology 10, 127.Google Scholar
Karanovic, T., Djurakic, M. & Eberhard, S.M. (2015) Cryptic species or inadequate taxonomy? Implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa. Systematic Biology 65, 304327.CrossRefGoogle ScholarPubMed
Kuntz, R.E. (1952) Exposure of planorbid snails from the western hemisphere to miracidia of the Egyptian strain of Schistosoma mansoni . Proceedings of the Helminthological Society of Washington 19, 915.Google Scholar
Kuris, A.M. (1990) Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. pp. 69100 in Esch, G.W., Bush, A.O. & Aho, J.M. (Eds) Parasite communities: Patterns and processes. London, Chapman & Hall.Google Scholar
Lajus, D., Sukhikh, N. & Alekseev, V. (2015) Cryptic or pseudocryptic: can morphological methods inform copepod taxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex. Ecology and Evolution 5, 23742385.Google Scholar
Lamothe-Argumedo, R. (1981) Un caso raro de parasitismo. Anales del Instituto de Biología de la Universidad Autónoma de México Seccion Zoología 51, 675682.Google Scholar
Lamothe-Argumedo, R., Damborenea, C., García-Prieto, L., Lunaschi, L.I. & Osorio-Sarabia, D. (2010) Guide to helminthological collections of Latin America. 1st edn. 62 pp. Instituto de Bología, UNAM, México.Google Scholar
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Missé, D., Poulin, R. & Thomas, F. (2009) The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 4148.Google Scholar
Leung, T.L.F., Mora, C. & Rohde, K. (2015) Patterns of diversity and distribution of aquatic invertebrates and their parasites. pp. 3957 in Morand, S., Krasnov, B.B. & Littlewood, D.T.J. (Eds) Parasite diversity and diversification: Evolutionary ecology meets phylogenetics. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Littlewood, D.T.J., Bray, R.A. & Waeschenbach, A. (2015) Phylogenetic patterns of diversity in cestodes and trematodes. pp. 304319 in Morand, S., Krasnov, B.B. & Littlewood, D.T.J. (Eds) Parasite diversity and diversification: Evolutionary ecology meets phylogenetics. Cambridge, Cambridge University Press.Google Scholar
Luque, J.L. & Poulin, R. (2007) Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology 134, 865878.Google Scholar
Luque, J.L., Mouillot, D. & Poulin, R. (2004) Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128, 671682.Google Scholar
Malek, E.A. (1980) Snail-transmitted parasitic diseases. Vol. I. 334 pp. Boca Raton, Florida, CRC Press.Google Scholar
Marcogliese, D.J. (1995) The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336371.Google Scholar
Martorelli, S.R. (1986) Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920 II: Desarrollo del ciclo biológico de Microphallus szidati en dos ambientes de condiciones ecológicas diferentes. Revista Iberica de Parasitología 46, 378385.Google Scholar
Martorelli, S.R. (1988) El ciclo biológico de Levinseniella cruzi Travassos, 1920 (Digenea: Microphallidae) parásita de los ciegos cólicos de Rollandia rolland chilensis (Aves: Podicipedidae) e Himantopus melanurus (Aves: Recurvirostridae). Iheringia 68, 4962.Google Scholar
Martorelli, S.R., Navone, G.T. & Navone, G.T. (2000) Proposed life cycle of Ascarophis marina (Nematoda: Cystidicolidae) in Argentine waters. Journal of Parasitology 86, 10471050.CrossRefGoogle ScholarPubMed
Martorelli, S.R., Alda, M.P., Marcotegui, P.S., La Sala, L.F. & Montes, M.M. (2013) Larval digeneans in Biomphalaria snails from the Salto Grande Dam area in the Uruguay River. pp. 113. Publicación del Laboratorio de Helmintos y Parasitos de Crustaceos del CEPAVE, La Plata, Argentina.Google Scholar
Morard, R., Escarguel, G., Weineri, A.K.M., Andre, A., Douady, C.J., Wade, C.M., Darliln, K.F., Ujiie, Y., Seears, H.A., Quillevere, F., de Garidel-Thoron, T., de Vargas, C. & Kucera, M. (2016) Nomenclature for the nameless: a proposal for an integrative molecular taxonomy of cryptic diversity exemplified by planktonic foraminifera. Systematic Biology. doi:10.1093/sysbio/syw031.Google Scholar
Muñóz, G., López, Z. & Cardenas, L. (2012) Morphological and molecular analyses of larval trematodes in the intertidal bivalve Perumytilus purpuratus from central Chile. Journal of Helminthology 8, 356363.Google Scholar
Nassi, H. & Bayssade-Dufour, C. (1980) Life cycle of Clinostomum golvani n. sp. (Trematoda: Clinostomidae) a larval parasite of Biomphalaria glabrata, the snail vector of Schistosoma mansoni in Guadeloupe (author's transl.). Annales de Parasitologie Humaine et comparée 55, 527540.Google Scholar
Nazir, P. (1980) Freshwater larval trematodes. Biophalarians as host of larval diageneans – an outline. Revista di Parassitologia 41, 451460.Google Scholar
Orlofske, S.A., Jadin, R.C. & Johnson, P.T.J. (2015) It's a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537547.Google Scholar
Ostrowski de Núñez, M. (1973) Sobre el ciclo biológico experimental de Posthodiplostomum nanum Dubois, 1937 (Trematoda, Diplostomatidae). Physis B 32, 121132.Google Scholar
Ostrowski de Núñez, M. (1977) El ciclo biológico de Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois, 1970 (Austrodiplostomum mordax Szidat y Nani, 1951) (Trematoda, Diplostomatidae). Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Parasitología 2, 763.Google Scholar
Ostrowski de Núñez, M. (1989) The life history of a trematode, Apharyngostrigea simplex (Johnston, 1904) from the ardeid bird Egretta thula in Argentina. Zoologischer Anzeiger 222, 322336.Google Scholar
Ostrowski de Núñez, M. (1993) Life-history studies of heterophyid trematodes in the Neotropical Region: Ascocotyle (Phagicola) diminuta (Stunkard & Haviland, 1924) and A. (P.) angrense Travassos, 1916. Systematic Parasitology 24, 191199.Google Scholar
Ostrowski de Núñez, M. & Quintana, M.G. (2008) The life cycle of Stephanoprora aylacostoman sp. (Digenea: Echinostomatidae), parasite of the threatened snail Aylacostoma chloroticum (Prosobranchia, Thiaridae), in Argentina. Parasitology Research 102, 647655.Google Scholar
Overstreet, R.M. (1978) Marine maladies? Worms, germs, and other symbionts from the Northern Gulf of Mexico. 140 pp. Ocean Springs, Mississippi, Mississippi–Alabama Sea Grant Consortium, Blossmand Printing, Inc.Google Scholar
Parker, G., Chubb, J.C., Ball, M.A. & Roberts, G.N. (2003) Evolution of complex life cycles in helminth parasites. Nature 425, 480484.Google Scholar
Parker, G.A., Ball, M.A. & Chubb, J.C. (2015) Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent. Journal of Evolutionary Biology 28, 267291.Google Scholar
Parr, C.S., Guralnick, R., Cellinese, N. & Page, R.D.M. (2012) Evolutionary informatics: unifying knowledge about the diversity of life. Trends in Ecology and Evolution 27, 94103.Google Scholar
Peoples, R.C. (2013) A review of the helminth parasites using polychaetes as hosts. Parasitology Research 112, 34093421.Google 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. (Ed.) Changing diversity in changing environment. China, InTech.Google Scholar
Poulin, R. (2007) Evolutionary ecology of parasites. 2nd edn. 342 pp. Oxford, UK, Princeton University Press.CrossRefGoogle Scholar
Poulin, R. (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology 44, 581589.Google Scholar
Poulin, R. & Morand, S. (2004) Parasite biodiversity. 216 pp. Washington DC, Smithsonian Institution Scholarly Press.Google Scholar
Rohde, K. (2005) Marine parasitology. 2nd edn. 565 pp. Wallingford, CABI Publishing and Collingwood, CSIRO Publishing.Google Scholar
Rohde, K. (2010) Marine parasite diversity and environmental gradients. pp. 7388 in Morand, S. & Krasnov, B.R. (Eds) The biogeography of host–parasite interactions. Oxford, Oxford University Press.Google Scholar
Rojas, D., Soto, C. & Rojas, A. (2013) Pathology and first report of natural eye infection with the trematode Philophthalmus gralli (Digenea, Philophthalmidae) in Tinamus major (Tinamiformes, Tinamidae), Costa Rica. Parasitology International 62, 571574.Google Scholar
Salgado-Maldonado, G. (2008) Helminth parasites of freshwater fish from Central America. Zootaxa 1915, 2953.Google Scholar
Scholz, T. & Salgado-Maldonado, G. (1994) On Genarchella isabellae (Digenea: Derogenidae) from cichlid and pimelodid fishes in Mexico. Journal of Parasitology 80, 10131017.CrossRefGoogle ScholarPubMed
Scholz, T., Lavadores, I.P., Vargas, V.J., Mendoza, E.F., Rodríguez, C.R. & Vivás, R.C. (1994) Life cycle of Oligogonotylus manteri (Digenea: Cryptogonimidae), a parasite of cichlid fishes in southern Mexico. Journal of the Helminthological Society of Washington 61, 190199.Google Scholar
Siquier, G.F. (2014) Hallazgo de la medusa Bougainvillia pagesi (Cnidaria, Hydrozoa, Anthoathecata) parasitada con metacercarias de Monascus filiformis (Digenea, Fellodistomidae) en el estuario del río de La Plata, Uruguay. Boletin de la Sociedad Zoológica del Uruguay 23, 4347.Google Scholar
Sousa, W.P. (1994) Patterns and processes in communities of helminth parasites. Trends in Ecology and Evolution 9, 5257.Google Scholar
Thompson, R.M., Mouritsen, K.I.M.N. & Poulin, R. (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. Journal of Animal Ecology 74, 7785.Google Scholar
Torchin, M.E., Miura, O. & Hechinger, R.F. (2015) Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts. Ecology 96, 30333042.Google Scholar
Velásquez, L.E., Bedoya, J.C., Areiza, A. & Vélez, I. (2006) Primer registro de Centrocestus formosanus (Digenea: Heterophyidae) en Colombia. Revista Mexicana de Biodiversidad 77, 119121.Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Del Rio-Rodrıíguez, R., Gold-Bouchot, G., Rendón-von Osten, J. & Miranda-Rosas, G.A. (2006) The pink shrimp Farfantepenaeus duorarum, its symbionts and helminths as bioindicators of chemical pollution in Campeche Sound, Mexico. Journal of Helminthology 80, 159174.Google Scholar
Williams, J.A. & Esch, G.W. (1991) Infra- and component community dynamics in the pulmonate snail, Helisoma anceps, with special emphasis on the hemiurid trematode, Halipegus occidualis . Journal of Parasitology 77, 247253.CrossRefGoogle Scholar
Wilson, E.O. & Peter, F.M. (1988) Biodiversity. 1st edn. 521 pp. Washington DC, National Academic Press.Google Scholar
Zbikowska, E. & Nowak, A. (2009) One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe. Parasitology Research 105, 301311.Google Scholar
Zeidan, C.G., Luz, M.S.A. & Boehs, G. (2012) Parasites of economically important bivalves from the southern coast of Bahia State, Brazil. Revista Brasilenia de Parasitologia Veterinária 21, 391398.Google Scholar
Supplementary material: File

Aguirre-Macedo supplementary material

Supplementary Table

Download Aguirre-Macedo supplementary material(File)
File 192.3 KB