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The phylogeny and life cycle of two species of Profilicollis (Acanthocephala: Polymorphidae) in marine hosts off the Pacific coast of Chile

Published online by Cambridge University Press:  26 September 2016

S.M. Rodríguez ,
G. D'Elía  and
N. Valdivia
S.M. Rodríguez*
Affiliation:
Doctorado en Biología Marina and Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias, Universidad Austral de Chile, campus Isla Teja s/n, Valdivia, Chile
G. D'Elía
Affiliation:
Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile
N. Valdivia
Affiliation:
Doctorado en Biología Marina and Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias, Universidad Austral de Chile, campus Isla Teja s/n, Valdivia, Chile Centro FONDAP de Investigación en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL)
*
*E-mail: saramrodriz@gmail.com
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Abstract

Resolving complex life cycles of parasites is a major goal of parasitological research. The aim of this study was to analyse the life cycle of two species of the genus Profilicollis, the taxonomy of which is still unstable and life cycles unclear. We extracted individuals of Profilicollis from two species of crustaceans (intermediate hosts) and four species of seagulls (definitive hosts) from sandy-shore and estuarine habitats along the south-east Pacific coast of Chile. Mitochondrial DNA analyses showed that two species of Profilicollis infected intermediate hosts from segregated habitats: while P. altmani larvae infected exclusively molecrabs of the genus Emerita from fully marine habitats, P. antarcticus larvae infected the crab Hemigrapsus crenulatus from estuarine habitats. Moreover, P. altmani completed its life cycle in four seagulls, Chroicocephalus maculipennis, Leucopheus pipixcan, Larus modestus and L. dominicanus, while P. antarcticus, on the other hand, completed its life cycle in the kelp gull L. dominicanus. Accordingly, our results show that two congeneric parasites use different and spatially segregated species as intermediate hosts, and both are capable of infecting one species of definitive hosts. As such, our analyses allow us to shed light on a complex interaction network.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 5 , September 2017 , pp. 589 - 596
Copyright
Copyright © Cambridge University Press 2016 

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References

Amin, O.M. (2013) Classification of Acanthocephala. Folia Parasitologica 60, 273–305.Google Scholar
Bahamondes, I. & Castilla, J.C. (1986) Predation of marine invertebrates by the kelp gull Larus dominicanus in an undisturbed intertidal rocky shore of central Chile. Revista Chilena de Historia Natural 59, 65–72.Google Scholar
Balboa, L., Hinojosa, A., Riquelme, C., Rodríguez, S., Bustos, J. & George-Nascimento, M. (2009) Alloxenic distribution of cyctacanths of two Profilicollis species in sympatric crustacean hosts in Chile. Journal of Parasitology 95, 1205–1208.Google Scholar
Blokpoel, H., Boersma, D.C., Hughes, R.H. & Tessier, G.D. (1992) Foraging by larids on sand crabs Emerita analoga along the coast of Southern Perú. Ardea 80, 99–104.Google Scholar
Bruschetti, M., Bazterrica, C., Luppi, T. & Iribarne, O. (2009) An invasive intertidal reef-forming polychaete affects habitat use and feeding behaviour of migratory and locals birds in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 375, 76–83.CrossRefGoogle Scholar
Buehler, D.M., Bugoni, L., Dorrestein, G.M., González, P.M., Pereira, J. Jr, Proença, L., De Lima Serrano, I., Baker, A.J. & Piersma, T. (2010) Local mortality events in migrating sandpipers (Calidris) at a stopover site in southern Brazil. Wader Study Group Bulletin 117, 150–156.Google Scholar
Bush, A., Lafferty, K.D., Lotz, J. & Shostak, A. (1997) Parasitology meets ecology on its own terms, Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cezilly, F., Gregoire, A. & Bertin, A. (2000) Conflict between co-ocurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behavior of Gammarus pulex. Parasitology 120, 625–630.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristic and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dezfuli, B.S., Giari, L. & Poulin, R. (2001) Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483–489.Google Scholar
Diaz, J.I., Cremonte, F. & Navone, G.T. (2011) Helminths of the kelp gull, Larus dominicanus, from the northern Patagonian coast. Parasitology Research 109, 1555–1562.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Garcés-Vargas, J., Ruiz, M., Pardo, L.M., Nuñez, S. & Pérez-Santos, I. (2013) Caracterización hidrográfica del estuario del río Valdivia, centro-sur de Chile. Latin American Journal of Aquatic Research 41, 113–125.Google Scholar
García-Varela, M., Pérez-Ponce de León, G., Aznar, F.J. & Nadler, S.A. (2013) Phylogenetic relationship among genera of Polymorphidae (Acanthocephala), inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 68, 176–184.CrossRefGoogle ScholarPubMed
Ghys, M.I. & Favero, M. (2004) Espectro trófico de la gaviota Capucho Café (Larus maculipennis) en agroecosistemas del sudeste de la provincia de Buenos Aires, Argentina. Ornitología Neotropical 15, 493–500.Google Scholar
González-Acuña, D., Cerda, F., López, J., Ortega, R., Mathieu, C. & Kinsella, M. (2009) Checklist of the helminths of the kelp gull, Larus dominicanus (Aves: Laridae), with new records from Chile. Zootaxa 2297, 27–43.Google Scholar
Goulding, T.C. & Cohen, C.S. (2014) Phylogeography of a marine acanthocephalan: lack of cryptic diversity in a cosmopolitan parasite of mole crabs. Journal of Biogeography 41, 965–976.Google Scholar
Haye, P.A. & Ojeda, P. (1998) Metabolic and behavioral alterations in the crab Hemigrapsus crenulatus (Milne-Edwards 1837) induced by its acanthocephalan parasite Profilicollis antarcticus (Zdzitowiecki 1985). Journal of Experimental Marine Biology and Ecology 228, 73–82.CrossRefGoogle Scholar
Hennessy, S.L. & Morejohn, V.J. (1977) Acanthocephalan parasites of the sea otter, Enhydra lutris, off coastal California. California Fish and Game 63, 268–272.Google Scholar
Hinojosa-Sáez, A., González-Acuña, D. & George-Nascimento, M. (2009) Parásitos metazoos de Anas georgica Gmelin, 1789 (Aves: Anseriformes) en Chile central: especificidad, prevalencia y variaciones entre localidades. Revista Chilena de Historia Natural 82, 337–345.CrossRefGoogle Scholar
Khatchikian, C.E., Favero, M. & Vassallo, I. (2002) Kleptoparasitism by Brown-hooded gulls and Grey-hooded gulls on American oystercatchers. Waterbirds 25, 137–264.Google Scholar
Kochin, B.F., Bull, J.J. & Antia, R. (2010) Parasite evolution and life history theory. PLoS Biology 8, e1000524.Google Scholar
Lafferty, K.D., McLaughlin, J.P. & Dugan, J.E. (2013) Novel foraging in the swash zone on pacific sand crabs (Emerita analoga, Hippidae) by mallards. The Wilson Journal of Ornithology 125, 423–426.CrossRefGoogle Scholar
La Sala, L.F. & Martorelli, S.R. (2007). Intestinal acanthocephaladiosis in Olrog's gulls (Larus atlanticus): Profilicollis chasmagnathi as possible cause of death. Journal of Wildlife Disseases 43, 269–273.CrossRefGoogle ScholarPubMed
La Sala, L.F., Perez, A.M., Smits, J.E. & Martorelli, S.R. (2013) Pathology of enteric infections induced by the acanthocephalan Profilicollis chasmagnathi in Olrog's gull, Larus atlanticus, from Argentina. Journal of Helmithology 87, 17–23.Google Scholar
Latham, A.D.M. & Poulin, R. (2002a) Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Marine Biology 141, 1131–1139.Google Scholar
Latham, A.D.M. & Poulin, R. (2002b) New records of gastrointestinal helminths from the southern black-backed gull (Larus dominicanus) in New Zealand. New Zealand Journal of Zoology 29, 253–257.CrossRefGoogle Scholar
Leiva, N., George-Nascimento, M. & Muñoz, G. (2015) Carga parasitaria en crustáceos decápodos de la costa de Chile: existe alguna asociación con la abundancia de los hospedadores definitivos? Latin American Journal of Aquatic Research 43, 726–738.CrossRefGoogle Scholar
Margolis, L., Groff, J.M., Johnson, S.C., McDonald, T.E., Kent, M.L. & Blaylock, R.B. (1997) Helminth parasites of sea otters (Enhydra lutris) from Prince William Sound, Alaska: comparisons with other populations of sea otters and comments on the origin of their parasites. Journal of Helminthology 64, 161–168.Google Scholar
Mayer, K.A., Dailey, M.D. & Miller, M.A. (2003) Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance, distribution and pathology. Diseased of Aquatic Organisms 53, 77–88.Google Scholar
Muñoz, G. & Olmos, V. (2008) Revisión bibliográfica de especies endoparásitas y hospedadoras de sistemas acuáticos de Chile. Revista de Biología Marina y Oceanografía 43, 173–245.Google Scholar
Near, T.J. (2002) Acanthocephalan phylogeny and the evolution of parasitism. Integrative and Comparative Biology 42, 668–677.Google Scholar
Near, T., Garey, J.J.R. & Nadler, S.A. (1998) Phylogenetic relationships of the Acanthocephala inferred from ribosomal DNA sequences. Molecular Phylogenetic and Evolution 10, 287–298.Google Scholar
Riquelme, C., George-Nascimento, M. & Balboa, L. (2006) Morfometría y fecundidad de Profilicollis bulloki Mateo, Córdova & Guzmán 1982 (Acanthocephala: Polymorphidae) en especies simpátricas de aves costeras de Chile. Revista Chilena de Historia Natural 79, 465–474.Google Scholar
Rodríguez, S.M. & D'Elía, G. (2016) Pan-American marine coastal distribution of Profilicollis altmani based on morfometric and phylogenetic analysis of cystacanths from the mole crab Emerita brasiliensis . Journal of Helminthology. doi:10.1017/S0022149X16000237.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Royal, L., Dailey, M., Demaree, R. & Sakanari, J. (2004) Acanthocephala cystacanth infections in sand crabs from Bodega Bay, California. California Fish and Game 90, 36–41.Google Scholar
Smith, N.F. (2007) Associations between shorebird abundance and parasites in the sand crab, Emerita analoga, along the California coast. Journal of Parasitology 93, 265–273.Google Scholar
Steinauer, M.L., Nickol, B.B. & Ortí, G. (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Molecular Ecology 16, 4097–4109.Google Scholar
Sures, B. (2002) Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). International Journal for Parasitology 32, 1117–1122.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Tantaleán, M., Cárdenas, J. & Güere, R. (2002) Profilicollis altmani (Perry, 1942) Van Cleave, 1947 (Acanthocephala) en el Perú. Con notas sobre la infección experimental de mamíferos terrestres. Revista Peruana de Biología 9, 49–51.Google Scholar
Thieltges, D.W., Amundsen, P.A., Hechinger, R.F., Johnson, P.T.J., Lafferty, K.D., Mouritsen, K.N., Preston, D.L., Reise, K., Zander, C.D. & Poulin, R. (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122, 1473–1482.Google Scholar
Thomas, F., Guégan, J.F. & Renaud, F. (2009) Ecology and evolution of parasitism. New York, Oxford University Press.Google Scholar
Torres, O., Ruiz, E., Gesche, W. & Montefusco, A. (1991) Gastrointestinal helminths of fish-eating birds from Chiloe Island, Chile. Journal of Wildlife Diseases 27, 178–179.Google Scholar
Torres, P., Contreras, A., Cubillos, V., Gesche, W., Montefusco, A., Rebolledo, C., Mira, A., Arenas, J., Miranda, J., Asenjo, S. & Schlatter, R. (1992) Parasitismo en peces, aves piscívoras y comunidades humañas rivereñas de los lagos Yelcho y Tagua Tagua, X región de Chile. Archivos de Medicina Veterinaria 24, 77–93.Google Scholar
Torres, P., Schlatter, R., Montefusco, A., Gesche, W., Ruiz, E. & Contreras, A. (1993) Helminth parasites of piscivorous birds from lakes in the south of Chile. Memórias do Instituto Oswaldo Cruz 88, 341–343.Google Scholar
Yorio, P., Marinao, C., Retana, M.V. & Suárez, N. (2013) Differential use of food resources between the Kelp gull Larus dominicanus and the threatened Olrog's gull L . atlanticus. Ardeola 60, 29–44.CrossRefGoogle Scholar
Zdzitowiecki, K. (1985) Acanthocephalans of birds from South Shetlands (Antarctic). Acta Parasitologica Polonica 30, 11–24.Google Scholar