Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T13:13:55.646Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic characterization of members of the genus Contracaecum (Nematoda: Anisakidae) from fish-eating birds from west-central Florida, USA, with evidence of new species

Published online by Cambridge University Press:  13 March 2007

S. D'AMELIO ,
N. B. BARROS ,
S. INGROSSO ,
D. A. FAUQUIER ,
R. RUSSO  and
L. PAGGI
S. D'AMELIO*
Affiliation:
Department of Public Health Science, University of Rome “La Sapienza”, P. le Aldo Moro, 5, 00185 Rome, Italy
N. B. BARROS
Affiliation:
Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL34236, USA
S. INGROSSO
Affiliation:
Department of Public Health Science, University of Rome “La Sapienza”, P. le Aldo Moro, 5, 00185 Rome, Italy
D. A. FAUQUIER
Affiliation:
Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL34236, USA
R. RUSSO
Affiliation:
Department of Pathology, University of California San Diego, La Jolla, CA 92093, USA
L. PAGGI
Affiliation:
Department of Public Health Science, University of Rome “La Sapienza”, P. le Aldo Moro, 5, 00185 Rome, Italy
*
*Corresponding author: Department of Public Health Science, University of Rome “La Sapienza”, P. le Aldo Moro, 5, 00185, Rome, Italy. Tel: +39 0649914671. Fax: +39 0649914644. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Specimens of Contracaecum spp. from Phalacrocorax auritus and Pelecanus occidentalis from Florida were characterized by sequencing of the small subunit of the mitochondrial ribosomal RNA gene (rrnS) and by PCR-based RFLP analysis of the same gene and of the internal transcribed spacers (ITS) of nuclear ribosomal DNA. Analyses of the rrnS sequence data using the MP and UPGMA approaches yielded trees with similar topologies, delineating 3 main clusters. Specimens from Ph. auritus, morphologically assigned to C. rudolphii (s.l.), were part of the cluster comprising also the other 2 species of the C. rudolphii complex (A and B), but representing a genetically distinct group, potentially corresponding to a distinct lineage within the complex, provisionally named as C. rudolphii C. The second cluster comprised 5 individuals from P. occidentalis, which formed a genetically relatively homogeneous group. The rrnS data indicate that these specimens (indicated as Contracaecum sp. 1) are clearly genetically different from the morphologically most closely related species, i.e. C. rudolphii (s.l.) and C. microcephalum, and could represent a new species. The third cluster comprised 7 specimens from P. occidentalis morphologically assigned to C. multipapillatum (s.l.). These were shown to be genetically homogeneous and related to but quite distinct from C. multipapillatum from Greece, although additional studies are needed to assess their status. PCR-RFLP based markers for the quick identification of these taxa are provided.

Keywords

ContracaecumPhalacrocorax auritusPelecanus occidentalisnuclear and mitochondrial ribosomal DNAFloridaUSA
Type
Research Article
Information
Parasitology , Volume 134 , Issue 7 , July 2007 , pp. 1041 - 1051
Copyright
Copyright © Cambridge University Press 2007

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

REFERENCES

Abollo, E., Gestal, C. and Pascual, S. (2001). Anisakid infection in the European shag Phalacrocorax aristotelis aristotelis. Journal of Helminthology 75, 209–214.Google ScholarPubMed
Abollo, E., Paggi, L., Pascual, S. and D'Amelio, S. (2003). Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infection, Genetics and Evolution 3, 175–181.CrossRefGoogle Scholar
Barus, V., Sergeeva, T. P., Sonin, M. D. and Ryzhikov, K. M. (1978). Helminths of Fish-Eating Birds of the Palaeartic Region. I Nematoda. Academia, Prague.CrossRefGoogle Scholar
Bunkley-Williams, L. and Williams, E. H. Jr. (1994). Parasites of Puerto Rican Freshwater Sport Fishes. Puerto Rico Department of Natural and Environmental Resources, San Juan, Puerto Rico, and Department of Marine Sciences, University of Puerto Rico, Mayaguez, Puerto Rico.Google Scholar
Cianchi, R., Orecchia, P., Berland, B., Paggi, L., D'Amelio, S., Mattiucci, S., Nascetti, G. and Bullini, L. (1992). Genetic studies on some Contracaecum species, parasites of fish-eating birds. In Abstracts, VIth European Multicolloquium of Parasitology, The Hague, The Netherlands, p. 127.Google Scholar
Courtney, C. H. and Forrester, D. J. (1974). Helminth parasites of the brown pelican in Florida and Louisiana. Journal of the Helminthological Society of Washington 41, 89–93.Google Scholar
Courtney, C. H., Forrester, D. J. and White, F. H. (1977). Anthelminthic treatment of brown pelicans. Journal of the American Veterinary Medicine Association 171, 921–922.Google ScholarPubMed
D'Amelio, S., Nascetti, G., Mattiucci, S., Cianchi, R., Orecchia, P., Paggi, L., Berland, B. and Bullini, L. (1990). Ricerche electroforetiche su alcune specie del genere Contracaecum, parassiti di uccelli ittiofagi (Ascaridida: Anisakidae). Parassitologia 32, 77.Google Scholar
D'Amelio, S., Mathiopoulos, K. D., Santos, C. P., Pugachev, O. N., Webb, S. C., Picanço, M. and Paggi, L. (2000). Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. International Journal for Parasitology 30, 223–226.CrossRefGoogle ScholarPubMed
Deardorff, T. L. and Overstreet, R. M. (1980). Contracaecum multipapillatum (=C. robustum) from Fishes and Birds in the Northern Gulf of Mexico. Journal of Parasitology 66, 853–856.CrossRefGoogle ScholarPubMed
Diaz-Ungria, C. (1978). Helminthos parasitos de vertebrados en el Estado Zulia. Algunas especies nuevas para Venezuela. Kasmera 6, 207–233.Google Scholar
Diaz-Ungria, C. (1979). Algunas especies de helmintos nuevas para Venezuela. Revista Iberica de Parasitologia 39, 313–336.Google Scholar
Dronen, N. O., Blend, C. K. and Anderson, C. K. (2003). Endohelminths from the Brown Pelican, Pelecanus occidentalis, and the American White Pelican, Pelecanus erythrorhynchus, from Galveston Bay, Texas, U.S.A., and checklist of pelican parasites. Comparative Parasitology 70, 140–154.CrossRefGoogle Scholar
Dyer, W. G., Williams, E. H. Jr., Mignucci-Giannoni, A. A., Jiménez-Marrero, N. M., Bunkley-Williams, L., Moore, D. P. and Pence, D. B. (2002). Helminth and arthropod parasites of the brown pelican, Pelecanus occidentalis, in Puerto Rico, with a compilation of all metazoan parasites reported from this host in the Western Hemisphere. Avian Pathology 31, 441–448.CrossRefGoogle ScholarPubMed
Fagerholm, H. P. (1991). Systematic implications of male caudal morphology in ascaridoid nematode parasites. Systematic Parasitology 19, 215–228.CrossRefGoogle Scholar
Flewelling, L. J., Naar, J. P., Abbott, J. P., Baden, D. G., Barros, N. B., Bossart, G. D., Bottein, M.-Y. D., Hammond, D. G., Haubold, E. M., Heil, C. A., Henry, M. S., Jacocks, H. M., Leighfield, T. A., Pierce, R. H., Pitchford, T. D., Rommel, S. A., Scott, P. S., Steindinger, K. A., Truby, E. W., Van Dolah, F. M. and Landsberg, J. H. (2005). Red tide and marine mammal mortalities. Nature, London 435, 755–756.CrossRefGoogle ScholarPubMed
Flores-Barroeta, L. (1957). Nematodes de Aves y Mamìferos. Revista Iberica de Parasitologia 17, 277–297.Google Scholar
Greve, J. H., Albers, H. F., Suto, B. and Grimes, J. (1986). Pathology of gastrointestinal helminthiasis in the brown pelican (Pelecanus occidentalis). Avian Diseases 30, 482–487.CrossRefGoogle ScholarPubMed
Grimes, J., Suto, B., Greve, I. H. and Albers, H. F. (1989). Effect of selected anthelminthics on three common helminths in the brown pelican (Pelecanus occidentalis). Journal of Wildlife Diseases 25, 139–142.CrossRefGoogle ScholarPubMed
Hartwich, G. (1964). Revision der vogelparasitischen Nematoden Mitteleuropas II. Die Gattung Contracaecum Railliet and Henry, 1912 (Ascaridoidea). Mitteilungen aus dem Zoologischen Museum, Berlin 40, 15–53.Google Scholar
Hatch, J. J. and Weseloh, D. V. (1999). Double-crested Cormorant (Phalacrocorax auritus). In The Birds of North America, No. 441 (ed. Poole, A. and Gill, F.). The Birds of North America, Inc., Philadelphia, PA.Google Scholar
Hu, M., D'Amelio, S., Zhu, X. Q., Paggi, L. and Gasser, R. B. (2001). Mutation scanning for sequence variation in three mitochondrial DNA regions for members of the Contracaecum osculatum (Nematoda: Ascaridoidea) complex. Electrophoresis 22, 1069–1075.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Huizinga, H. W. (1966). Studies on the life cycle and development of Contracaecum spiculigerum (Rudolphi, 1809) (Ascaroidea: Heterocheilidae) from marine piscivorous birds. Journal of the Elisha Mitchell Scientific Society 82, 181–195.Google Scholar
Huizinga, H. W. (1971). Contracaeciasis in pelecaniform birds. Journal of Wildlife Diseases 7, 198–204.CrossRefGoogle Scholar
Humphrey, S. R., Courtney, C. H. and Forrester, D. J. (1978). Community ecology of the helminth parasites of the brown pelican. The Wilson Bulletin 90, 587–598.Google Scholar
Hutton, R. F. (1964). A second list of parasites from marine and coastal animals of Florida. Transactions of the American Microscopical Society 83, 439–444.CrossRefGoogle Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Li, A., D'Amelio, S., Paggi, L., He, F., Gasser, R. B., Lun, Z. R., Abollo, E., Turchetto, M. and Zhu, X. Q. (2005). Genetic evidence for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) and the validity of Contracaecum septentrionale (Kreis, 1955) (Nematoda: Anisakidae). Parasitology Research 96, 361–366.CrossRefGoogle ScholarPubMed
Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J., Webb, S., D'Amelio, S., Orecchia, P. and Bullini, L. (1997). Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology 83, 401–416.CrossRefGoogle ScholarPubMed
Mattiucci, S., Paggi, L., Nascetti, G., Ishikura, H., Kikuchi, K., Sato, N., Cianchi, R. and Bullini, L. (1998). Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Systematic Parasitology 40, 81–92.CrossRefGoogle Scholar
Mattiucci, S., Turchetto, M., Bragantini, F. and Nascetti, G. (2002). On the occurrence of the sibling species of Contracaecum rudolphii complex (Nematoda: Anisakidae) in cormorants (Phalacrocorax carbo sinensis) from Venice and Caorle lagoons: genetic markers and ecological studies. Parassitologia 44, 105.Google Scholar
Mozgovoi, A. A. (1953). Principles of nematodology II. Ascaridata of animals and man and the diseases caused by them. Part II. Izdatel'stvo Akademii Nauk SSSR, Moscow. (In Russian.)Google Scholar
Nadler, S. A., D'Amelio, S., Fagerholm, H. P., Berland, B. and Paggi, L. (2000). Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Høst, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121, 455–463.CrossRefGoogle ScholarPubMed
Nascetti, G., Cianchi, R., Mattiucci, S., D'Amelio, S., Orecchia, P., Paggi, L., Brattey, J., Berland, B. and Smith, J. W. (1993). Three sibling species within Contracaecum osculatum (Nematoda, Ascaridida, Ascaridoidea) from the Atlantic Arctic-Boreal region: reproductive isolation and host preferences. International Journal for Parasitology 23, 105–120.CrossRefGoogle ScholarPubMed
Nascetti, G., Mattiucci, S., Cianchi, R., Berland, B., Bullini, L. and Paggi, L. (2000). Genetic relationship among Contracaecum spp. (Nematoda: Anisakidae), parasites of cormorants and pelicans of the Boreal Region. Acta Parasitologica 45, 153.Google Scholar
Orecchia, P., Mattiucci, S., D'Amelio, S., Paggi, L., Plotz, J., Cianchi, R., Nascetti, G., Arduino, P. and Bullini, L. (1994). Two new members in the Contracaecum osculatum complex (Nematoda, Ascaridoidea) from the Antarctic. International Journal for Parasitology 24, 367–377.CrossRefGoogle ScholarPubMed
Padgett, K. A., Nadler, S. A., Munson, L., Sacks, B. and Boyce, W. M. (2005). Systematics of Mesocestoides (Cestoda: Mesocestoididae): evaluation of molecular and morphological variation among isolates. Journal of Parasitology 91, 1435–1443.CrossRefGoogle ScholarPubMed
Paggi, L., Nascetti, G., Cianchi, R., Orecchia, P., Mattiucci, S., D'Amelio, S., Berland, B., Brattey, J., Smith, J. W. and Bullini, L. (1991). Genetic evidence for three species within Pseudoterranova decipiens (Nematoda, Ascaridida, Ascaridoidea) in the North Atlantic and Norwegian and Barents Seas. International Journal for Parasitology 21, 195–212.CrossRefGoogle ScholarPubMed
Paggi, L., Mattiucci, S., Gibson, D. I., Berland, B., Nascetti, G., Cianchi, R. and Bullini, L. (2000). Pseudoterranova decipiens species A and B (Nematoda, Ascaridoidea): nomenclatural designation, morphological diagnostic characters and genetic markers. Systematic Parasitology 45, 185–197.CrossRefGoogle Scholar
Shields, M. (2002). Brown Pelican (Pelecanus occidentalis). In The Birds of North America, No. 609 (ed. Poole, A. and Gill, F.). The Birds of North America, Inc., Philadelphia, PA.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
Zhu, X. Q., D'Amelio, S., Gasser, R. B., Yang, T. B., Paggi, L., He, F., Lin, R. Q., Song, H. Q., Ai, L. and Li, A. X. (2007). Practical PCR tools for the delineation of Contracaecum rudolphii A and Contracaecum rudolphii B (Ascaridoidea: Anisakidae) using genetic markers in nuclear ribosomal DNA. Molecular and Cellular Probes 21, 97–102.CrossRefGoogle ScholarPubMed
Zhu, X. Q., D'Amelio, S., Hu, M., Paggi, L. and Gasser, R. B. (2001). Electrophoretic detection of population variation within Contracaecum ogmorhini (Nematoda: Ascaridoidea: Anisakidae). Electrophoresis 22, 1930–1934.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Zhu, X. Q., D'Amelio, S., Paggi, L. and Gasser, R. B. (2000). Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitology Research 86, 677–683.CrossRefGoogle ScholarPubMed
Zhu, X. Q., D'Amelio, S., Palm, H. W., Paggi, L., George-Nascimento, M. and Gasser, R. B. (2002). SSCP-based identification of members within the Pseudoterranova decipiens complex (Nematoda: Ascaridoidea: Anisakidae) using genetic markers in the internal transcribed spacers of ribosomal DNA. Parasitology 24, 615–623.CrossRefGoogle Scholar