Abstract
Studies of marine mammal parasites in the Caribbean are scarce. An assessment for marine mammal endo- and ectoparasites from Puerto Rico and the Virgin Islands, but extending to other areas of the Caribbean, was conducted between 1989 and 1994. The present study complements the latter and enhances identification of anisakid nematodes using molecular markers. Parasites were collected from 59 carcasses of stranded cetaceans and manatees from 1994 to 2006, including Globicephala macrorhynchus, Kogia breviceps, Kogia sima, Lagenodelphis hosei, Mesoplodon densirostris, Peponocephala electra, Stenella longirostris, Steno bredanensis, Trichechus manatus. Tursiops truncatus, and Ziphius cavirostris. Sixteen species of endoparasitic helminthes were morphologically identified, including two species of acanthocephalans (Bolbosoma capitatum, Bolbosoma vasculosum), nine species of nematodes (Anisakis sp., Anisakis brevispiculata, Anisakis paggiae, Anisakis simplex, Anisakis typica, Anisakis ziphidarium, Crassicauda anthonyi, Heterocheilus tunicatus, Pseudoterranova ceticola), two species of cestodes (Monorygma grimaldi, Phyllobothrium delphini), and three species of trematodes (Chiorchis groschafti, Pulmonicola cochleotrema, Monoligerum blairi). The nematodes belonging to the genus Anisakis recovered in some stranded animals were genetically identified to species level based on their sequence analysis of mitochondrial DNA (629 bp of mtDNA cox 2). A total of five new host records and six new geographic records are presented.
Similar content being viewed by others
References
Anderson RC, Chabaud AG, Willmott S (1974–1982) CIH Keys to the nematode parasites of vertebrates. Commonwealth Institute of Helminthology, Commonwealth Agricultural Bureau, Bucks, England
Arnold PW, Gaskin DE (1975) Lungworms (Metastrogyloidea: Pseudaliidae) of harbour porpoise Phocoena phocoena (L. 1785). Can J Zool 53:713–735
Aznar FJ, Balbuena JA, Fernandez M, Raga JA (2001) Living together: The parasites of marine mammals. In: Evans P, Raga JA (eds) Marine mammals: Biology and conservation. Kluwer Academic, New York, pp 385–423
Aznar FJ, Agustí C, Littlewood DTJ, Raga JA, Olson PD (2007) Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). Int J Parasitol 37:243–255
Bannister JL, Kemper CM, Warneke RM (1996) The action plan for Australian cetaceans. Australian Nature Conservation Agency, Canberra Printing Services, Canberra, Australia
Baylis HA (1932) A list of worms parasitic in Cetacea. Discov Rep 6:393–418
Beck CA, Forrester DJ (1988) Helminthes of the Florida manatee, Trichechus manatus latirostris, with a discussion and summary of the parasites of sirenians. J Parasitol 74:628–637
Berland B (1961) Nematodes from some Norwegian marine fishes. Sarsia 2:1–50
Blair D (2005) Family Opisthotrematidae Poche, 1926. In: Jones A, Bray RA, Gibson DI (eds) Keys to Trematoda, vol. 2. CABI International and The Natural History Museum, London, pp 401–406
Bonde RK, Lewis P, Samuelson D, Self-Sullivan C, Auil N, Powell JA (2005a) Belize manatee (Trichechus manatus manatus) epibionts–SEM viewing techniques. Abstracts, Florida Marine Mammal Health Conference, University of Florida, 7–10 April 2005, Gainesville, Florida
Bonde RK, Lewis P, Samuelson D, Self-Sullivan C, Auil N, Powell JA (2005b) Epibionts identified on manatees (Trichechus manatus manatus) in Belize. Abstracts, Sixteenth Biennial Conference on the Biology of Marine Mammals, 12–16 December 2005, San Diego, California.
Bray RA, Gibson DI, Jones A (eds) (2008) Keys to the Trematoda, Volume 3. CABI Publishing, Wallingford, UK
Bryden MM, Dawbin WH, Heinsohn GE, Brown DH (1976) Melon-headed whale, Peponocephala electra, on the east coast of Australia. J Mammal 58:180–187
Cintrón-de Jesús J (2001) Barnacles associated with marine vertebrates in Puerto Rico and Florida. Master’s thesis, University of Puerto Rico, Mayagüez, Puerto Rico
Cintrón-de Jesús J, Williams Jr. EH, Bunkley-Williams L, Mignucci-Gianonni AA (1999) Barnacles associated with Caribbean marine mammals. Page 34 in Abstracts of the Thirteenth Biennial Conference on the Biology of Marine Mammals, Maui, Hawaii, November 1999
Cintrón-de Jesús J, Williams Jr. EH, Mignucci-Gianonni AA (2005) Barnacles associated to marine vertebrates in Florida and Puerto Rico. Page 198 in Coyne MS, Clark RD (eds) Proceedings of the 21st Annual Symposium on Sea Turtle Biology and Conservation, Philadelphia, 24–28 February 2001. NOAA Tech Memo NMFS-SEFSC-528
Cowan DF (1967) Helminth parasites of the pilot whale Globicephala melaena (Traill 1809). J Parasitol 53:153–168
Coy-Otero A (1989) Una nueva especie de tremátodo del género Chiorchis (Diplodiscidae), un parásito del manatí Trichechus manatus (Sirenia) de Cuba. Poeyana 378:1–4
Dailey MD (2001) Parasitic diseases. In: Dierauf LA, Gulland FMD (eds) CRC Handbook of marine mammal medicine: health, disease, and rehabilitation. CRC Press, Boca Raton, Florida, pp 357–379
Dailey MD, Brownell RL Jr (1972) A checklist of marine mammal populations. In: Ridgway SH (ed) Mammals of the sea: Biology and medicine. Charles C. Thomas, Springfield, Illinois, pp 528–589
Dailey MD, Vogelbein W, Forrester DJ (1988) Moniligerum blairi n. g. sp. and Nudacotyle undicola n. sp. (Trematoda: Digenea) from the West Indian manatee, Trichechus manatus L. Syst Parasitol 11:159–163
Davey JT (1971) A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata). J Helminthol 45:51–72
Deardorff TL, Overstreet RM (1981) Terranova ceticola n. sp. (Nematoda: Anisakidae) from the dwarf sperm whale, Kogia simus (Owen), in the Gulf of Mexico. Syst Parasitol 3:25–28
Debrot AO, Barros NB (1994) Additional cetacean records for the Leeward Dutch Antilles. Mar Mamm Sci 10:359–368
Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Moscow, Akademiia Nauk SSSR
Dierauf LA (1990) Marine mammal parasitology. In: Dierauf L (ed) Handbook of marine mammal medicine: Health, disease, and rehabilitation. CRC Press, Boca Raton, Florida, pp 89–96
Dollfus RP (1966) Helminthofaune de Kogia breviceps (Blaineville 1838) cetace odontocetes recoltes du Dr. R. Duguy. Ann Soc Sci Nat Charente-Maritime 4:3–6
Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791
Fernández M, Aznar J, Montero FE, Georgiev BB, Raga JA (2004) Gastrointestinal helminthes of Cuvier’s beaked whale, Ziphius cavirostris, from the Western Mediterranean. J Parasitol 90:418–420
Forrester DJ (1992) Parasites and diseases of wild mammals in Florida. University Press of Florida, Gainesville, Florida
García-Rodríguez AI, Bowen BW, Domning DP, Mignucci-Giannoni AA, M. Marmontel M, Montoya-Ospina RA, Morales-Vela B, Rudin M, Bonde RK, McGuire PM (1998) Phylogeography of the West Indian manatee (Trichechus manatus): How many populations and how many taxa? Mol Ecol 7:1737–1749
Gibson DI, Harris EA, Bray RA, Jepson PD, Kuiken T, Baker JR, Simpson VR (1998) A survey of the helminth parasite of cetaceans stranded on the coast of England and Wales during the period 1990–1994. J Zool Lond 244:563–574
Gibson DI, Jones A, Bray RA (eds) (2002) Keys to the Trematoda, vol.1. CABI Publishing, Wallingford, UK, p 544
Gunter G, Overstreet RM (1974) Cetacea notes. I. Sei and rorqual whales on the Mississippi coast, a correction. II. A dwarf sperm whale in Mississippi sound and its helminth parasites. Gulf Res Rep 4:479–481
Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Heyning JE (1989) Cuvier’s beaked whales–Ziphius cavirostris G. Cuvier 1823. In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol. 4: River dolphins and the larger toothed whales. Academic Press, San Diego, California, pp 289–308
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192
Hoberg EP, Daoust PY, McBurney S (1993) Bolbosoma capitatum and Bolbosoma sp. (Acanthocephala) from sperm whales (Physeter macrocephalus) stranded on Prince Edward Island. J Helminthol Soc Wash 60:205–210
Iglesias R, D’Amelio S, Ingrosso S, Farjallah S, Martinez-Cedeira JA, García-Estevez JM (2008) Molecular and morphological evidence for the occurrence of Anisakis sp. A (Nematoda: Anisakidae) in the Blainville’s beaked whale Mesoplodon densirostris. J Helmith 82:305–308
Jones A, Bray RA, Gibson DI (eds) (2005) Keys to the Trematoda, vol. 2. CABI Publishing, Wallingford, UK, p 768
Kagei N, Oshima T, Kobayashii A, Kumada M, Koyama T, Komiya Y, Takemura A (1967) A survey of Anisakis spp. (Anisakinae, Nematoda) in marine mammals on the coast of Japan. Jpn J Parasitol 16:427–435
Khalil LF, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CAB International, Wallingford, UK, p 768
Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA 2: Molecular evolutionary genetics analysis software. Arizona State University, Tempe, Arizona
Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: An update. Parasite 13:99–113
Mattiucci S, Nascetti G (2008) Advances and trends in molecular systematics of anisakid nematodes with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 66:47–148
Mattiucci S, Nascetti G, Cianchi R, Paggi L, Arduino P, Margolis L, Brattey J, Webb SC, D’Amelio S, Orecchia P, Bullini L (1997) Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol 83:401–416
Mattiucci S, Paggi L, Nascetti G, Abollo E, Webb SC, Pascual S, Cianchi R, Bullini L (2001) Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). Int J Parasitol 31:9–14
Mattiucci S, Paggi L, Nascetti G, Portes Santos C, Costa G, Di Benedetto AP, Ramos R, Argyrou M, Cianchi R, Bullini L (2002) Genetic markers in the study of Anisakis typica (Diesing, 1860): Larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Syst Parasitol 51:159–170
Mattiucci S, Nascetti G, Dailey MD, Barros NB, Webb SC, Cianchi R, Bullini L (2005) Evidence for a new species of Anisakis Dujardin, 1845: Morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Syst Parasitol 61:157–171
McAlpine DF, Murison LD, Hoberg EP (1997) New records for the pygmy sperm whale, Kogia breviceps (Physeteridae) from Atlantic Canada with notes on diet and parasites. Mar Mamm Sci 13:701–704
McColl KA, Obendorf DL (1982) Helminth parasites and associated pathology in stranded Fraser’s dolphins, Lagenodelphis hosei Fraser 1956. Aquat Mamm 9:30–34
Mignucci-Giannoni AA, Hoberg EP, Sigel-Causey D, Williams EH Jr (1998) Metazoan parasites and other symbionts of cetaceans in the Caribbean. J Parasitol 84:939–946
Mignucci-Giannoni AA, Beck CA, Montoya-Ospina RA, Williams EH Jr (1999a) Parasites and commensals of the West Indian manatee from Puerto Rico. J Helminthol 66:67–69
Mignucci-Giannoni AA, Williams EH Jr, Toyos-González GM, Pérez-Padilla J, Rodríguez-López MA, Vega-Guerrera MB, Ventura-González M (1999b) Helminthes from a stranded manatee in the Dominican Republic. Vet Parasitol 81:69–71
Milinkovitch MC (1995) Molecular phylogeny of cetaceans prompts revision of morphological transformations. Trends Ecol Evol 10:328–334
Morales-Vela B, Olivera-Gómez LD (1993) Varamiento de calderones Globicephala macrorhynchus (Cetacea: Delphinidae) en la isla de Cozumel, Quintana Roo. An Inst Biol Univ Nac Auton Mex Ser Zool 64:177–180
Morales-Vela B, Suárez-Morales E, Padilla-Saldívar J, Heard RW (2008) The tanaid Hexapleomera robusta (Crustacea: Peracarida) from the Caribbean manatee, with comments on other crustacean epibionts. J Mar Biol Assoc UK 88:591–596
Mora-Pinto DM (2000) Morphometric variation of the trematodes Chiorchis fabaceus and C. groschafti parasitic in the West Indian manatee (Trichechus manatus). Master’s thesis, University of Puerto Rico, Mayagüez, Puerto Rico
Nadler SA, Hudspeth DSS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: Hypotheses of structural and sequence evolution. J Parasitol 86:380–393
Nikaido MF, Matsuno H, Hamilton H, Brownell RL, Cao Y, Ding W, Zuoyan Z, Sheldock AM, Fordyce M, Hasegawa M, Okada N (2001) Retroposon analysis of major cetacean lineages: The monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA 98:7384–7389
Ortíz M, Lalana R, Torres-Fundora O (1992) Un nuevo género y una nueva especie de copépodo Harpacticoida asociada al manatí Trichechus manatus en aguas cubanas. Rev Invest Mar 13:117–127
Paggi L, Nascetti G, Webb SC, Mattiucci S, Cianchi R, Bullini L (1998) A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): Allozyme and morphological evidence. Syst Parasitol 40:161–174
Pendergraph GE (1971) First report of the acanthocephalan Bolbosoma vasculosum (Rudolphi, 1819) from the pygmy sperm whale, Kogia breviceps. J Parasitol 57:1109
Pontes T, D’Amelio S, Costa G, Paggi L (2005) Molecular characterization of larval anisakid nematodes from marine fishes of Madeira, by PCR based approaches with evidence for a new species. J Parasitol 91:1430–1434
Raga JA (1994) Parasitisms beiden Cetacea. In: Robineau D, Duguy R, Klima M (eds) Handbuch der Saugetiere Europas, vol. 6. Aula-Verlag, Wiesbaden, Germany, pp 133–179
Raga JA, Balbuena JA (1990) A new species of the genus Crassicauda Leiper et Atkinson 1914 (Nematoda: Spiruroidea) from the penis of Globicephala melas (Traill 1809) (Cetacea: Globicephalidae) in the western Mediterranean Sea. Ann Parasitol Hum Comp 65:255–261
Raga JA, Balbuena JA, Aznar J, Fernández M (1997) The impact of parasites on marine mammals: A review. Parassitologia 39:293–296
Rice DW (1989) Sperm whale Physeter macrocephalus Linnaeus, 1758. In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol. 4: River dolphins and the larger toothed whales. Academic Press, San Diego, California, pp 177–233
Ross GJB (1978) Records of pygmy and dwarf sperm whales, genus Kogia, from southern Africa, with biological notes and some comparisons. Ann Cape Prov Mus (Nat Hist) 11:259–327
Ross GJB (2006) Review of the conservation status of Australia’s smaller whales and dolphins. Report to the Australian Department of the Environment and Heritage, Canberra, Australia, p 124
Schell SC (1985) Handbook of trematodes of North America north of Mexico. University Press of Idaho, Moscow, Idaho
Schmidt SC (1986) CRC handbook of tapeworm identification. CRC Press, Boca Raton, Florida
Skrjabin AS (1972) Lichinki tsestod roda Phyllobothrium Van Beneden 1850 (Tetraphyllidea), parasitiruiushchie u kitov I drugikh morskikh zhivotnykh. Parazitolgiia 6:426–434
Sokolov VE (1955) Raspredelenie lichinok tsestody Phyllobotrium delphini Bosc. V kozhnom pokrove kashalotov v zavisimosti ot struktury kozhi. Dokl Akad Nauk SSSR 103:1135–1137
Testa J, Dailey MD (1976) Five new morphotypes of Phyllobothrium delphini (Cestoda: Tetraphyllidea), their relationship to existing morphotypes, and their zoogeography. Bull So Cal Acad Sci 67:99–110
Thompson JD, Higgins DG, Gibson TJ (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, postion-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tomilin AG (1957) Mammals of the U. S. S. R. and adjacent countries, Vol. IX: Cetacea. (In Russian, translated 1967). Israel Program for Scientific Translations, Jerusalem, p 717
Upton SJ, Odell DK, Bossart GD, Walsh MT (1989) Description of the oocysts of two new species of Eimeria (Apicomplexa: Eimeriidae) from the Florida manatee, Trichechus manatus (Sirenia: Trichechidae). J Protozool 36:87–90
Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannoni AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae), inferred from mitochondrial cox2 sequences, and comparison with allozyme data. J Parasitol 92:156–66
Vianna JA, Bonde RK, Caballero S, Giraldo JP, Lima RP, Clark A, Marmontel M, Morales-Vela B, de Sousa MJ, Parr L, Rodríguez-López MA, Mignucci-Giannoni AA, Powell JA, Santos FR (2006) Phylogeography, phylogeny and hybridization in trichechid sirenians: Implications for manatee conservation. Mol Ecol 15:433–447
Williams EH Jr, Bunkley-Williams L (1996) Parasites of offshore big game sport fishes of Puerto Rico and the Western North Atlantic. Puerto Rico Department of Natural and Environmental Resources and Department of Biology, University of Puerto Rico, Mayagüez, Puerto Rico
Yamaguti S (1959) Systema Helminthium: The Cestoda of vertebrates. Interscience Publishers, New York
Yamaguti S (1961) Systema Helminthium: The nematodes of vertebrates. Interscience Publishers, New York
Yamaguti S (1963a) Systema Helminthium: Monogenea and Aspidocotylea. Interscience Publishers, New York
Yamaguti S (1963b) Systema Helminthium: Acanthocephala. Interscience Publishers, New York
Yamaguti S (1963c) Systema Helminthium: Parasitic Copepoda and Branchiura of fishes. Interscience Publishers, New York
Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates, vols. 1–2. Keigaku Publishing Company, Tokyo
Yang HEM, Golenberg M, Shoshani J (1997) Proboscidean DNA from museum and fossil specimens: An assessment of ancient DNA extraction and amplification techniques. Biochem Genet 35:165–179
Zam SG, Caldwell DK, Caldwell MC (1971) Some endoparasites from small odontocete cetaceans collected in Florida and Georgia. Cetology 2:1–11
Acknowledgments
Marine mammal salvage and specimen collection were conducted under the authority of US Fish and Wildlife permits PRT-770191 and MA791721-2 (issued to the US Geological Survey, Sirenia Project) and a cooperative agreement with the Puerto Rico Department of Natural and Environmental Resources and US Virgin Islands Department of Planning and Natural Resources. We gratefully acknowledge the assistance of Caribbean Stranding Network participants and volunteers in the salvage and necropsy of the carcasses and the collection of parasite samples. We thank J. R. García-Sais, L. Bunkley-Williams and C. Ríos-Velázquez for comments on early drafts of this manuscript as part of one of the author’s (MMCLl) master’s thesis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Colón-Llavina, M.M., Mignucci-Giannoni, A.A., Mattiucci, S. et al. Additional records of metazoan parasites from Caribbean marine mammals, including genetically identified anisakid nematodes. Parasitol Res 105, 1239–1252 (2009). https://doi.org/10.1007/s00436-009-1544-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-009-1544-4