Larval anisakid nematodes in teleost fishes from Lizard Island, northern Great Barrier Reef, Australia
Abdul Jabbar A F , Abdouslam Asnoussi B , Luke J. Norbury B , Albert Eisenbarth B , Shokoofeh Shamsi C , Robin B. Gasser A , Andreas L. Lopata B D E and Ian Beveridge AA Faculty of Veterinary Science, The University of Melbourne, Werribee, Vic. 3030, Australia.
B School of Applied Science, RMIT University, Bundoora, Vic. 3083, Australia.
C School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2678, Australia.
D School of Pharmacy and Molecular Sciences, James Cook University, Townsville, Qld 4811, Australia.
E Centre for Biodiscovery and Molecular Development of Therapeutics, Qld 4878, Australia.
F Corresponding author. Email: jabbara@unimelb.edu.au
Marine and Freshwater Research 63(12) 1283-1299 https://doi.org/10.1071/MF12211
Submitted: 7 August 2012 Accepted: 12 October 2012 Published: 12 December 2012
Abstract
A survey was undertaken to characterise larval anisakid nematodes present in teleosts at Lizard Island on the northern Great Barrier Reef. In total, 464 fish were examined from 32 families, 62 genera and 107 species. Anisakid nematodes were found in 46 (9.9%) of the fish examined. Infections in Atherinidae, Lethrinidae, Lutjanidae and Serranidae were moderately prevalent, with the intensities of infection ranging from 1 to 80; whereas in the Sphyraenidae and Scombridae, the prevalence of infection was very high, with intensities ranging from 1 to >375 anisakids. A combined morphological and molecular-phylogenetic approach was employed to identify larval anisakid nematodes to species and/or genotypes. The nematodes examined were identified as Anisakis typica (three genotypes based on molecular characterisation), Terranova Types I (five genotypes) and II (five genotypes) and Hysterothylacium Types IV, V (four genotypes), VI and X. The findings of the present study provide some insights into the distribution of larval anisakid nematodes in coral-reef fishes and a basis for future investigations of anisakid populations in marine fishes.
Additional keywords: Anisakidae, first and second internal transcribed spacers (ITS-1 and ITS-2) of nuclear ribosomal DNA, Nematoda, single-strand conformation polymorphism (SSCP) analysis.
References
Anderson, R. C. (2000). ‘Nematode Parasites of Vertebrates, their Development and Transmission.’ 2nd edn. (CAB International: Wallingford, UK.)Audicana, M. T., and Kennedy, M. W. (2008). Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews 21, 360–379.
| Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtFKlsrY%3D&md5=ec0d959c317ed9d3a2691f9948037e40CAS |
Audicana, M. T., Ansotegui, I. J., de Corres, L. F., and Kennedy, M. W. (2002). Anisakis simplex: dangerous – dead and alive? Trends in Parasitology 18, 20–25.
| Anisakis simplex: dangerous – dead and alive?Crossref | GoogleScholarGoogle Scholar |
Bruce, N. L. (1990a). Hysterothylacium Ward & Magath, 1917, and Ichthyascaris Wu, 1949, ascaridoid nematodes from Australian demersal fishes. Memoirs of the Queensland Museum 28, 389–426.
Bruce, N. L. (1990b). Redescription of the ascaridoid nematode Hysterothylacium scomberomori (Yamaguti) from Australian Spanish mackerel Scomberomorus commerson (Lacépède). Memoirs of the Queensland Museum 28, 427–434.
Bruce, N. L., and Cannon, L. R. G. (1989). Hysterothylacium, Iheringascaris and Maricostula new genus, nematodes (Ascaridoidea) from Australian pelagic marine fishes. Journal of Natural History 23, 1397–1441.
| Hysterothylacium, Iheringascaris and Maricostula new genus, nematodes (Ascaridoidea) from Australian pelagic marine fishes.Crossref | GoogleScholarGoogle Scholar |
Bruce, N. L., and Cannon, L. R. G. (1990). Ascaridoid nematodes from sharks from Australia and the Solomon Islands, southwestern Pacific Ocean. Invertebrate Taxonomy 4, 763–783.
| Ascaridoid nematodes from sharks from Australia and the Solomon Islands, southwestern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Bush, A. O., Lafferty, K. D., Lotz, J. M., and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.
| Parasitology meets ecology on its own terms: Margolis et al. revisited.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svht1OmsA%3D%3D&md5=7ddc5f65b90c64115b4e300d8946a433CAS |
Cannon, L. R. (1977a). Some ecological relationships of larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology 7, 227–232.
| Some ecological relationships of larval ascaridoids from south-eastern Queensland marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3islSnuw%3D%3D&md5=4e2a40466ef56be3fff6388dde36a77fCAS |
Cannon, L. R. (1977b). Some larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology 7, 233–243.
| Some larval ascaridoids from south-eastern Queensland marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3islSmsg%3D%3D&md5=430f141a3a833e6e8e227ed89c164317CAS |
Cole, A. J., Pratchett, M. S., and Jones, G. P. (2008). Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish and Fisheries 9, 286–307.
| Diversity and functional importance of coral-feeding fishes on tropical coral reefs.Crossref | GoogleScholarGoogle Scholar |
Damin, L., and Heqing, H. (2001). Heliconema minnanensis n. sp. (Physalopteroidae: Physalopteridae) and Raphidascaris trichiuri (Yin and Zhang) n. comb. (Ascaridoidea: Anisakidae) in marine fishes. The Journal of Parasitology 87, 1090–1094.
| 1:STN:280:DC%2BD3MnktlyhsA%3D%3D&md5=84481d30f1e2825de6441ff7311b3e09CAS |
Deardorff, T. L., and Overstreet, R. M. (1980). Review of Hysterothylacium and Iheringascaris (both previously = Thynnascaris) (Nematoda: Anisakidae) from the northern Gulf of Mexico. Proceedings of the Biological Society of Washington 93, 1035–1079.
Doupé, R. G., Lymbery, A. J., Wong, S., and Hobbs, R. P. (2003). Larval anisakid infections of some tropical fish species from north-west Australia. Journal of Helminthology 77, 363–365.
| Larval anisakid infections of some tropical fish species from north-west Australia.Crossref | GoogleScholarGoogle Scholar |
Gasser, R. B., Hu, M., Chilton, N. B., Campbell, B. E., Jex, A. J., Otranto, D., Cafarchia, C., Beveridge, I., and Zhu, X. (2006). Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nature Protocols 1, 3121–3128.
| Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGjt7vF&md5=12b16ee6802df4f5a5b6b8168800a476CAS |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=71d302d37bed8d2f0868dd79572b2183CAS |
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=ce960498bda333e27ce1994905bc3e6bCAS |
Iñiguez, A. M., Santos, C. P., and Vicente, A. C. (2009). Genetic characterization of Anisakis typica and Anisakis physeteris from marine mammals and fish from the Atlantic Ocean off Brazil. Veterinary Parasitology 165, 350–356.
| Genetic characterization of Anisakis typica and Anisakis physeteris from marine mammals and fish from the Atlantic Ocean off Brazil.Crossref | GoogleScholarGoogle Scholar |
Jabbar, A., Khoon, A. T., Hui, T. X., Schaeffner, B. C., Jex, A. R., Nolan, M. J., Lopata, A., Gasser, R. B., and Beveridge, I. (2012). Mutation scanning-based analysis of anisakid larvae from Sillago flindersi from Bass Strait, Australia. Electrophoresis 33, 499–505.
| Mutation scanning-based analysis of anisakid larvae from Sillago flindersi from Bass Strait, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtl2htLw%3D&md5=cbc197b05fa638657b1cd541082478d3CAS |
Jabbar, A., Fong, R. W., J. Kok, K. X., Lopata, A. L., Gasser, R. B., and Beveridge, I. (2012b). Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. International Journal of Food Microbiology (in Press).
Kasuya, S., Hamano, H., and Izumi, S. (1990). Mackerel-induced urticaria and Anisakis. Lancet 335, 665.
| Mackerel-induced urticaria and Anisakis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7ptVWitA%3D%3D&md5=ceb5c134011565feebb4378d76b99887CAS |
Kijewska, A., Dzido, J., Shukhgalter, O., and Rokicki, J. (2009). Anisakid parasites of fishes caught on the African shelf. The Journal of Parasitology 95, 639–645.
| Anisakid parasites of fishes caught on the African shelf.Crossref | GoogleScholarGoogle Scholar |
Kuhn, T., García-Màrquez, J., and Klimpel, S. (2011). Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS ONE 6, e28642.
| Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFajsw%3D%3D&md5=750b76ad3caa71a8e28abde92c11990bCAS |
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R., and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.
| Parasites in food webs: the ultimate missing links.Crossref | GoogleScholarGoogle Scholar |
Lopata, A. L., and Lehrer, S. B. (2009). New insights into seafood allergy. Current Opinion in Allergy and Clinical Immunology 9, 270–277.
| New insights into seafood allergy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt1ygtLo%3D&md5=a29787782a4d6c39d89ffa10534244a2CAS |
Lymbery, A. J., Doupé, R. G., Munshi, M. A., and Wong, T. (2002). Larvae of Contraceacum sp. among inshore fish species of southwestern Australia. Diseases of Aquatic Organisms 51, 157–159.
| Larvae of Contraceacum sp. among inshore fish species of southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38ngvVOmtw%3D%3D&md5=2473c59f2d37974f9e32c2170d431ff0CAS |
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124, S83–S99.
| Food webs and the transmission of parasites to marine fish.Crossref | GoogleScholarGoogle Scholar |
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theater. EcoHealth 1, 151–164.
| Parasites: small players with crucial roles in the ecological theater.Crossref | GoogleScholarGoogle Scholar |
Marnane, M., and Bellwood, D. R. (2002). Diet and nocturnal foraging in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef, Australia. Marine Ecology Progress Series 231, 261–268.
| Diet and nocturnal foraging in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |
Mattiucci, S., and Nascetti, G. (2006). Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13, 99–113.
| 1:STN:280:DC%2BD28zotl2itQ%3D%3D&md5=9ee1d9453375354ebda334fe7122328dCAS |
Mattiucci, S., and Nascetti, G. (2008). Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.
| Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes.Crossref | GoogleScholarGoogle Scholar |
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, C. M., Lo-Yat, A., Pichelin, S., and Sasal, P. (2000). Endoparasite species richness of New Caledonia butterfly fishes: host density and diet matter. Parasitology 121, 65–73.
| Endoparasite species richness of New Caledonia butterfly fishes: host density and diet matter.Crossref | GoogleScholarGoogle Scholar |
Muñoz, G., Grutter, A. S., and Cribb, T. H. (2007). Structure of the parasite communities of a coral reef fish assemblage (Labridae): testing ecological and phylogenetic host factors. The Journal of Parasitology 93, 17–30.
| Structure of the parasite communities of a coral reef fish assemblage (Labridae): testing ecological and phylogenetic host factors.Crossref | GoogleScholarGoogle 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 Host, 1932 (Nematoda:Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121, 455–463.
| Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda:Ascaridoidea) based on nuclear rDNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2ntro%3D&md5=6003d817e373906f881f5e9edfa66182CAS |
Nadler, S. A., D’Amelio, S., Dailey, M. D., Paggi, L., Siu, S., and Sakanari, J. A. (2005). Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. The Journal of Parasitology 91, 1413–1429.
| Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVGksLc%3D&md5=aae77bfee9ce268609e05a8b703ec8d7CAS |
Nash, J. A. (1998). The ecology of endoparasites of whiting, Sillago flindersi. The University of New England, Armidale, NSW.
Nieuwenhuizen, N., Lopata, A. L., Jeebhay, M. F., Herbert, D. R., Robins, T. G., and Brombacher, F. (2006). Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis. The Journal of Allergy and Clinical Immunology 117, 1098–1105.
| Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVOrsLs%3D&md5=ee5e01da7c2caca0b80acf38e7d5a4baCAS |
Palm, H. W., Linda, L., Damriyasa, I. M., and Oka, I. B. M. (2008). Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45, 3–12.
| Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvFSms7c%3D&md5=59f5dc72a297f3f9438864e35533a4c7CAS |
Posada, G., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=84f91ead5424fe4266d2c65de2bd77eeCAS |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=56f459c0687ddde2c29620b124592b42CAS |
Shamsi, S. (2007). Morphologic and genetic characterisation of selected ascaridoid nematodes. Ph.D. Thesis, The University of Melbourne.
Shamsi, S., and Butcher, A. R. (2011). First report of human anisakidosis in Australia. The Medical Journal of Australia 194, 199–200.
Shamsi, S., Gasser, R., Beveridge, I., and Alizadeh Shabani, A. (2008). Contracaecum pyripapillatum n. sp. (Nematoda: Anisakidae) and a description of C. multipapillatum (von Drasche, 1882) from the Australian pelican, Pelecanus conspicillatus. Parasitology Research 103, 1031–1039.
| Contracaecum pyripapillatum n. sp. (Nematoda: Anisakidae) and a description of C. multipapillatum (von Drasche, 1882) from the Australian pelican, Pelecanus conspicillatus.Crossref | GoogleScholarGoogle Scholar |
Shamsi, S., Eisenbarth, A., Saptarshi, S., Beveridge, I., Gasser, R. B., and Lopata, A. L. (2011a). Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitology Research 108, 927–934.
| Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters.Crossref | GoogleScholarGoogle Scholar |
Shamsi, S., Gasser, R., and Beveridge, I. (2011b). Mutation scanning-coupled sequencing of nuclear ribosomal DNA spacers as a tool for the specific identification of different Contracaecum (Nematoda: Anisakidae) larval types. Molecular and Cellular Probes 25, 13–18.
| Mutation scanning-coupled sequencing of nuclear ribosomal DNA spacers as a tool for the specific identification of different Contracaecum (Nematoda: Anisakidae) larval types.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ansbY%3D&md5=563ee05621864554f20f878524f0548fCAS |
Shamsi, S., Gasser, R., and Beveridge, I. (2012). Redescription and genetic characterisation of Anisakis spp. (Nematoda: Anisakidae) in selected Australian marine mammals. Invertebrate Systematics 26, 204–212.
| Redescription and genetic characterisation of Anisakis spp. (Nematoda: Anisakidae) in selected Australian marine mammals.Crossref | GoogleScholarGoogle Scholar |
Szostakowska, B., Myjak, P., Kur, J., and Sywula, T. (2001). Molecular evaluation of Hysterothylacium auctum (Nematoda, Ascaridida, Raphidascarididae) taxonomy from fish of the southern Baltic. Acta Parasitologica 46, 196–201.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=d5a3eb94a42b31811205d08353924da8CAS |
Umehara, A., Kawakami, Y., Araki, J., and Uchida, A. (2008). Multiplex PCR for the identification of Anisakis simplex sensu stricto, Anisakis pegreffii and the other anisakid nematodes. Parasitology International 57, 49–53.
| Multiplex PCR for the identification of Anisakis simplex sensu stricto, Anisakis pegreffii and the other anisakid nematodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlGiu7vK&md5=cd88cdee49175e3204843c557df7e72fCAS |
Umehara, A., Kawakami, Y., Ooi, H. K., Uchida, A., Ohmae, H., and Sugiyama, H. (2010). Molecular identification of Anisakis Type I larvae isolated from hairtail fish off the coasts of Taiwan and Japan. International Journal of Food Microbiology 143, 161–165.
| Molecular identification of Anisakis Type I larvae isolated from hairtail fish off the coasts of Taiwan and Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1CmurnJ&md5=1006965d5e7e2e74142a6662e09e6f34CAS |
Van Thiel, P. H. (1962). Anisakiasis. Parasitology 52, 16–17.
Yagi, K., Nagasawa, K., Ishikura, H., Nakagawa, A., Sato, N., Kikuchi, K., and Ishikura, H. (1996). Female worm Hysterothylacium aduncum excreted from human: a case report. Japanese Journal of Parasitology 45, 12–23.
Zhang, L., Hu, M., Shamsi, S., Beveridge, I., Li, H., Xu, Z., Li, L., Cantacessi, C., and Gasser, R. B. (2007). The specific identification of anisakid larvae from fishes from the Yellow Sea, China, using mutation scanning-coupled sequence analysis of nuclear ribosomal DNA. Molecular and Cellular Probes 21, 386–390.
| The specific identification of anisakid larvae from fishes from the Yellow Sea, China, using mutation scanning-coupled sequence analysis of nuclear ribosomal DNA.Crossref | GoogleScholarGoogle Scholar |
Zhu, X., Gasser, R. B., Podolska, M., and Chilton, N. B. (1998). Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal for Parasitology 28, 1911–1921.
| Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsF2jsA%3D%3D&md5=670f802ef293f0a66862e0f1e4620e22CAS |
Zhu, X. Q., Podolska, M., Liu, J. S., Yu, H. Q., Chen, H. H., Lin, Z. X., Luo, C. B., Song, H. Q., and Lin, R. Q. (2007). Identification of anisakid nematodes with zoonotic potential from Europe and China by single-strand conformation polymorphism analysis of nuclear ribosomal DNA. Parasitology Research 101, 1703–1707.
| Identification of anisakid nematodes with zoonotic potential from Europe and China by single-strand conformation polymorphism analysis of nuclear ribosomal DNA.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snpsVemtA%3D%3D&md5=fbe47aab1d37607be6c6cbd6d5a8bfd2CAS |