Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-26T15:25:56.786Z Has data issue: false hasContentIssue false
  • English
  • Français

Gaining insights into the ecological role of the New Zealand sole (Peltorhamphus novaezeelandiae) through parasites

Published online by Cambridge University Press:  20 April 2017

T. Anglade  and
H.S. Randhawa
T. Anglade
Affiliation:
Département de Biologie, École Normale Supérieure de Lyon, Site Jacques Monod, 46 Allée d'Italie, 69364 Lyon CEDEX 07, France
H.S. Randhawa*
Affiliation:
Ecology Degree Programme, University of Otago, PO Box 56, Dunedin, New Zealand, 9054
*
*E-mail: hrandhawa@fisheries.gov.fk
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the fact that tapeworms comprise the bulk of parasite communities of sharks in marine ecosystems, little is known about their life cycles and, more specifically, about the potential intermediate hosts they utilize as transmission routes. In the absence of morphological features required for specific identification of larval tapeworms from potential intermediate hosts, recent molecular advances have contributed to linking larval and adult parasites and, in some instances, uncovering unknown trophic links. Host–parasite checklists are often the first source of information consulted to assess the diversity and host specificity of parasites, and provide insights into parasite identification. However, these host–parasite checklists are only useful if they encompass the full spectrum of associations between hosts and parasites. A checklist of New Zealand fishes and their parasites has been published, but recent parasitological examinations of commercial fish species reveal that the checklist appears to be far from complete. We focused our current study on a comprehensive survey of macroparasites of a commercial species, the New Zealand sole (Peltorhamphus novaezeelandiae) off the coast of Otago, New Zealand. Specifically, we were expecting to recover marine tapeworms using sharks as their definitive hosts that are generally underreported in parasite surveys. The parasites recovered included tapeworms, flukes, round worms and thorny-headed worms. Surprisingly, a large proportion of the non-tapeworm parasites we recovered were not previously reported from this fish species. A discussion on the potential ecological roles played by this fish species in the transmission of parasites is included.

Type
Research Papers
Information
Journal of Helminthology , Volume 92 , Issue 2 , March 2018 , pp. 187 - 196
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

†

Current addresses: Directorate of Natural Resources, Fisheries Department, Falkland Islands Government, Bypass Road, Stanley, Falkland Islands, FIQQ 1ZZ; South Atlantic Environmental Institute, Stanley Cottage, Stanley, Falkland Islands, FIQQ 1ZZ; New Brunswick Museum, 277 Douglas Avenue, Saint John, New Brunswick, Canada, E2 K 1E5.

References

Alexander, C.G. (1963) Tetraphyllidean and diphyllidean cestodes of New Zealand selachians. Transactions of the Royal Society of New Zealand 3, 117–142.Google Scholar
Aznar, F.J., Agusti, C., Littlewood, D.T.J., Raga, J.A. & Olson, P.D. (2007) Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). International Journal for Parasitology 37, 243–255.Google Scholar
Baker, A.N. (1971) Food and feeding habits of the kahawai, Arripis trutta (Bloch & Schneider) (Teleostei, Arripidae). New Zealand Journal of Marine and Freshwater Research 5, 291–299.Google Scholar
Beveridge, I. & Campbell, R.A. (1996) New records and descriptions of trypanorhynch cestodes from Australian fishes. Records of the South Australian Museum 29, 1–22.Google Scholar
Bowman, R.E., Stillwell, C.E., Michaels, W.L. & Grosslein, M.D. (2000) Food of northwest Atlantic fishes and two common species of squid. NOAA Technical Memorandum NMFS-NE 155, 1–138.Google Scholar
Caira, J.N. & Healy, C.J. (2004) Elasmobranchs as hosts of metazoan parasites. pp. 523–551 in Musick, J.A., Carrier, J.C. & Heithaus, M.R. (Eds) Biology of sharks and their relatives. Boca Raton, CRC Press.Google Scholar
Caira, J.N. & Reyda, F.B. (2005) Eucestoda (true tapeworms). pp. 92–104 in Rohde, K. (Ed.) Marine parasitology. Collingwood, CSIRO Publishing.Google Scholar
Chervy, L. (2002) The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 1–33.Google Scholar
Compagno, L.J. (1984) Sharks of the world: an annotated and illustrated catalogue of sharks known to date. FAO Fisheries Synopsis No. 125, Vol 4. 655 pp. Rome, FAO.Google Scholar
Compagno, L.J., Ebert, D.A. & Smale, M.J. (1989) Guide to the sharks and rays of southern Africa. 160 pp. London, New Holland.Google Scholar
Cortés, E. (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.Google Scholar
Cox, G. & Francis, M. (1997) Sharks and rays of New Zealand. 64 pp. Christchurch, Canterbury University Press.Google Scholar
Deardorff, T.L. & Overstreet, R.M. (1980). Review of Hysterothylacium and Iberingascaris (both previously Thynnascaris) (Nematoda: Anisakidae) from the northern gulf of Mexico. Proceedings of the Biological Society of Washington 93, 1035–1079.Google Scholar
Devlin, C.M., Diamond, A.W. & Saunders, G.W. (2004) Sexing Arctic terns in the field and laboratory. Waterbirds 27, 314–320.CrossRefGoogle Scholar
Dunn, M.R., Connell, A.M, Stevens, D.W. & Horn, P.L. (2010) Diet of two large sympatric teleosts, the ling (Genypterus blacodes) and hake (Merluccius australis). PLoS One 5, e13647.Google Scholar
Ebert, D.A. (1991) Diet of the seven gill shark Notorynchus cepedianus in the temperate coastal waters of southern Africa. South African Journal of Marine Science 11, 565–572.Google Scholar
Ellis, J.R., Pawson, M.G. & Shackley, S.E. (1996) The comparative feeding ecology of six species of shark and four species of ray (Elasmobranchii) in the north-east Atlantic. Fishery Bulletin 101, 590–602.Google Scholar
Fadeev, N.S. (1960) [Some data on spiny dogfish from the eastern coast of southern Sakhalin. Izv.] TINRO 46, 217–249 (in Russian).Google Scholar
García-Varela, M. & Pérez-Ponce de León, G. (2008) Validating the systematic position of Profilicollis Meyer, 1931 and Hexaglandula Petrochenko, 1950 (Acanthocephala: Polymorphidae) using cytochrome c oxidase (cox 1). Journal of Parasitology 94, 212–217.CrossRefGoogle ScholarPubMed
Gomes, D.C., Knoff, M., Sao Clemente, S.C., Lanfredi, R.M. & Pinto, R.M. (2005) Taxonomic reports of Homeacanthoidea (Eucestoda: Trypanorhyncha) in lamnid and sphyrnid elasmobranchs collected off the coast of Santa Catarina, Brazil. Parasite 12, 15–22.Google Scholar
Grabda, J. & Slósarczyk, W. (1981) Parasites of marine fishes from New Zealand. Acta Parasitological et Piscatoria 11, 85–103.Google Scholar
Grémillet, D., Argentin, G., Schulte, B. & Culi, B.M. (1998) Flexible foraging techniques in breeding cormorants Phalacrocorax carbo and shags Phalacrocorax aristotelis: benthic or pelagic feeding? Ibis 140, 113–119.Google Scholar
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J.C. & Parker, G.A. (2009) When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.Google Scholar
Hanchet, S. (1991) Diet of the spiny dogfish, Squalus acanthias Linnaeus, on the east coast, South Island, New Zealand. Journal of Fish Biology 39, 313–323.Google Scholar
Harper, J.T. & Saunders, G.W. (2001) The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cahiers de Biologie Marine 42, 25–38.Google Scholar
Harvey, J.T. (1989) Food habits, seasonal abundance, size, and sex of the blue shark, Prionace glauca, in Monterey Bay, California. California Fish and Game 75, 33–44.Google Scholar
Hernández-Orts, J.S., Smales, L.R., Pinacho-Pinacho, C.D., García-Varela, M. & Presswell, B. (2017) Novel morphological and molecular data for Corynosoma hannae Zdzitowiecki, 1984 (Acanthocephala: Polymorphidae) from teleosts, fish-eating birds and pinnipeds from New Zealand. Parasitology International 66, 905–917.Google Scholar
Hewitt, G.C. & Hine, P.M. (1972) Checklist of parasites of New Zealand fishes and of their hosts. New Zealand Journal of Marine and Freshwater Research 6, 69–114.Google Scholar
Hine, P.M., Jones, J.B. & Diggles, B.K. (2000) A checklist of the parasites of New Zealand fishes, including previously unpublished records. 95 pp. Wellington, National Institute of Water and Atmospheric Research (NIWA).Google Scholar
Holden, M.J. (1966) The food of the spurdog, Squalus acanthias (L). ICES Journal of Marine Science 30, 255–266.Google Scholar
Horn, P.L., Forman, J.S. & Dunn, M.R. (2012) Dietary partitioning by two sympatric fish species, red cod (Pseudophycis bachus) and sea perch (Helicolenus percoides), on Chatham Rise, New Zealand. Marine Biology Research 8, 624–634.Google Scholar
Jensen, K. & Bullard, S.A. (2010) Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. International Journal for Parasitology 40, 889–910.Google Scholar
Jones, J.B. (1991) Movements of albacore tuna (Thunnus alalunga) in the South Pacific: evidence from parasites. Marine Biology 111, 1–9.Google Scholar
Joyeux, C. & Baer, J.G. (1936) Faune de France: Cestodes. Fédération Française des Sciences Naturelles 30, 1–613.Google Scholar
Køie, M. (1993) Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Canadian Journal of Zoology 71, 1289–1296.CrossRefGoogle Scholar
Korotaeva, V.D. (1975) [Contribution to the fauna of helminths and parasitic crustaceans of marine commercial fishes of the Australian and New Zealand region.] Trudy Academii Nauk SSR (Novaja Serija) 26, 46–60 (in Russian).Google Scholar
Knoff, M., Sao Clemente, S.C., Pinto, R.M., Lanfredi, R.M. & Gomes, D.C. (2004) Taxonomic reports of Otobothrioidea (Eucestoda, Trypanorhyncha) from elasmobranch fishes of the southern coast of Brazil. Memorias do Instituto Oswaldo Cruz 99, 31–36.Google Scholar
Lance, M.M., Orr, A.J., Riemer, S.D., Weise, M.J. & Leake, J.L. (2001) Pinniped food habits and prey identification technique protocol (AFSC Processed Report 2001–04). 36 pp. Seattle, National Oceanic and Atmospheric Administration (NOAA).Google Scholar
Lester, R.J.G., Barnes, A. & Habib, G. (1985) Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fishery Bulletin 83, 343–356.Google Scholar
Linton, E. (1905) Parasites of fishes of Beaufort, North Carolina. Bulletin of the United States Bureau of Fisheries (1904) 24, 321–428.Google Scholar
Manter, H.W. (1954) Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand 82, 475–568.Google Scholar
Manter, H.W. (1960) Some additional Digenea (Trematoda) from New Zealand fishes. pp. 197–201 in Libro homenaje al Dr. Eduardo Caballero y Caballero, Eduardo, Jubilero, 1930–1960. Secretaria de Educacion Publica, Mexico.Google Scholar
Mattiucci, S. & 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.Google Scholar
McFarlane, G.A., Beamish, R.J., Saunders, M.W., Smith, M.S. and Butler, T. (1984) Data for the biology and diet studies of spiny dogfish (Squalus acanthias) in Hecate Strait, B.C., August 1977 and June 1978. Canadian Data Report of Fisheries and Aquatic Sciences No. 443. 410 pp. Nainaimo, Department of Fisheries and Oceans.Google Scholar
McGinnis, S. & Madden, T.L. (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Research 32, W20–25.Google Scholar
Moore, P.J. & Wakelin, M.D. (1997) Diet of the yellow-eyed penguin Megadyptes antipodes, South Islands, New Zealand, 1991–1993. Marine Ornithology 25, 17–29.Google Scholar
Morisita, M. (1959) Measuring of the dispersion and analysis of distribution patterns. Memoires of the Faculty of Science, Kyushu University, Series E, Biology 2, 215–235.Google Scholar
Myers, R.A., Baum, J.K., Shepherd, T., Powers, S.P. & Peterson, C.H. (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.Google Scholar
Nadler, S.A. & Hudspeth, D.S.S. (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. Journal of Parasitology 86, 380–393.CrossRefGoogle ScholarPubMed
Nadler, S.A., D'Amelio, S., Dailey, M.D., Paggi, L., Siu, S. & Sakanari, J.A. (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. Journal of Parasitology 91, 1413–1429.Google Scholar
Navone, G.T., Sardella, N.H. & Timi, J.T. (1998) Larvae and adults of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda: Anisakidae) in fishes and crustaceans in the South West Atlantic. Parasite 5, 127–136.Google Scholar
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.M., Szoecs, E. & Wagner, H. (2016) Package ‘vegan’. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. R Package 3.2.2. Available at https://cran.r-project.org/web/packages/vegan/vegan.pdf (accessed 9 January 2017).Google Scholar
Palm, H.W. (1999) Nybelinia Poche, 1926, Heteronybelinia gen. nov. and Mixonybelinia gen. nov. (Cestoda: Trypanorhyncha) in the collections of the Natural History Museum, London. Bulletin of the Natural History Museum of London (Zoology Series) 65, 133–153.Google Scholar
Palm, H.W. & Beveridge, I. (2002) Tentaculariid cestodes of the order Trypanorhyncha (Platyhelminthes) from the Australian region. Records of the South Australian Museum 35, 49–78.Google Scholar
Palm, H.W. & Walter, T. (2005) Tentaculariid cestodes (Trypanorhyncha) from the Museum National d'Histoire Naturelle, Paris. Zoosystema 22, 641–666.Google Scholar
Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. & Thollesson, M. (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.Google Scholar
Poulin, R. (2007) Evolutionary ecology of parasites. 2nd edn. 332 pp. Princeton, Princeton University Press.Google Scholar
Poulin, R. & Keeney, D.B. (2008) Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28.Google Scholar
Poulin, R., Besson, A.A., Morin, M.B. & Randhawa, H.S. (2016a) Missing links: testing the completeness of host–parasite checklists. Parasitology 143, 114–122.Google Scholar
Poulin, R., Blasco-Costa, I. & Randhawa, H.S. (2016b) Integrating parasitology and marine ecology: seven challenges towards greater synergy. Journal of Sea Research 113, 3–10.Google Scholar
Rail, J.-F. & Chapdelaine, G. (1998) Food of the double-crested cormorants, Phalacrocorax auritus, in the Gulf and Estuary of the St. Lawrence River, Quebec, Canada. Canadian Journal of Zoology 76, 635–643.Google Scholar
Randhawa, H.S. (2011) Insights using a molecular approach into the life cycle of a tapeworm infecting great white sharks. Journal of Parasitology 97, 275–280.Google Scholar
Randhawa, H.S. & Brickle, P. (2011) Larval parasite gene sequence data reveal cryptic trophic links in the life cycle of porbeagle shark tapeworms. Marine Ecology Progress Series 431, 215–222.Google Scholar
Randhawa, H.S. & Poulin, R. (2010) Determinants of tapeworm species richness in elasmobranch fishes: untangling environmental and phylogenetic influences. Ecography 33, 866–877.Google Scholar
Randhawa, H.S., Saunders, G.W. & Burt, M.D.B. (2007) Establishment of the onset of host specificity in four phyllobothriid tapeworm species (Cestoda: Tetraphyllidea) using a molecular approach. Parasitology 134, 1291–1300.Google Scholar
Randhawa, H.S., Saunders, G.W., Scott, M.E. & Burt, M.D.B. (2008) Redescription of Pseudanthobothrium hanseni Baer, 1956 and description of P. purtoni n. sp. (Cestoda: Tetraphyllidea) from different pairs of rajid skate hosts, with comments on the host-specificity of the genus in the northwest Atlantic. Systematic Parasitology 70, 41–60.Google Scholar
R Development Core Team (2015) R: a language and environment for statistical computing. Version 3.2.2. Available at http://www.r-project.org (accessed 9 January 2017s).Google Scholar
Robinson, E.S. (1959) Records of cestodes from marine fishes of New Zealand. Transactions of the Royal Society of New Zealand 86, 143–153.Google Scholar
Russell, B. (1983) The food and feeding-habits of rocky reef fish of northeastern New Zealand. New Zealand Journal of Marine and Freshwater Research 17, 121–145.Google Scholar
Sao Clemente, S.C. & Gomes, D.C. (1992) Description of the adult form of Nybelinia (Syngenes) rougetcampanae Dollfus, 1960 and some new data on N. (N.) bisculata (Linton, 1889) (Trypanorhyncha: Tentaculariidae). Memorias Instituto Oswaldo Cruz (Suppl.) 1, 251–255.Google Scholar
Shiel, R.J., Smales, L., Sterrer, W., Duggan, I., Pichelin, S. & Green, J.D. (2009) Phylum Gnathifera: lesser jaw worms, rotifers, thorny-headed worms. pp. 134–156 in Gordon, D.P. (Ed.) Kingdom Animalia: Radiata, Lophotrochozoa, Deuterostomia. Christchurch, Canterbury University Press.Google Scholar
Szoboszlai, A.I., Thayer, J.A., Wood, S.A., Sydeman, W.J. & Koehn, L.E. (2015) Forage species in predator diets: synthesis of data from the California Current. Ecological Informatics 29, 45–56.Google Scholar
Tollit, D.J., Schulze, A.D., Trites, A.W., Olesiuk, P.F., Crockford, S.J., Gelatt, T.S., Ream, R.R. & Miller, K.M. (2009) Development and application of DNA techniques for validating and improving pinniped diet estimates. Ecological Applications 19, 889–905.Google Scholar
Vooren, C.M. & Tracey, D. (1976) Parasites in tarakihi (Pisces: Cheilodactylidae) from three areas around New Zealand. New Zealand Journal of Marine and Freshwater Research 10, 499–509.Google Scholar
Walther, B.A., Cotgreave, P., Price, R.D., Gregory, R.D. & Clayton, D.H. (1995) Sampling effort and parasite species richness. Parasitology Today 11, 306–310.Google Scholar
Williams, H. & Jones, A. (1994) Parasitic worms of fish. 593 pp. London, Taylor & Francis.Google Scholar
Zdzitowiecki, K. (1984) Some Antarctic acanthocephalans of the genus Corynosoma parasitizing Pinnipedia, with descriptions of three new species. Acta Parasitologica 29, 359–377.Google Scholar
Zdzitowiecki, K. & Presler, P. (2001) Occurrence of Acanthocephala in intermediate hosts, Amphipoda in Admirality Bay, south Shetland Islands, Antarctica. Polar Research 22, 205–212.Google Scholar
Zhang, J. (2016) Package ‘spaa’. Miscellaneous functions for analysing species association and niche overlap. R Package 3.2.2. Available at https://cran.r-project.org/web/packages/spaa/spaa.pdf (accessed 9 January 2017).Google Scholar