Hydrobiologia

, Volume 734, Issue 1, pp 187–199 | Cite as

The haematophagous feeding stage of anadromous populations of sea lamprey Petromyzon marinus: low host selectivity and wide range of habitats

  • Sergio Silva
  • Mário J. Araújo
  • Miguel Bao
  • Gonzalo Mucientes
  • Fernando Cobo
Primary Research Paper

Abstract

Limited information is available regarding habitat use and host species of the haematophagous feeding stage of the anadromous sea lamprey Petromyzon marinus Linnaeus, 1758, due to the difficulties in capturing feeding lampreys and wounded hosts. The aim of this study is to provide new records of P. marinus feeding on host species and to review the available information in this regard to better know the ecology and distribution of sea lamprey during this stage. Thus, new records of P. marinus individuals or wounds on 23 species of fishes and cetaceans are provided. Nineteen of these species were described for the first time as hosts of P. marinus. As a result, an updated list of 54 host species is provided. They belong to diverse taxonomic groups and exhibit different morphological, physiological and ecological patterns. The attacks were located from fresh and brackish waters to open sea. The results suggest that the marine distribution of P. marinus is mainly related to coastal areas with part of the population widely dispersed in offshore areas. This remarkable capacity of inhabiting a broad range of aquatic ecosystems and exploiting different host species could have favoured the dispersal ability and evolutionary success of sea lamprey.

Keywords

Parasite-host interaction Distribution Trophic ecology North Atlantic Ocean Fisheries Sea 

Supplementary material

Online resource 1 First evidence of Petromyzon marinus feeding on Prionace glauca (MP4 81666 kb)

References

  1. Araújo, M. J., D. Novais & C. Antunes, 2013a. Record of a newly metamorphosed anadromous sea lamprey (Petromyzon marinus Linnaeus, 1758) feeding on a freshwater fish. Journal of Applied Ichthyology 29: 1380–1381.CrossRefGoogle Scholar
  2. Araújo, M. J., R. O. A. Ozório, R. J. B. Bessa, A. Kijjoa, J. F. M. Gonçalves & C. Antunes, 2013b. Nutritional status of adult sea lamprey (Petromyzon marinus Linnaeus, 1758) during spawning migration in the Minho River, NW Iberian Peninsula. Journal of Applied Ichthyology 29: 808–814.CrossRefGoogle Scholar
  3. Beamish, F. W. H., 1980. Biology of the North American anadromous sea lamprey, Petromyzon marinus. Canadian Journal of Fisheries and Aquatic Sciences 37: 1924–1943.CrossRefGoogle Scholar
  4. Bence, J. R., R. A. Bergstedt, G. C. Christie, P. A. Cochran, M. P. Ebener, J. F. Koonce, M. A. Rutter & W. D. Swink, 2003. Sea lamprey (Petromyzon marinus) parasite host interactions in the Great Lakes. Journal of Great Lakes Research 29: 253–282.CrossRefGoogle Scholar
  5. Benz, G. & S. A. Bullard, 2004. Metazoan parasites and associates of chondrichthyans with emphasis on taxa harmful to captive hosts. In Smith, M., D. Warmolts, D. Thoney & R. Hueter (eds), The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays, and Their Relatives. Ohio Biological Survey, Columbus, OH: 325–416.Google Scholar
  6. Bergstedt, R. A. & W. D. Swink, 1995. Seasonal growth and duration of the parasitic life stage of landlocked sea lampreys (Petromyzon marinus). Canadian Journal of Fisheries and Aquatic Sciences 52: 1257–1264.CrossRefGoogle Scholar
  7. BOPDEPO, 2013. Boletín oficial provincia de Pontevedra, No 152. Deputación de Pontevedra.http://www.bop.depo.es/bop.PONTEVEDRA/2013/bop.PONTEVEDRA.20130809.152.pdf. Accessed 9 August 2013.
  8. Clemens, B. J., T. R. Binder, M. F. Docker, M. L. Moser & S. A. Sower, 2010. Similarities, differences, and unknowns in biology and management of three parasitic lampreys of North America. Fisheries 35: 580–594.CrossRefGoogle Scholar
  9. Cobo, F., S. Silva, R. Vieira-Lanero, M. J. Servia, J. Sánchez-Hernández, S. Barca, S. Rivas, M. Couto, P. Gómez, D. J. Nachón, C. Morquecho, L. Lago & M. C. Cobo, 2010. Estado de conservación das poboacións de lamprea mariña en ríos de Galicia. Xunta de Galicia, Consellería do Medio Rural, Dirección Xeral de Conservation da Natureza, Santiago de Compostela.Google Scholar
  10. Cochran, P. A., 1986. Attachment sites of parasitic lampreys: comparisons among species. Environmental Biology of Fishes 17: 71–79.CrossRefGoogle Scholar
  11. Cochran, P. A. & J. Lyons, 2010. Attachments by parasitic lampreys within the branchial cavities of their hosts. Environmental Biology of Fishes 88: 343–348.CrossRefGoogle Scholar
  12. Dempson, J. B. & T. R. Porter, 1993. Occurrence of sea lamprey, Petromyzon marinus, in a Newfoundland river, with additional records from the northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 50: 1265–1269.CrossRefGoogle Scholar
  13. Ebener, M. P., E. L. King, Jr. & T. A. Edsall, 2006. Application of a dichotomous key to the classification of sea lamprey marks on Great Lakes fish. Great Lakes Fish Com Misc Publ. http://www.glfc.org/pubs/SpecialPubs/2006-02.pdf. Accessed 9 August 2013.
  14. Farmer, G. J., 1980. Biology and physiology of feeding in adult lampreys. Canadian Journal of Fisheries and Aquatic Sciences 37: 1751–1761.CrossRefGoogle Scholar
  15. Farmer, G. J. & F. W. H. Beamish, 1973. Sea lamprey (Petromyzon marinus) predation on freshwater teleosts. Journal of the Fisheries Research Board of Canada 30: 601–605.CrossRefGoogle Scholar
  16. Froese, R. & D. Pauly (eds), 2011. FishBase version 12/2013. World Wide Web electronic publication. http://www.fishbase.org. Accessed 10 August 2013.
  17. Gallant, J., C. Harvey-Clark, R. A. Myers & M. J. W. Stokesbury, 2006. Sea lamprey attached to a Greenland Shark in the St. Lawrence Estuary. Canada. Northeastern Naturalist 13: 35–38.CrossRefGoogle Scholar
  18. García-Orellán, R., 2010. Terranova: The Spanish Cod Fishery on the Grand Banks of New-Foundland in the Twentieth Century. BrownWalker Press, Boca Raton.Google Scholar
  19. Genner, M. J., R. Hillman, M. McHugh, S. J. Hawkins & M. C. Lucas, 2012. Contrasting demographic histories of European and North American sea lamprey (Petromyzon marinus) populations inferred from mitochondrial DNA sequence variation. Marine & Freshwater Research 63: 827–833.CrossRefGoogle Scholar
  20. González-Costas, F., D. González-Troncoso, G. Ramilo, E. Román, J. Lorenzo, M. Casas, C. Gonzalez, A. Vázquez & M. Sacau, 2013. Scientific Council meeting – June 2013, Spanish Research Report for 2012, NAFO SCS Doc. 13/07 – Serial No N6150. http://digital.csic.es/bitstream/10261/86585/1/scs13-07.pdf. Accessed 9 August 2013.
  21. Haedrich, R. C., 1977. A sea lamprey from the deep. Copeia 4: 767–768.CrossRefGoogle Scholar
  22. Halliday, R. G., 1991. Marine distribution of the sea lamprey (Petromyzon marinus) in the northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 48: 832–842.CrossRefGoogle Scholar
  23. Hardisty, M. W., 1986. Petromyzon marinus (Linnaeus 1758). In Holčík, J. (ed.), The Freshwater Fishes of Europe, Vol 1 Part 1 – Petromyzontiformes, Vol. 1. Aula-Verlag, Wiesbaden: 94–116.Google Scholar
  24. Hardisty, M. W., 2006. Lampreys: Life without Jaws. Forrest Text, Ceredigion.Google Scholar
  25. Hardisty, M. W. & I. C. Potter, 1971. The general biology of adult lampreys. In Hardisty, M. W. & I. C. Potter (eds), The Biology of Lampreys, Vol. 1. Academic Press, London: 127–206.Google Scholar
  26. Heyning, J. E., 2003. Cuvier’s Beaked Whale (Ziphius cavirostris). In Perrin, W. F., B. Würsig & J. G. M. Thewissen (eds), Encyclopedia of Marine Mammal. Academic Press, San Diego, CA: 305–307.Google Scholar
  27. Holčík, J., 1986. The freshwater fishes of Europe, Vol. 1 Part I – Petromyzontiformes, Vol. 1. Aula-Verlag, Wiesbaden.Google Scholar
  28. Hume, J. B., C. E. Adams, C. W. Bean & P. E. Maitland, 2013. Evidence of a recent decline in lampreys parasitism of a nationally rare whitefish Coregonus clupeoides in Loch Lomond, Scotland: is there a diamond in the ruffe? Journal of Fish Biology 82: 1708–1716.PubMedCrossRefGoogle Scholar
  29. Hurrell, J. W., Y. Kushnir, G. Ottersen & M. Visbeck, 2003. The North Atlantic Oscillation: climatic significance and environmental impact. Geophysical Monograph Series. doi:10.1029/GM134.Google Scholar
  30. Igoe, F., D. T. G. Quigley, F. Marnell, E. Meskell, W. O’Connor & C. Byrne, 2004. The sea lamprey Petromyzon marinus (L.), river lamprey Lampetra fluviatilis (L.) and brook lamprey Lampetra planeri (Bloch) in Ireland: General biology, ecology, distribution and status with recommendations for conservation. Proceedings of the Royal Irish Academy, Section B 104: 43–56.CrossRefGoogle Scholar
  31. Inger, R., R. A. McDonald, D. Rogowski, A. L. Jackson, A. Parnell, S. J. Preston, C. Harrod, C. Goodwin, D. Griffiths, J. T. A. Dick, R. W. Elwood, J. Newton & S. Bearhop, 2010. Do non-native invasive fish support elevated lamprey populations? Journal of Applied Ecology 47: 121–129.CrossRefGoogle Scholar
  32. IUCN, 2013. IUCN Red List of Threatened Species. Version 2013.2. http://www.iucnredlist.org. Accessed 20 December 2013.
  33. Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner & R. R. Warner, 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–638.PubMedCrossRefGoogle Scholar
  34. Japha, A., 1910. Further contributions to the knowledge of whale skin. Zoologische Jahrbuecher 12: 711–718.Google Scholar
  35. Jensen, C. & F. J. Schwartz, 1994. Atlantic Ocean occurrences of the sea lamprey, Petromyzon marinus (Petromyzontiformes, Petromyzontidae), parasitizing sandbar, Carcharhinus plumbeus, and dusky, C. obscurus (Carcharhiniformes: Carcharhinidae), sharks off North and South Carolina. Brimleyana 21: 69–72.Google Scholar
  36. Jensen, C., F. J. Schwartz & G. Hopkins, 1998. A sea lamprey (Petromyzon marinus)-tiger shark (Galeocerdo cuvier) parasitic relationship off North Carolina. Journal of the Elisha Mitchell Scientific Society 114: 72–73.Google Scholar
  37. Johnson, B. G. H. & W. C. Anderson, 1980. Predatory-phase sea lampreys (Petromyzon marinus) in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 37: 2007–2020.CrossRefGoogle Scholar
  38. Kelly, F. L. & J. J. King, 2001. A review of the ecology and distribution of three lamprey species, Lampetra fluviatilis (L.), Lampetra planeri (Bloch) and Petromyzon marinus (L.): a context for conservation and biodiversity considerations in Ireland. Biology and Environment: Proceedings of the Royal Irish Academy 101B: 165–185.Google Scholar
  39. King, E. L. Jr. & T. A. Edsall, 1979. Illustrated field guide for the classification of sea lamprey attack marks on great lakes lake trout. Great Lakes Fishery Commission – Special Publication, 79-1.Google Scholar
  40. Lança, M. J., M. Machado, R. Ferreira, I. Alves-Pereira, B. R. Quintella & P. R. Almeida, 2013. Feeding strategy assessment through fatty acid profiles in muscles of adult sea lampreys from the western Iberian coast. Scientia Marina 77: 281–291.CrossRefGoogle Scholar
  41. Lelek, A., 1973. Occurrence of the sea lamprey in midwater off Europe. Copeia 1: 136–137.CrossRefGoogle Scholar
  42. Mansueti, J., 1962. Distribution of small, newly metamorphosed sea lampreys, Petromyzon marinus, and their parasitism on men-haden, Brevoortia tyrannus, in mid-Chesapeake Bay during winter months. Chesapeake Science 3: 137–139.CrossRefGoogle Scholar
  43. McAlpine, D., 2003. Pygmy and Dwarf Sperm Whales (Kogia breviceps and K. sima) In: Perrin W. F., B. Würsig & J. G. M. Thewissen (eds), Encyclopedia of Marine Mammal. Academic Press, San Diego, CA: 1007–1009.Google Scholar
  44. Meckley, T. D., C. M. Wagner & E. Gurarie, 2014. Coastal movements of migrating sea lamprey (Petromyzon marinus) in response to a partial pheromone added to river water: implications for management of invasive populations. Canadian Journal of Fisheries and Aquatic Sciences 71: 533–544.CrossRefGoogle Scholar
  45. Murauskas, J. G., A. M. Orlov & K. A. Siwicke, 2013. Relationships between the abundance of Pacific lamprey in the Columbia River and their common hosts in the marine environment. Transactions of the American Fisheries Society 142: 143–155.CrossRefGoogle Scholar
  46. Nichols, O. C. & P. K. Hamilton, 2004. Occurrence of the parasitic sea lamprey, Petromyzon marinus, on western North Atlantic right whales, Eubalaena glacialis. Environmental Biology of Fishes 71: 413–417.CrossRefGoogle Scholar
  47. Nichols, O. C. & U. T. Tscherter, 2011. Feeding of sea lampreys Petromyzon marinus on minke whales Balaenoptera acutorostrata in the St Lawrence Estuary. Journal of Fish Biology 78: 338–343.PubMedCrossRefGoogle Scholar
  48. Ólafsdóttir, D. & A. P. Shinn, 2013. Epibiotic macrofauna on common minke whales, Balaenoptera acutorostrata Lacépède, 1804, in Icelandic waters. Parasites & Vectors 6: 105.CrossRefGoogle Scholar
  49. Orlov, A. M., R. K. Beamish, A. V. Vinnikov & D. Pelenev, 2009. Feeding and prey of Pacific Lamprey in coastal waters of the western North Pacific. In: Haro, A., K. L. Smith, R. A. Rulifson, C. M. Moffitt, R. J. Klauda, M. J. Dadswell, R. A. Cunjak, J. E. Cooper, K. L. Beal & T. S. Avery (eds), Challenges For Diadromous Fishes In A Dynamic Global Environment. American Fisheries Society Symposium 69. Bethesda, Maryland: 875–877.Google Scholar
  50. Orlov, A. M., V. F. Savinykh & D. V. Pelenev, 2008. Features of spatial distribution and size composition of Pacific lamprey Lampetra tridentata in the North Pacific. Russian Journal of Marine Biology 34: 276–287.CrossRefGoogle Scholar
  51. Pauly, D., V. Christensen, J. Dalsgaard, R. Froese & F. Torres Jr., 1998. Fishing down marine food webs. Science 279: 860–863.PubMedCrossRefGoogle Scholar
  52. Pereira, A. M., B. Jonsson, M. Johannsson, J. I. Robalo & V. C. Almada, 2012. Icelandic lampreys (Petromyzon marinus): where do they come from? Ichthyological Research 59: 83–85.CrossRefGoogle Scholar
  53. Potter, C. & F. W. H. Beamish, 1977. The freshwater biology of adult anadromous sea lampreys Petromyzon marinus. Journal of Zoology 181: 113–130.CrossRefGoogle Scholar
  54. Powell, K., J. G. Trial, N. Dubé & M. Opitz, 1999. External parasite infestation of sea-run Atlantic salmon (Salmo salar) during spawning migration in the Penobscot River, Maine. Northeastern Naturalist 6: 363–370.CrossRefGoogle Scholar
  55. Quintella, B. R., N. O. Andrade & P. R. Almeida, 2003. Distribution, larval stage duration and growth of the sea lamprey ammocoetes, Petromyzon marinus L., in a highly modified river basin. Ecology of Freshwater Fish 12: 286–293.CrossRefGoogle Scholar
  56. Quintella, B. R., N. O. Andrade, A. Koed & P. R. Almeida, 2004. Behavioural patterns of sea lampreys’ spawning migration through difficult passage areas, studied by electromyogram telemetry. Journal of Fish Biology 65: 961–972.CrossRefGoogle Scholar
  57. Renaud, C. B., 2011. Lampreys of the world: an annotated and illustrated catalogue of lamprey species known to date. FAO Species Catalogue for Fisheries Purposes No. 5. Rome, FAO 2011.Google Scholar
  58. Renaud, C. B., H. S. Gill & I. C. Potter, 2009. Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lamprey. Journal of Zoology 278: 231–242.CrossRefGoogle Scholar
  59. Rodríguez-Muñoz, R., J. R. Waldman, C. Grunwald, N. K. Roy & I. Wirgin, 2004. Absence of shared mitochondrial DNA haplotypes between sea lamprey from North American and Spanish rivers. Journal of Fish Biology 64: 783–787.CrossRefGoogle Scholar
  60. Samarra, F. I. P., A. Fennell, K. Aoki, V. B. Deeck & P. J. O. Miller, 2012. Persistence of skin marks on killer whales (Orcinus orca) caused by the parasitic sea lamprey (Petromyzon marinus) in Iceland. Marine Mammal Science 28: 395–401.CrossRefGoogle Scholar
  61. Silva, S., R. Vieira-Lanero, J. Sánchez-Hernández, M. J. Servia & F. Cobo, in press. Accidental introduction of anadromous sea lampreys (Petromyzon marinus Linnaeus, 1758) into a European reservoir. Limnetica. Google Scholar
  62. Silva, S., M. J. Servia, R. Vieira-Lanero, S. Barca & F. Cobo, 2013a. Life cycle of the sea lamprey Petromyzon marinus: duration of and growth in the marine life stage. Aquatic Biolology 18: 59–62.CrossRefGoogle Scholar
  63. Silva, S., M. J. Servia, R. Vieira-Lanero & F. Cobo, 2013b. Downstream migration and hematophagous feeding of newly metamorphosed sea lampreys (Petromyzon marinus Linnaeus, 1758). Hydrobiologia 700: 277–286.CrossRefGoogle Scholar
  64. Silva, S., M. J. Servia, R. Vieira-Lanero, D. J. Nachón & F. Cobo, 2013c. Haematophagous feeding of newly metamorphosed European sea lampreys Petromyzon marinus on strictly freshwater species. Journal of Fish Biology 82: 1739–1745.PubMedCrossRefGoogle Scholar
  65. Spice, E. K., D. H. Goodman, S. B. Reid & M. F. Docker, 2012. Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey. Molecular Ecology 21: 2916–2930.PubMedCrossRefGoogle Scholar
  66. Taverny, C. & P. Elie, 2010. Les lamproies en Europe de l’Ouest: écophases, espèces et habitats. Quae, Versailles.Google Scholar
  67. van Utrecht, W. L., 1959. Wounds and scars in the skin of the common porpoise Phocaena phocaena (L.). Mammalia 13: 100–122.Google Scholar
  68. Waldman, J. R., C. Grunwald & I. Wirgin, 2008. Sea lamprey Petromyzon marinus: an exception to the rule of homing in anadromous fishes. Biology Letters 4: 659–662.PubMedCentralPubMedCrossRefGoogle Scholar
  69. Wilkie, M. P., S. Turnbull, J. Bird, Y. S. Wang, J. F. Claude & J. H. Youson, 2004. Lamprey parasitism of sharks and teleosts: high capacity urea excretion in an extant vertebrate relic. Comparative Biochemistry and Physiology 138A: 485–492.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Sergio Silva
    • 1
    • 2
  • Mário J. Araújo
    • 3
  • Miguel Bao
    • 4
  • Gonzalo Mucientes
    • 5
    • 6
  • Fernando Cobo
    • 1
    • 2
  1. 1.Department of Zoology and Physical Anthropology, Faculty of BiologyUniversity of Santiago de CompostelaSantiago de CompostelaSpain
  2. 2.Hydrobiology Station ‘Encoro do Con’Vilagarcía de ArousaSpain
  3. 3.CIMAR-LA/CIIMAR Interdisciplinary Centre of Marine and Environmental ResearchPortoPortugal
  4. 4.ECOBIOMAR, Instituto de Investigaciones Marinas (CSIC)VigoSpain
  5. 5.Grupo de Ecología PesqueraInstituto de Investigaciones Marinas (CSIC)VigoSpain
  6. 6.Centro de Investigação em Biodiversidade e Recursos GenéticosCIBIO – Universidade de PortoVairãoPortugal

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