Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-24T13:10:48.088Z Has data issue: false hasContentIssue false
  • English
  • Français

The relationship between polychlorinated biphenyls in blubber and levels of nematode infestations in harbour porpoises, Phocoena phocoena

Published online by Cambridge University Press:  03 January 2006

J. C. BULL ,
P. D. JEPSON ,
R. K. SSUNA ,
R. DEAVILLE ,
C. R. ALLCHIN ,
R. J. LAW  and
A. FENTON
J. C. BULL
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY, UK
P. D. JEPSON
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY, UK
R. K. SSUNA
Affiliation:
Royal Veterinary College, London NW1 0TU, UK
R. DEAVILLE
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY, UK
C. R. ALLCHIN
Affiliation:
CEFAS, Burnham Laboratory, Remembrance Avenue, Burnham on Crouch, Essex CM0 8HA, UK
R. J. LAW
Affiliation:
CEFAS, Burnham Laboratory, Remembrance Avenue, Burnham on Crouch, Essex CM0 8HA, UK
A. FENTON
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY, UK School of Biological Sciences, Biosciences Building, Crown Street, University of Liverpool L69 7ZB, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Post-mortem examinations of harbour porpoises, Phocoena phocoena, regularly reveal heavy parasitic worm burdens. These same post-mortem records show varying levels of polychlorinated biphenyls (PCBs) accumulating in the blubber of porpoises. Although a number of papers have documented geospatial and temporal changes of PCBs and their detrimental effects on marine mammal health, as yet none have examined their role in determining nematode burdens in wild marine mammal populations. Using a data set consisting of harbour porpoises stranded in the UK between 1989 and 2002, we found a significant, positive association between PCB levels and nematode burdens, although the nature of the relationship was confounded with porpoise sex, age and cause of death. It was also apparent that individuals with the heaviest infestations of nematodes did not have the highest PCB level: while PCBs are important, they are clearly not the sole determinants of nematode burdens in wild populations of the harbour porpoise around the UK.

Keywords

harbour porpoisespolychlorinated biphenylsnematode burdensblubber
Type
Research Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 565 - 573
Copyright
2006 Cambridge University Press

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

Aguilar, A. and Borrell, A. ( 1994). Reproductive transfer and variation of body load of organochlorine pollutants with age in fin whales (Balaenoptera physalis). Archives of Environmental Contamination and Toxicology 27, 546–554.Google Scholar
Aguilar, A., Borrell, A. and Pastor, T. ( 1999). Biological factors affecting variability of persistent pollutant levels in cetaceans. Journal of Cetacean Research and Management (Special Issue 1) 83–116.Google Scholar
Akaike, H. ( 1973). Information theory and an extension of the maximum likelihood principle. In 2nd International Symposium on Information Theory ( ed. Petrov, B. N. and Csaki, F.), pp. 268–281. Publishing House of the Hungarian Academy of Science, Budapest.
Allchin, C. R., Kelly, C. A. and Portmann, J. E. ( 1989). Methods of Analysis for Chlorinated Hydrocarbons in Marine and Other Samples. Aquatic Environment Protection: Analytical Methods, Vol. 6, MAFF Directorate of Fisheries Research. Lowestoft, UK.
Anderson, R. M. and Gordon, D. M. ( 1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1995). Age-related changes in the rate of disease transmission: implications for the design of vaccination programmes. Journal of Hygiene 64, 365–436.Google Scholar
Baker, J. R. and Martin, A. R. ( 1992). Causes of mortality and parasites and incidental lesions in harbour porpoises (Phocoena phocoena) from British waters. Veterinary Record 130, 554–558.CrossRefGoogle Scholar
Bennett, P. M., Jepson, P. D., Law, R. J., Jones, B. R., Kuiken, T., Baker, J. R., Rogan, E. and Kirkwood, J. K. ( 2001). Exposure to heavy metals and infectious disease mortality in harbour porpoises from England and Wales. Environmental Pollution 112, 33–40.CrossRefGoogle Scholar
Bonsall, M. B. and Hastings, A. ( 2004). Demographic and environmental stochasticity in predator-prey metapopulation dynamics. Journal of Animal Ecology 73, 1043–1055.CrossRefGoogle Scholar
Bonsall, M. B., Bull, J. C., Pickup, N. J. and Hassell, M. P. ( 2005). Indirect effects and spatial scaling affect the persistence of multispecies metapopulations. Proceedings of the Royal Society of London, B 272, 1465–1471.CrossRefGoogle Scholar
Borrell, A. and Aguilar, A. ( 1990). Loss of organochlorine compounds in the tissues of a decomposing stranded dolphin. Bulletin of Environmental Contamination and Toxicology 45, 46–53.CrossRefGoogle Scholar
Borrell, A., Bloch, D. and Desportes, G. ( 1995). Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands. Environmental Pollution 88, 283–292.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. ( 2000). Model Selection and Inference: A Practical Information-Theoretic Approach. Springer, New York.
Crawley, M. J. ( 2002). Tree models. In Statistical Computing: An Introduction to Data Analysis Using S-Plus, chapter 31, pp. 581–593. John Wiley and Sons. Ltd, Chichester, UK.
Dailey, M. D. ( 1985). Diseases of Mammalia: Cetacea. In Diseases of Marine Animals, vol. 4, part 2, ( ed. Kinne, O.), pp. 805–845. Helgoland, Biologische Anstalt.
DETR ( 2000). Cetacean Strandings Investigation in Scotland. Project Report to the Department of the Environment, Transport and the Regions (Contract No. CRO179). The Scottish Agricultural College, Veterinary Science Division, Inverness, Scotland.
Dhermain, F., Soulier, L. and Bompar, J. M. ( 2002). Natural factors affecting cetaceans in the Mediterranean Sea. In Cetaceans of the Mediterranean and Black Seas: State of Knowledge and Conservation Strategies, section 15, p. 4. ACCOBAMS
Dierauf, L. A. ( 1990). Marine mammal parasitology. In Handbook of Marine Mammal Medicine ( ed. Dierauf, L. A.), chapter 4, pp. 89–90. CRC Press Inc., Boca Raton, Florida.
Duinker, J. C., Hillebrand, M. T. J., Zeinstra, T. and Boon, J. P. ( 1989). Individual chlorinated biphenyls and pesticides in tissues of some cetacean species from the North Sea and the Atlantic Ocean; tissue distribution and biotransformation. Aquatic Mammals 15, 95–124.Google Scholar
Evans, P. G. H. ( 1991). Whales, dolphins and porpoises: order Cetacea. In The Handbook of British Mammals ( ed. Corbet, G. B. and Harris, S.), pp. 299–350. Blackwell, Oxford.
Falyandysz, J., Yamashita, N., Tanabe, S., Tatsukawa, R., Rucinska, L. and Skora, K. ( 1994). Congener-specific data on polychlorinated-biphenyls in tissues of common porpoise from Puck Bay, Baltic Sea. Archives of Environmental Contamination and Toxicology 26, 267–272.CrossRefGoogle Scholar
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. L. ( 1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
Hammond, P., Benke, H., Berggren, P., Collet, A., Heide-Jørgensen, M. P., Heimlich-Boran, S., Leopold, M. and Øien, N. ( 1995). The distribution and abundance of harbour porpoises and other small cetaceans in the North Sea and adjacent waters. International Council for the Exploration of the Seas Report. Sea Mammal Research Unit, Fife, UK.
Hutchinson, J. and Simmonds, M. ( 1994). Organochlorine contamination in pinnipeds. Reviews in Environmental Contamination and Toxicology 136, 123–167.CrossRefGoogle Scholar
Jauniaux, T., Petitjean, D., Brenez, C., Borrens, M., Brosens, L., Haelters, J., Tavernier, T. and Coignoul, F. ( 2002). Post-mortem findings and causes of death of harbour porpoises (Phocoena phocoena) stranded from 1990 to 2000 along the coastlines of Belgium and Northern France. Journal of Comparative Pathology 126, 243–253.CrossRefGoogle Scholar
Jepson, P. D. ( 2003). Pathology and toxicology of stranded harbour porpoises (Phocoena phocoena) in UK waters. PhD thesis. Royal Veterinary College, University of London, UK.
Jepson, P. D., Bennett, P. M., Allchin, C. R., Law, R. J., Kuiken, T., Baker, J. R., Rogan, E. and Kirkwood, J. K. ( 1999). Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. The Science of the Total Environment 243, 339–348.CrossRefGoogle Scholar
Jepson, P. D., Baker, J. R., Kuiken, T., Simpson, V. R., Kennedy, S. and Bennett, P. M. ( 2000). Pulmonary pathology of harbour porpoises stranded in England and Wales between 1990 and 1996. Veterinary Record 146, 721–728.CrossRefGoogle Scholar
Jepson, P. D., Bennet, P. M., Deaville, R., Allchin, C. R., Baker, J. R. and Law, R. J. ( 2005). Relationships between polychlorinated biphenyls and health status in harbour porpoises (Phocoena phocoena) stranded in the United Kingdom. Environmental Toxicology and Chemistry 24, 238–248.CrossRefGoogle Scholar
Kannan, K., Blakenship, A. L., Jones, P. D. and Giesy, J. P. ( 2000). Toxicity reference values for the toxic effects of polychlorinated biphenyls to aquatic mammals. Human and Ecological Risk Assessment 6, 181–201.CrossRefGoogle Scholar
Kirkwood, J. K., Bennett, P. M., Jepson, P. D., Kuiken, T., Simpson, V. R. and Baker, J. R. ( 1997). Entanglement in fishing gear and other causes of death in cetaceans stranded on the coasts of England and Wales. Veterinary Record 141, 94–98.CrossRefGoogle Scholar
Kleivane, L., Skaare, J. U., Bjorge, A., DeRuiter, E. and Reijnders, P. J. H. ( 1995). Organochlorine pesticide-residue and PCBs in harbour porpoise (Phocoena phocoena) incidentally caught in Scandinavian waters. Environmental Pollution 89, 137–146.CrossRefGoogle Scholar
Kuiken, T., Höfle, U., Bennett, P. M., Allchin, C. R., Kirkwood, J. K., Baker, J. K., Appleby, E. C., Lockyer, C. H., Walton, M. J. and Sheldrick, M. C. ( 1993). Adrenocortical hyperplasia, disease and chlorinated hydrocarbons in the harbour porpoise (Phocoena phocoena). Marine Pollution Bulletin 26, 440–446.CrossRefGoogle Scholar
Kuiken, T., Bennett, P. M., Allchin, C. R., Kirkwood, J. K., Baker, J. R., Lockyer, C. H., Walton, M. J. and Sheldrick, M. C. ( 1994). PCBs, cause of death and body condition in harbour porpoises (Phocoena phocoena) from British waters. Aquatic Toxicology 28, 13–28.CrossRefGoogle Scholar
Law, R. J. ( 1994). (compiler) Collaborative UK marine mammal project: summary of data produced 1988–1992. Fisheries Research Technical Report97Lowestoft: MAFF Directorate of Fisheries Research.
Law, R. J., Fileman, C. F., Hopkins, A. D., Baker, J. R., Harwood, J., Jackson, D. B., Kennedy, S., Martin, A. R. and Morris, R. J. ( 1991). Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles. Marine Pollution Bulletin 22, 183–191.CrossRefGoogle Scholar
Law, R. J. and Whinnett, J. A. ( 1992). Polycyclic aromatic hydrocarbons in muscle tissue of harbour porpoises (Phocoena phocoena) from UK waters. Marine Pollution Bulletin 24, 550–553.CrossRefGoogle Scholar
Law, R. J., Blake, S. J., Jones, B. R. and Rogan, E. ( 1998). Organotin compounds in liver tissues of harbour porpoises (Phocoena phocoena) and grey seals (Halichoerus grypus) from the coastal waters of England and Wales. Marine Pollution Bulletin 36, 241–247.CrossRefGoogle Scholar
Law, R. J., Allchin, C. R., Bennett, M. E., Morris, S. and Rogan, E. ( 2002). Polybrominated diphenyl ethers in two species of marine top predators from England and Wales. Chemosphere 46, 673–681.CrossRefGoogle Scholar
Lockyer, C. ( 1995). Investigation of aspects of the life history of the harbour porpoise, Phocoena phocoena, in British waters. In The Biology of the Phocoenids Report of the International Whaling Commission ( ed. Bjørge, A. and Donovan, G. P.), Special Issue 16, pp. 189–197.
Pacala, S. W. and Dobson, A. P. ( 1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle Scholar
Pinheiro, J. C. and Bates, D. M. ( 2000). Mixed Effects Models in S and S-Plus. Springer, New York.CrossRef
Safe, S. H. ( 1994). Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Critical Reviews in Toxicology 24, 87–149.CrossRefGoogle Scholar
Siebert, U., Wünschmann, A., Weiss, R., Frank, H., Benke, H. and Frese, K. ( 2001). Postmortem findings in harbour porpoises (Phocoena phocoena) from the German North and Baltic Seas. Journal of Comparative Pathology 124, 102–114.CrossRefGoogle Scholar
Tanabe, S., Iwata, H. and Tatsukawa, R. ( 1994). Global contamination by persistent organochlorines and their ecotoxicological impact on marine mammals. Science of the Total Environment 154, 163–177.CrossRefGoogle Scholar
van Scheppingen, W. B., Verhoeven, A. J. I. M., Mulder, P., Addink, M. J. and Smeenk, C. ( 1996). Polychlorinated-biphenyls, dibenzo-p-dioxins, and dibenzofurans in harbor porpoises (Phocoena phocoena) stranded on the Dutch coast between 1990 and 1993. Archives of Environmental Contamination and Toxicology 30, 492–502.CrossRefGoogle Scholar
Westgate, A. J., Muir, D. C. G., Gaskin, D. E. and Kingsley, M. C. S. ( 1997). Concentrations and accumulation patterns of organochlorine contaminants in the blubber of harbour porpoises, Phocoena phocoena, from the coast of Newfoundland, the Gulf of St Lawrence and the Bay of Fundy Gulf of Maine. Environmental Pollution 95, 105–119.CrossRefGoogle Scholar
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. ( 2003). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A.), chapter 3, pp. 6–44. Oxford University Press, Oxford.