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Dentinal anomalies in teeth of harbour porpoises (Phocoena phocoena) from Scottish waters: are they linked to sexual maturation and environmental events?

Published online by Cambridge University Press:  27 May 2009

P.L. Luque*
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK Facultade de Ciencias do Mar, Campus Universitario Lagoas-Marcosende, 36200 Vigo, Spain
G.J. Pierce
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
J.A. Learmonth
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
M.B. Santos
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK Instituto Español de Oceanografía, Centro Costero de Vigo, Cabo Estay, Canido, 36200 Vigo, Spain
E. Ieno
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK Highland Statistics Ltd, 6 Laverock Road, Newburgh, Ellon, Aberdeenshire, AB41 6FN, UK
A. López
Affiliation:
CEMMA (Coordinadora para o Estudio dos Mamíferos Mariños), R/Tomás Mirambell 90 Paxón, 36340, Nigran, Pontevedra (Spain)
R.J. Reid
Affiliation:
SAC Veterinary Science Division. Drummondhill, Stratherrick Road Inverness, IV2 4JZ, UK
E. Rogan
Affiliation:
ADC, Department of Zoology, Ecology and Plant Science, University College, National University of Ireland, Lee Maltings, Prospect Row, Cork, Ireland
A.F. González
Affiliation:
Instituto de Investigaciones Marinas, Eduardo Cabello 6, 36208 Vigo, Spain
J. Boon
Affiliation:
Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands
R.J. Law
Affiliation:
The Centre for Environment, Fisheries and Aquaculture Science, Cefas Burnham Laboratory, Remembrance Avenue, Burnham on Crouch, Essex CM0 8HA, UK
C.H. Lockyer
Affiliation:
Age Dynamics, Huldbergs Allé 42, DK-2800 Kongens Lyngby, Denmark
*
Correspondence should be addressed to: P.L. Luque, School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK email: [email protected]

Abstract

We examined the tooth ultra-structure of harbour porpoises (Phocoena phocoena) from Scottish waters to determine whether the incidence of mineralization anomalies could be related to certain life history events (e.g. the achievement of sexual maturation) as well as other factors that affect the general health of the individual (e.g. persistent organic pollutant (POP) concentrations in blubber). Five distinct types of mineralization anomalies were recorded: accessory lines, marker lines, dentinal resorption, cemental disturbance and pulp stones and the occurrence of these anomalies was scored by sex, age and maturity state. Overall, the incidence of mineralization anomalies was high and tended to increase with age. Marker lines and accessory lines were the most commonly recorded anomalies while pulp stones were least frequent. Duplicate teeth (i.e. from the same individual) always showed the same pattern of anomaly occurrence.

Fitted binary generalized linear and additive models indicated that the presence of dentinal resorption, cemental disturbance and marker lines in harbour porpoise teeth increased with age, body length and maturity. Males displayed marker lines more frequently than females. Age was the best predictor of the incidence of dentinal resorption and cemental disturbance while age and sex were the best predictors of the incidence of marker lines. The time course of appearance of dentinal resorption and cemental disturbance suggests that their occurrence could be related to physiological stress linked to sexual maturation. Marker lines were found within growth layer groups which coincided with the beginning of weaning and sexual maturation, suggesting an association with these two major life history events. Accessory lines were found in most teeth and may be a normal characteristic of porpoise teeth or reflect regular events. Pulp stones appeared only in mature animals. We found no evidence that the presence of anomalies in teeth was significantly related to POP concentrations in the blubber.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

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. Lowestoft: MAFF Directorate of Fisheries Research, 6, 25 pp.Google Scholar
Bengtson, J.L. (1988) Long-term trends in the foraging patterns of female Antartic fur seals at South Georgia. In Sahrhage, D. (ed.) Antarctic Ocean resource variability. Berlin: Springer-Verlag, pp. 286291.CrossRefGoogle Scholar
Bergman, A., Olsson, M. and Reiland, S. (1992) Skull lesions in the Baltic grey seal (Halichoerus grypus). Ambio 21, 517519.Google Scholar
Boshma, H. (1950) Absorption of tooth tissue in the sperm whale. Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen 53, 289293.Google Scholar
Boyde, A. (1984) Dependence of rate physical erosion on orientation and density in mineralized tissues. Anatomy and Embryology 170, 5762.CrossRefGoogle Scholar
Bull, J.C., Jepson, P.D., Ssuna, R.K., Deaville, R., Allchin, C.R., Law, R.J. and Fenton, A. (2006) The relationship between polychlorinated biphenyls in blubber and levels of nematode infestations in harbour porpoises, Phocoena phocoena. Parasitology 132, 565573.CrossRefGoogle ScholarPubMed
Campbell, N.A. (1990) Biology, Second Edition. Redwood City, California: Benjamin/Cummings Publishing Company, Inc., 1165 pp.Google Scholar
Collet, A. and Saint-Girons, H. (1984) Preliminary study of the male reproductive cycle in common dolphins, Delphinus delphis, in the Eastern North Atlantic. In Perrin, W.F., Brownell, R.L.J. and DeMaster, D.P. (eds) Reproduction in whales, dolphins and porpoises. Report of the International Whaling Commission Special Issue 6, Cambridge: International Whaling Commission, pp. 355360.Google Scholar
Evans, K., Hindall, A.M., Bobertson, K., Lockyer, C. and Rice, D. (2002) Factors affecting the precision of age determination of sperm whales (Physater macrocephalus). Journal of Cetacean Research and Management 4, 193201.Google Scholar
Faraway, J.J. (2004) Linear models with R. Boca Raton, FL: Chapman & Hall/CRC.CrossRefGoogle Scholar
Hall, A.J., Hugunin, K., Deaville, R., Law, R.J., Allchin, C.R. and Jepson, P.D. (2006) The risk of infection from polychlorinated biphenyl exposure in harbor porpoise (Phocoena phocoena): a case–control approach. Environmental Health Perspectives 114, 704711.CrossRefGoogle ScholarPubMed
Hastie, T.J. and Tibshirani, R.J. (1990) Generalized additive models. London: Chapman & Hall.Google Scholar
Hess, R.A. (1999) Spermatogenesis, overview. In Knobil, E. and Neill, J.D. (eds) Encyclopedia of reproduction. Volume 4. New York: Academic Press, pp. 539545.Google Scholar
Hohn, A.A. (1980) Age determination and age related factors in the teeth of Western North Atlantic bottlenose dolphins. Scientific Reports of the Whales Research Institute, Tokyo 32, 3966.Google Scholar
Hohn, A.A. (1990) Reading between the lines: analysis of age estimation in dolphins. In Leatherwood, S. and Reeves, R.R. (eds) The bottlenose dolphins, Volume 33. New York: Academic Press, pp. 578585.Google Scholar
Hohn, A.A. (2002) Age estimation. In Perrin, W.F., Würsig, B. and Thewissen, J.G.M. (eds) Encyclopedia of marine mammals. San Diego: Academic Press, pp. 613.Google Scholar
Hohn, A.A and Lockyer, C. (1995) Protocol for obtaining age estimates from harbour porpoise teeth. Appendix 3, Report of the harbour porpoise age determination workshop. In Bjørge, A. and Donovan, G.P. (eds) Biology of phocoenids. Report of the International Whaling Commission, Special Issue 16. Cambridge: International Whaling Commission, pp. 478493.Google Scholar
Hohn, A.A., Scott, M.D., Wells, R.S., Sweeney, J.S. and Irvine, A.B. (1989) Growth layers in the teeth from known-age, free-ranging bottlenose dolphins. Marine Mammal Science 5, 315342.CrossRefGoogle Scholar
Jepson, P.D., Bennett, P.M., Deaville, R., Allchin, C.R., Baker, J.R. and Law, R.J. (2005) Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environmental Toxicology and Chemistry 24, 238248.CrossRefGoogle ScholarPubMed
Kleinbaum, D.G. and Klein, M. (2002) Logistic regression: a self-learning text. New York: Springer-Verlag.Google Scholar
Kleinenberg, S.E., Yablokov, A.V., Bel'Kovich, V.M. and Tarasevish, M.N. (1964) Beluga (Delphinapterus leucas). Investigation of the species. Nauka., M. Translated from Russian in 1969. Jerusalem: Israel Program for Scientific Translations.Google Scholar
Klevezal, G.A. (1980) Layers in the hard tissues of mammals as a record of growth rhythms of individuals. In Perrin, W.F. and Myrick, A.C. (eds) Age determination of toothed whales and sirenians. Report of the International Whaling Commission, Special Issue 3. Cambridge: International Whaling Commission, pp. 8994.Google Scholar
Klevezal, G.A. (1996) Recording structures of mammals: determination of age and reconstruction of life history. Rotterdam: A.A. Balkema. 274 pp.Google Scholar
Klevezal, G.A. and Myrick, A.C. (1984) Marks in tooth dentine of female dolphins (Genus Stenella) as indicators of parturition. Journal of Mammology 65, 103110.CrossRefGoogle Scholar
Klevezal, G.A. and Phillips, C.J. (1986) The nature of sclerotic dentine in the teeth of mammals: new clues to life history. In 66th Annual Meeting of American Society of Mammologists. 15–19 June 1986. Abstract 41.Google Scholar
Klevezal, G.A., Sukhovskaya, L.I. and Vilenkin, A.Ya. (1987) [Structure of “marks of breeding” in Odontoceti dentine]. Zoologichesky Zhurnal 66, 18861891. [In Russian.]Google Scholar
Klevezal, G.A. and Tormosov, D.D. (1971) [Revealing of local groups of sperm whale by growth layer patterns in tooth dentine]. Trudy Atlant NIRO 39, 3543. [In Russian.]Google Scholar
Kuiken, T. and Hartmann, M.G. (1991) Cetacean pathology: dissection techniques and tissue sampling. In Proceedings of the first European Cetacean Society workshop on cetacean pathology: dissection techniques and tissue sampling, Leiden, The Netherlands. European Cetacean Society Newsletter no. 17Google Scholar
Langvatan, R. (1995) Age determination of mammals—some aspects of biochemistry and physiological mechanisms relating to deposition of incremental lines in dental tissue. In Bjørge, A. and Donovan, G.P. (eds) Biology of phocoenids. Report of the International Whaling Commission, Special Issue 16. Cambridge: International Whaling Commission, pp. 499509.Google Scholar
Learmonth, J.A. (2006) Life history and fatty acid analysis of harbour porpoises (Phocoena phocoena) from Scottish waters. PhD thesis, University of Aberdeen, Aberdeen.Google Scholar
Lieberman, D.E. (1993) Life history variables preserved in dental cementum microstructure. Science 261, 19621964.CrossRefGoogle ScholarPubMed
Lockyer, C. (1993) A report on patterns of deposition of dentine and cement in teeth of pilot whales, genus Globicephala. In Donovan, G.P., Lockyer, C.H. and Martin, A.R. (eds) Biology of Northern Hemisphere Pilot Whales. Report of the International Whaling Commission, Special Issue 14. Cambridge: International Whaling Commission. pp. 137161.Google Scholar
Lockyer, C. (1995a) Investigations of aspects of the life history of harbour porpoise, Phocoena phocoena, in British waters. In Bjørge, A. and Donovan, G.P. (eds) Biology of phocoenids. Report of the International Whaling Commission, Special Issue 16. Cambridge: International Whaling Commission, pp. 189197.Google Scholar
Lockyer, C. (1995c) A review of factors involved in zonation in odontocete teeth, and an investigation of the likely impact of environment factors and major life events on harbour porpoise tooth structure. In Bjørge, A. and Donovan, G.P. (eds) Biology of phocoenids. Report of the International Whaling Commission, Special Issue 16. Cambridge: International Whaling Commission, pp. 511529.Google Scholar
Lockyer, C. (1999) Application of a new method to investigate population structure in the harbour porpoise, Phocoena phocoena, with special reference to the North and Baltic seas. Journal of Cetacean Research and Management 1, 297304.Google Scholar
Lockyer, C. (2003) Harbour porpoise in the North Atlantic: biological parameters. NAMMCO Scientific Publications 5, 7190.CrossRefGoogle Scholar
Manzanilla, S.R. (1989) The 1982–1983 El Niño event recorded in dentinal growth layers in teeth of Peruvian dusky dolphins (Lagenorhynchus obscurus). Canadian Journal of Zoology 67, 21202125.CrossRefGoogle Scholar
McCullagh, P. and Nelder, J.A. (1989) Generalized linear models, 2nd edition. London: Chapman & Hall.CrossRefGoogle Scholar
Montgomery, D.C. and Peck, E.A. (1992) Introduction to linear regression analysis, 2nd edition. New York: John Wiley & Sons.Google Scholar
Myrick, A.C. Jr (1988) Is tissue resorption and replacement in permanent teeth of mammals caused by stress-induced hypocalcemia? In Davidovitch, Z. (ed.) The biological mechanisms of tooth eruption and root resorption. Birmingham, Alabama: EBSCO Media, pp. 379389.Google Scholar
Myrick, A.C. Jr (1991) Some new and potential uses of the dental layers in studying delphinid populations. In Pryor, K. and Norris, K.S. (eds) Dolphin societies: discoveries and puzzles. Berkeley and Los Angeles: University of California Press, pp. 251279.Google Scholar
Myrick, A.C. Jr, Shallenberger, E.W., Kang, I. and Mackay, D.B. (1984) Calibration of dental layers in seven captive Hawaiian spinner dolphin Stenella longirostris, based on tetracycline labeling. Fisheries Bulletin 82, 207225.Google Scholar
Perrin, W.F. and Donovan, G.P. (1984) Report of the workshop on reproduction of whales, dolphins and porpoises. In Perrin, W.F., Brownell, R.L. and De master, D.P. (eds) Reproduction in whales, dolphin and porpoises. Report of the International Whaling Commission, Special Issue 6. Cambridge: International Whaling Commission, pp. 124.Google Scholar
Perrin, W.F. and Myrick, A.C. Jr (1980) Age determination of toothed whales and sirenians. In Perrin, W.F. and Myrick, A.C. (eds) Age determination of toothed whales and sirenians. Report of the International Whaling Commission, Special Issue 3. Cambridge: International Whaling Commission, pp. 150.Google Scholar
Perrin, W.F. and Reilly, S.B. (1984) Reproductive parameters of dolphins and small whales of the family Delphinidae. Reproduction in whales, dolphins and porpoises. In Perrin, W.F., Brownell, J.R.L. and DeMaster, D.P. (eds) Report of the International Whaling Commission Special Issue 6, 97125.Google Scholar
Rogan, E., Murphy, S., Learmonth, J.A., Gonzalez, A. and Dabin, W. (2004) Age determination in small cetaceans from the NE Atlantic. BIOCET Workpackage 4—final report. Bioaccumulation of persistent organic pollutants in small cetaceans in European waters: transport pathways and impact on reproduction. Project Reference: EVK3-2000-00027. 34.Google Scholar
Santos, M.B., Pierce, G.J., Learmonth, J.A., Reid, R.J., Ross, H.M., Patterson, I.A.P., Reid, D.G. and Beare, D. (2004) Variability in the diet of harbour porpoises (Phocoena phocoena) in Scottish waters 1992–2003. Marine Mammal Science 20, 127.CrossRefGoogle Scholar
Silva, V.M.F. (1995) Age estimation of the Amazon dolphin Inia geoffrensis, using laminae in the teeth. In Bjørge, A. and Donovan, G.P. (eds) Biology of phocoenids. Report of the International Whaling Commission, Special Issue 16. Cambridge: International Whaling Commission, pp. 531543.Google Scholar
Stede, G. and Stede, M. (1990) Oreintuerenede Untersuchungen von Seehundschädeln auf pathologische Knochenveränderungen (Orientating investigations on harbour seal skulls regarding pathological bone changes). In Zoologishe und Ethologische Untersuchungen zum Roggensterben. Kiel, Germany: Institute fur Haustierkunde, pp. 3153.Google Scholar
Wheater, P.R., Burkitt, H.G. and Daniels, V.G. (1987) Functional histology. Edinburgh: Churchill Livingstone.Google Scholar
Wood, S.N. (2006) Generalized additive models: an introduction with R. Boca Raton, FL: Taylor & Francis Ltd.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N. and Smith, G.M. (2007) Analysing ecological data. New York: Springer.CrossRefGoogle Scholar