Abstract
Harbor seals (Phoca vitulina) inhabit the seas surrounding Denmark and are an important top predator in the marine food chain. This trophic position exposes them to environmental contaminants with disease epidemics and hunting being additional threats to this population. It is therefore important to study how environmental pollution at the current order of magnitude affects the health of the population. Earlier studies have shown that occurrence of periodontitis could be linked to the amount of pollution the seals were subjected to. In order to investigate this further, 380 skulls and 141 mandibles of harbor seals (Phoca vitulina) from the Wadden Sea, the Limfjord, and Kattegat collected during the period 1970–2014 were examined. The skulls were examined for pathological lesions. The Hounsfield Units (HU) which are correlated to the bone mineral density (BMD) were measured in a subsample (n = 34) using CT scans. The macroscopic examination revealed (with the exception of the Swedish part of Kattegat) a significant increase of pathological lesions over the study period of 1981–2014. The examination of HU showed that median HU measured at multiple sites was highest in the healthy skulls compared to the skulls with one or more of the lesions. A discriminant analysis allowed high discriminatory capacity to separate healthy skulls from the skulls with pathologies, simply by the utilization of the HU data. Former studies of BMD in marine mammals have shown that exposure to environmental chemicals alter BMD and cause periodontitis. The present study, based on temporal and spatial trends in BMD, confirms the results of previous studies.
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References
Alveblom AK, Rylander L, Johnell O, Hagmar L (2003) Incidence of hospitalized osteoporotic fractures in cohorts with high dietary intake of persistent organic compounds. Int Arch Occup Environ Health 76:246–248
AMAP 2015 AMAP Assessment (2015) Temporal trends in persistent organic pollutants in the arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo. vi+71pp
Antoniades DZ, Belazi M, Papanayiotou P (1998) Concurrence of torus palantinus with palatal and buccal exostoses. Oral surgery oral medicine. Oral Pathol 85:552–557
Bergman A, Olsson M, Reiland S (1992) Skull-bone lesions in the Baltic grey seal Halichoerus grypus. Ambio 21:517–519
Burns JJ (2002) Harbour seal and spotted seal. In: Perrin WE, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, New York, pp 552–560
de Swart RL, Ross PS, Vedder LJ, Timmerman HH, Heisterkamp SH, Van Loveren H, Vos JG, Reijnders PJH, Osterhaus ADME (1994) Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23:155–159
Desforges JPW, Sonne C, Levin M, Siebert U, De Guise S, Dietz R (2016) Immunotoxic effects of environmental pollutants in marine mammals. Environ Int 86:126–139
Dietz R, Hansen CT, Have P, Heide-Jørgensen MP (1989a) Clue to seal epizootic? Nature 338:627
Dietz R, Heide-Jørgensen MP, Härkönen T (1989b) Mass deaths of harbor seals. Ambio 18:258–264
Dietz R, Teilmann J, Andersen SM, Rigét F, Olsen MT (2013) Movements and site fidelity of harbour seals (Phoca vitulina) in Kattegat, Denmark, with implications for the epidemiology of the phocine distemper virus. ICES J Mar Sci 70:186–195
Emlen JM, Freeman DC, Graham JH (1993) Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica 89:77–96
Gorrel C (2004) Veterinary Dentistry for the general practitioner. 1 red. London: Saunders. First edition, Elsevier
Griesel S, Kakuschke A, Siebert U, Prange A (2008) Trace element concentrations in blood of harbour seals (Phoca vitulina) from the Wadden Sea. Sci Total Environ 392:313–323
Hall AJ, Law RJ, Wells DE, Harwood J, Ross HM, Kennedy S, Allchin CR, Campbell LA, Pomeroy PP (1992) Organochlorine levels in common seals (Phoca vitulina) which were victims and survivors of the 1988 phocine distemper epizootic. Sci Total Environ 115:145–162
Harding KC, Salmon M, Teilmann J, Dietz R, Härkönen T (in prep) Population wide decline in somatic growth in harbour seals—a smooth route towards carrying capacity
Härkönen T, Dietz R, Reijnders P, Teilmann J, Thompson P, Harding K, Hall A, Brasseur S, Siebert U, Goodman SJ, Jepson PD, Dau Rasmussen T (2006) Review of the seal epizootics in Europe. DisAquat Organ 68:115–130
Härkönen T, Bäcklin BM, Barrett T, Bergman A, Corteyn M, Dietz R, Harding KC, Malmsten J, Roos A, Teilmann J (2008) Unknown mass mortality in harbour seals and harbour porpoises caused by an unknown pathogen. Vet Rec 162:555–556
Jain R, Kapoor D, Sujay J (2014) Mandibular exostosis in canine with single tooth recession –a rare case report. J Int Oral Health 6:89–91
Jainkittivong A, Langlais RP (2000) Buccal and palatal exostoses: prevalence and concurrence with tori. Oral surgery oral medicine. Oral Pathol 90:48–53
Jensen TH, Van de Bildt M, Dietz HH, Holmen Andersen T, Hammer AS, Kuiken T, Osterhaus A (2002) Another Phocine distemper outbreak in Europe. Science 297:209
Jenssen BM, Dehli Villanger G, Gabrielsen KM, Bytingsvik J, Ciesielski TM, Sonne C, Dietz R (2015) Anthropogenic flank attack on polar bears: interacting consequences of climate warming and pollutant exposure. Front Ecol Evol 3:1–7
Jepson PD, Deaville R, Barber JL, Aguilar À, Borrell A, Murphy S, Barry J, Brownlow A, Barnett J, Berrow S, Cunningham AA, Davison NJ, ten Doeschate M, Esteban R, Ferreira M, Foote AD, Genov T, Giménez J, Loveridge J, Llavona Á, Martin V, Maxwell DL, Papachlimitzou A, Penrose R, Perkins MW, Smith B, de Stephanis R, Tregenza N, Verborgh P, Fernandez A, Law RJ (2016) PCB pollution continues to impact populations of orcas and other dolphins in European waters. Sci Rep 6:18573
Kattainen H, Tuukkanen J, Simanainen U, Tuomisto JT, Kovero O, Lukinmaa PL et al (2001) In utero/lactational 2,3,7,8-tetrachloro-dibenzo-pdioxin exposure impairs molar tooth development in rats. Toxicol Appl Pharmacol 174:216–224
Khalil N, Chen A, Lee M, Czerwinski SA, Ebert JR, DeWitt JC, Kannan K (2016) Association of perfluoroalkyl substances, bone mineral density, and osteoporosis in the U.S. population in NHANES 2009-2010. Environ Health Perspect 124:81–87
Koskela A, Koponen J, Lehenkari P, Viluksela M, Korkalainen M, Tuukkanen J (2017) Perfluoroalkyl substances in human bone: concentrations in bones and effects on bone cell differentiation. Sci Rep 28:6841
Krog JS, Hansen MS, Holm E, Hjulsager CK, Chriél M, Pedersen K, Andresen LO, Abildstrøm M, Jensen TH, Larsen LE (2005) Influenza A virus H10N7 detected in dead harbor seals (Phoca vitulina) in Denmark. Emerg Infect Dis 21:684–687
Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C, Verreault J, Vijayan MM, Gabrielsen GW (2010) Effects assessment of persistent Organohalogen contaminants in Arctic wildlife and fish. Sci Total Environ 408:2995–3043
Lind PM, Larsson S, Oxlund H, Hâkansson H, Nyberg K, Eklund T, Orberg J (2000) Change of bone tissue composition and impaired bone strength in rats exposed to 3,3_,4,4_,5-pentachlorobiphenyl (PCB126). Toxicology 150:41–51
Lind PM, Bergman A, Olsson M, Orberg J (2003) Bone mineral density in male Baltic grey seal (Halichoerus grypus). Ambio 32:385–388
Lind PM, Milnes MR, Lundberg R, Bermudez D, Örberg J, Guillette LJ (2004) Abnormal bone composition in female juvenile American alligators from a pesticide-polluted lake (Lake Apopka, Florida). Environ Health Perspect 112:359–362
Lukinmaa PL, Sahlberg C, Leppäniemi A, Partanen AM, Kovero O, Pohjanvirta R et al (2001) Arrest of rat molar tooth development by lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 173:38–47
Martini FH, Nath JL (2009) Fundamentals of anatomy and physiology. 8 red. Pearson Education, San Fransisco
Measures LN (2001) Lungworms of marine mammals. In: Samuel WM, Pybus MJ, Kocan AA (eds) Prasitic Diseases of Wild Mammals. Iowa State University Press, Iowa, pp 279–288
Mortensen PÅ, Bergman A, Bignert A, Hansen HJ, Härkönen T, Olsson M (1992) Prevalence of skull lesions in harbour seals (Phoca vitulina) in Swedish and Danish museum collections: 1835–1988. Ambio 21:520–524
Nilsson JA (1994) Energetic stress and the degree of fluctuating asymmetry—implications for a long-lasting, honest signal. Evol Ecol 8:248–255
Nørgaard N, Larsen BH (1991) Age determination of harbour seals Phoca vitulina by cementum growth layers, X-ray of teeth and body length, Rønde: Ministry of the Environment, National Environmental Research Institute Department of Wildlife Ecology
Olsen MT, Andersen SM, Teilmann J, Dietz R, Edrén SMC, Linnet A, Harkonen T (2010) Status of the harbour seal (Phoca vitulina) in southern Scandinavia. NAMMCO Special Issue 8:161–178
Olsen MT, Andersen LW, Dietz R, Teilmann J, Härkönen T, Siegismund HR (2014) Integrating genetic data and population viability analyses for the identification of harbour seal (Phoca vitulina) populations and management units. Mol Ecol 23:815–831
Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability:implications of non-normal distribution and power of statistical test. Acta Zool Fenn 191:55–70
Pertoldi C, Kristensen TN (2015) A new fluctuating asymmetry index, or the solution for the scaling effect? Symmetry-Basel 7:327–335
Pertoldi C, Leoschcke V, Maden AB, Randi E (1997) Development stability in the European otter (Lutra lutra) in Denmark. Annales Zoologi Fennici 34:187–196
Pertoldi C, Loeschcke V, Braun A, Madsen AB, Randi E (2000) Craniometrical variability and developmental stability. Two useful tools for assessing the population viability of Eurasian otter (Lutra lutra) populations in Europe. Biol J Linn Soc 70:309–323
Reijnders PJH (1986) Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324:456–457
Reijnders PJH, Brassaur SMJM, Borchardt T, Camphuysen K, Czeck R, Gilles A, Jensen LF, Leopold M, Lucke K, Ramdohr S, Scheidat M, Siebert U, Teilmann J (2009) Marine Mammals. Thematic Report no. 20 in H. Marencic and J. de Vlas, eds. Quality Status Report. Wadden Sea Ecosystem no. 25. Common Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group. Wilhelmshaven. Germany
Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225
Roos AM, Bäcklin BM, Helander BO, Rigét FF, Eriksson UC (2012) Improved reproductive success in otters (Lutra lutra), grey seals (Halichoerus grypus) and sea eagles (Haliaeetus albicilla) from Sweden in relation to concentrations of organochlorine contaminants. Environ Pollut 170:268–275
Schandorff S (1997) Developmental stability and skull lesions in the harbour seal (Phoca vitulina) in the 19th and 20th centuries. Ann Zool Fenn 34:151–166
Schreiber JJ, Hsu WK (2014) Use of computed tomography for assessing bone mineral density. Neurosurg Focus 37(1)
Siebert U, Joiris C, Holsbeek L, Benke H, Failing K, Frese K, Petzinger E (1999) Potential relation between mercury concentrations and necropsy findings in cetaceans from German waters of the north and Baltic seas. Mar Pollut Bull 38:285–295
Siegel M, Doyle WJ (1975) The effects of cold stress on fluctuating asymmetry in the dentition of the mouse. J Exp Zoolog 191:385–389
Siegel M, Doyle WJ, Kelley C (1977) Heat stress, fluctuating asymmetry and prenatal selection in the laboratory rat. Am J Phys Anthropol 46:121–126
Sonne C (2010) Health effects from long-range transported contaminants in Arctic top predators: an integrated review based on studies of polar bears and relevant model species. Environ Int 36:461–491
Sonne C, Dietz R, Born EW, Rigét FF, Kirkegaard M, Hyldstrup L, Letcher RJ, Muir DCG (2004) Is bone mineral composition disrupted by organochlorines in East Greenland polar bears (Ursus maritimus)? Environ Health Perspect 112:1711–1716
Sonne C, Rigét FF, Dietz R, Kirkegaard M, Born EW, Letcher RJ, Muir DCG (2005) Trends in fluctuating asymmetry in East Greenland polar bears (Ursus maritimus) from 1892 to 2002 in relation to organohalogen pollution. Sci Total Environ 341:81–96
Sonne C, Rigét FF, Dietz R, Wiig Ø, Kirkegaard M, Born EW (2007) Gross skull pathology in East Greenland and Svalbard polar bears (Ursus maritimus) during 1892 to 2002 in relation to Organohalogen pollution. Sci Total Environ 372:554–561
Sonne C, Wolkers H, Rigét FF, Beck Jensen JE, Teilmann J, Jenssen BM, Fuglei E, Ahlstrøm Ø, Dietz R, Muir DCG, Jørgensen E (2009) Mineral density and biomechanical properties of bone tissue from male arctic foxes (Vulpes lagopus) exposed to organochlorines and emaciation. Comp Biochem Phys C 149:97–103
Sonne C, Letcher RJ, Bechshøft TØ, Rigét FF, Muir DCG, Leifsson PS, Born EW, Hyldstrup L, Basu N, Kirkegaard M, Dietz R (2012) Two decades of biomonitoring polar bear health in Greenland: a review. Acta Vet Scan 54:S15
Sonne C, Bechshøft TØ, Rigét FF, Baagøe HJ, Hedayat A, Andersen M, Bech-Jensen JE, Hyldstrup L, Letcher RJ, Dietz R (2013) Size and density of East Greenland polar bear (Ursus maritimus) skulls as bio-indicators of environmental changes. Ecol Indic 34:290–295
Teilmann J, Riget F, Härkönen T (2010) Optimizing survey design for Scandinavian harbour seals: population trend as an ecological quality element. ICES J Mar Sci 67:952–958
van Beurden SJ, van de Bildt M, Kik MJL, Rijks JM, van Asten JAM, de Vriege G, Brasser MJM, Osterhaus ADME, Jensen TH, Grone A, Verheije MH, Kuiken T, Ijzer J. 2017 Persistent phocine distemper virus (PDV) infection in two harbour seals (Phoca vitulina) in the Netherlands. The Zoo and Wildlife Health Conference 2017 May 24-27th 2017
Vercruysse J, Salomez A, Ulloa A, Alvinerie M, Osterhaus A, Kuiken T (2003) Efficacy of ivermectin and moxidectin against Otostrongylus circumlitus and Parafilaroides gymnurus in harbour seals (Phoca vitulina). Vet Rec 152:130–134
Weijs L, Das K, Siebert U (2009) Concentration of chlorinated and brominated contaminants and their metabolites in serum of harbour seals and harbour porpoises. Envir Intern 35:842–850
Zohari S, Neimanis A, Harkonen T, Moraeus C, Valarcher JF (2014) Avian influenza A(H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014. Euro Surveill 19(46):20967
Acknowledgements
We would like to thank the Aalborg Zoo Conservation Foundation for supporting this study. Furthermore, we would like to thank the Swedish Museum of Natural History (Stockholm, Sweden), the Natural History Musem of Denmark (Copenhagen, Denmark), and the Fisheries and Maritime Museum (Esbjerg, Denmark). Finally, we would like to thank two anonymous reviewers for invaluable suggestions and help.
Funding
The study was funded by the local financing body and the BONUS BaltHealth has received funding from BONUS (Art. 185), funded jointly by the EU, Innovation Fund Denmark (grants 6180-00001B and 6180-00002B), Forschungszentrum Jülich GmbH, German Federal Ministry of Education and Research (grant FKZ 03F0767A), Academy of Finland (grant 311966) and Swedish Foundation for Strategic Environmental Research (MISTRA) (C. Sonne, M. T. Olsen, T. Härkönen, K.C. Harding and R. Dietz).
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Pertoldi, C., Jensen, L.F., Alstrup, A.K.O. et al. Prevalence of skull pathologies in European harbor seals (Phoca vitulina) during 1981–2014. Mamm Res 63, 55–63 (2018). https://doi.org/10.1007/s13364-017-0340-2
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DOI: https://doi.org/10.1007/s13364-017-0340-2