Ecological factors affecting eruption timing of mandibular teeth in roe deer

  • Anna Maria De Marinis
  • Roberta ChirichellaEmail author
  • Elisa Bottero
  • Marco Apollonio
Original Article


Increasing evidence suggests that conditions in early life have important consequences for body size and fitness in mammals. As regards herbivores, teeth play a central role in the long-term performance of individuals. So far, however, patterns of teeth eruption have been scarcely investigated in relation to environmental and climatic factors experienced by herbivores. We described the eruption timing of mandibular teeth in a population of roe deer (Capreolus capreolus) located in the Apennines (Central Italy), through the analysis of 2161 jaws of fawns (1176 females and 985 males) shot in their first winter of life over three hunting seasons (2013–2015). Results showed that the percentage of juveniles exhibiting permanent teeth depends on the cohort. Among the factors that may affect both incisiviform and molariform teeth replacement timing, our findings include body mass and population density. Additional factors determining the relative speed of teeth replacement are (1) food availability for the mother during the last part of gestation, the birth period and the lactation, (2) winter temperature experienced by the mother, and (3) temperature experienced by fawns during their first summer and autumn. Besides, for the first time in literature, elevation was reported to delay front teeth replacement. A greater number of climatic factors were found to shape the eruption timing of the third molar (M3) in comparison to that of incisiviform teeth. Also, a different pattern was found in males and females. The eruption of M3 is, indeed, a costly and long-lasting process requesting optimal nutritional conditions and the meeting of a threshold jaw size. Our results indicate a strong correlation between environmental conditions and eruption process, i.e., between resource availability during the gestation and rearing periods and eruption timing.


Tooth eruption Body condition Climate Forage resource Cohort effect Capreolus capreolus 



We are grateful to Arezzo Province for supplying data. We are indebted to L. Mattioli and M. Meacci for their logistic support in collecting data. We would like to thank all the hunters who provided samples of roe deer jaws, without which the study would not be possible. G. Falceri revised the English version of this article.

Compliance with ethical standards

The study complies with all relevant national, regional, and provincial Italian laws and with the ethical standards of scholarly research.

Supplementary material

10344_2018_1211_MOESM1_ESM.docx (184 kb)
Fig. S1 (DOCX 184 kb)
10344_2018_1211_MOESM2_ESM.docx (132 kb)
Fig. S2 (DOCX 132 kb)
10344_2018_1211_MOESM3_ESM.docx (19 kb)
Table S1 (DOCX 19 kb)


  1. Albon SD, Clutton-Brock TH (1988) Climate and the population dynamics of red deer in Scotland. In: Usher MB, Thompson DBA (eds) Ecological change in the uplands. Blackwell Scientic, Oxford, pp 93–107Google Scholar
  2. Albon SD, Mitchell B, Staines BW (1983) Fertility and body mass in female red deer: a density-dependent relationship. J Anim Ecol 52:969–980CrossRefGoogle Scholar
  3. Albon SD, Clutton-Brock TH, Langvaten R (1992) Cohort variation in reproduction and survival: implications for population demography. In: Brown RD (ed) The biology of deer. Springer-Verlag, New York, pp 15–21CrossRefGoogle Scholar
  4. Angibault JM, Bideau E, Vincent JP, Quéré JP, Khazraie K (1993) Détermination de l’âge chez le Chevreuil (Capreolus capreolus L.). Test de critères morphologiques à partir d’animaux d’âge connu. Mammalia 57:579–587 [in French]CrossRefGoogle Scholar
  5. Apollonio M, Mattioli L (2006) Il lupo in provincia di Arezzo. Editrice Le Balze, Montepulciano [in Italian]Google Scholar
  6. Apollonio M, Putman R, Andersen R (2010) Ungulate management in Europe in the XXI century. Cambridge University Press, CambridgeGoogle Scholar
  7. Barry RG (1981) Mountain weather and climate. Methuen, LondonGoogle Scholar
  8. Bassi E, Willis SG, Passilongo D, Mattioli L, Apollonio M (2015) Predicting the spatial distribution of wolf (Canis lupus) breeding areas in a mountainous region of Central Italy. PLoS One 10(6):e0124698CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  10. Chapman DI, Chapman NG (1997) Fallow deer: their history, distribution and biology, 2nd edn. Coch-y-bonddu books, Machynl-lethGoogle Scholar
  11. Chianucci F, Mattioli L, Amorini E, Giannini T, Marcon A, Chirichella R, Apollonio M, Cutini A (2014) Early and long-term impacts of browsing by roe deer in oak coppiced woods along a gradient of population density. Ann Silvicult Res 38:10–14Google Scholar
  12. Clutton-Brock TH, Price OF, Albon SD, Jewell PA (1992) Early development and population fluctuations in Soay sheep. J Anim Ecol 61:381–396CrossRefGoogle Scholar
  13. Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238CrossRefPubMedGoogle Scholar
  14. Cutini A, Chianucci F, Chirichella R, Donaggio E, Mattioli L, Apollonio M (2013) Mast seeding in deciduous forests of the northern Apennines (Italy) and its influence on wild boar population dynamics. Ann For Sci 70:493–502CrossRefGoogle Scholar
  15. Davis ML, Stephens PA, Willis SG, Bassi E, Marcon A, Donaggio E, Capitani C, Apollonio M (2012) Prey selection by an apex predator: the importance of sampling uncertainty. PLoS One 7(10):1–10Google Scholar
  16. Flajšman K, Jerina K, Pokorny B (2017) Age-related effects of body mass on fertility and litter size in roe deer. PLoS One 12(4):e0175579CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gaillard JM, Semperé AJ, Van Laere G, Boutin JM, Boisaubert B (1992) Effects of age and body mass on the proportion of females breeding in a population of roe deer. Can J Zool 70:1541–1545CrossRefGoogle Scholar
  18. Gaillard JM, Delorme D, Jullien JM (1993a) Effects of cohort, sex, and birth date on body development of roe deer (Capreolus capreolus) fawns. Oecologia 94:57–61CrossRefPubMedGoogle Scholar
  19. Gaillard JM, Delorme D, Jullien JM, Tatin D (1993b) Timing and synchrony of births in roe deer. J Mammal 74:738–744CrossRefGoogle Scholar
  20. Gaillard JM, Delorme D, Jullien JM (1993c) Croissance précoce et poids à l’entrée de l’hiver chez le faon de chevreuil (Capreolus capreolus). Mammalia 57:359–366CrossRefGoogle Scholar
  21. Gaillard JM, Delorme D, Boutin JM, Van Laere G, Boisaubert B (1996) Body mass of roe deer fawns during winter in 2 contrasting populations. J Wildl Manag 60:29–36CrossRefGoogle Scholar
  22. Gaillard JM, Delorme D, Van Laere G, Duncan P, Lebreton JD (1997) Early survival in roe deer: causes and consequences of cohort variation in two contrasted populations. Oecologia 112:502–513CrossRefPubMedGoogle Scholar
  23. Gaillard JM, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63CrossRefPubMedGoogle Scholar
  24. Gaillard JM, Festa-Bianchet M, Yoccoz NG, Loison A, Toigo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393CrossRefGoogle Scholar
  25. Gaillard JM, Duncan P, Delorme D, Van Laere G, Pettorelli N, Maillard D, Renaud G (2003) Effects of hurricane Lothar on the population dynamics of European roe deer. J Wildl Manag 67:767–773CrossRefGoogle Scholar
  26. Garel M, Gaillard JM, Delorme D, Van Laere G (2014) Eruption patterns of permanent front teeth as an indicator of performance in roe deer. Ecol Indic 45:300–307CrossRefGoogle Scholar
  27. Garn S, Lewis AB, Kerewsky RS (1965) Genetic, nutritional, and maturational correlates of dental development. J Dent Res 44:228–242CrossRefGoogle Scholar
  28. Garratt M, Lemaître JF, Douhard M, Bonenfant C, Capron G, Warnant C, Klein F, Brooks RC, Gaillard JM (2015) High juvenile mortality is associated with sex-specific adult survival and lifespan in wild roe deer. Curr Biol 25:759–763CrossRefPubMedGoogle Scholar
  29. Habermehl KH (1985) Altersbestimmung bei Wild- und Pelztieren – Möglichkeiten und Methoden – ein praktischer Leitfaden für Jäger, Biologen und Tierärzte, 2nd edn. Verlag Paul Parey, Hamburg [in German]Google Scholar
  30. Hamel S, Gaillard JM, Festa-Bianchet M, Côté SD (2009) Individual quality, early-life conditions, and reproductive success in contrasted populations of large herbivores. Ecology 90:1981–1995CrossRefPubMedGoogle Scholar
  31. Herring SW (1985) The ontogeny of mammalian mastication. Am Zool 25:339–349CrossRefGoogle Scholar
  32. Hewison AJM (1996) Variation in the fecundity of roe deer in Britain: effects of age and body weight. Acta Theriol 41:187–198CrossRefGoogle Scholar
  33. Hewison AJM, Vincent JP, Bideau E, Angibault JM, Putman RJ (1996) Variation in cohort mandible size as an index of roe deer (Capreolus capreolus) densities and population trends. J Zool 239:573–581CrossRefGoogle Scholar
  34. Hillson S (2005) Teeth, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  35. Hobbs NT (1989) Linking energy balance to survival in mule deer: development and test of a simulation model. Wildl Monogr 101:1–39Google Scholar
  36. Høye T, Forchhammer MC (2006) Early developed section of the jaw as an index of prenatal growth conditions in adult roe deer Capreolus capreolus. Wildl Biol 12:71–76CrossRefGoogle Scholar
  37. Klein DR (1964) Range-related differences in growth of deer reflected in skeletal ratios. J Mammal 45:226–235CrossRefGoogle Scholar
  38. Langvatn R (1977) Criteria of physical condition, growth and development in Cervidae - suitable for routine studies. Nordic council for wildlife research, StockholmGoogle Scholar
  39. Langvatn R, Albon SD (1986) Geographic clines in body weight of Norwegian red deer: a novel explanation to Bergmann’s rule? Holarct Ecol 9:285–293Google Scholar
  40. Langvatn R, Mysterud A, Stenseth NC (2004) Relationships in red deer Cervus elaphus mandibles. Acta Theriol 49:527–542CrossRefGoogle Scholar
  41. Lesage L, Crête M, Huot J, Ouellet JP (2000) Quality of plant species utilized by northern white-tailed deer in summer along a climatic gradient. Ecoscience 7:439–451CrossRefGoogle Scholar
  42. Li J, Heap AD (2008) A review of spatial interpolation methods for environmental scientists. Geosci Aust 23:137Google Scholar
  43. Linnell JDC, Andersen R (1998) Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. J Zool 244:497–504CrossRefGoogle Scholar
  44. Loe LE, Meisingset EL, Mysterud A, Langvatn R, Stenseth NC (2004) Phenotypic and environmental correlates of tooth eruption in red deer (Cervus elaphus). J Zool 262:83–89CrossRefGoogle Scholar
  45. Loison A, Langvatn R, Solberg E (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30CrossRefGoogle Scholar
  46. Lutz W (1993) Beitrag zur Zahn-und Unterkieferentwicklung bei Damwildkälbern aus einem großstädtischen Ballungsraum. Z Jagdwiss 39:73–86 [in German]Google Scholar
  47. Mattioli S, Spada A (2009) Il Capriolo. Caratteristiche biometriche della popolazione del territorio bolognese. Quaderni di Caccia e Pesca 2, Provincia di Bologna [in Italian]Google Scholar
  48. Mattioli L, Capitani C, Avanzinelli E, Bertelli I, Gazzola A, Apollonio M (2004) Predation by wolves (Canis lupus) on roe deer (Capreolus capreolus) in north eastern Apennine, Italy. J Zool 264:249–258CrossRefGoogle Scholar
  49. McCance RA, Brown WAB (1961) Severe undernutrition in growing of adult animals. 7. Development of the skull, jaws and teeth in pigs. Br J Nutr 15:213–224CrossRefPubMedGoogle Scholar
  50. McLoughlin PD, Gaillard JM, Boyce MS, Bonenfant C, Messier F, Duncan P, Delorme D, Van Moorter B, Saïd S, Klein F (2007) Lifetime reproductive success and composition of the home range in a large herbivore. Ecology 88:3192–3201CrossRefPubMedGoogle Scholar
  51. Oftedal OT (1984) Body size and reproductive strategy as correlates of milk energy output in lactating mammals. Acta Zool Fenn 171:183–186Google Scholar
  52. Patterson BR, Power VA (2002) Contributions of forage competition, harvest, and climate fluctuation to changes in population growth of northern white-tailed deer. Oecologia 130:62–71CrossRefPubMedGoogle Scholar
  53. Pelliccioni ER, Scremin M, Toso S (2004) Early body development of roe deer Capreolus capreolus in a sub-Mediterranean ecosystem. Wildl Biol 10:107–113CrossRefGoogle Scholar
  54. Pérez-Barberia FJ, Gordon IJ (1998) The influence of molar occlusal surface area on the voluntary intake, digestion, chewing behaviour and diet selection of red deer (Cervus elaphus). J Zool 245:307–316CrossRefGoogle Scholar
  55. Pettorelli N, Gaillard JM, Van Laere G, Duncan P, Kjellander P, Liberg O, Delorme D, Maillard D (2002) Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality. Proc R Soc Lond B Biol Sci 269:747–753CrossRefGoogle Scholar
  56. Pettorelli N, Gaillard JM, Yoccoz NG, Duncan P, Maillard D, Delorme D, Van Laere G, Toïgo C (2005) The response of fawn survival to changes in habitat quality varies according to cohort quality and spatial scale. J Anim Ecol 74:972–981CrossRefGoogle Scholar
  57. Pettorelli N, Gaillard JM, Mysterud A, Duncan P, Delorme D, Van Laere G, Toïgo C, Klein F (2006) Using a proxy of plant productivity (NDVI) to find key periods for animal performance: the case of roe deer. Oikos 112:565–572CrossRefGoogle Scholar
  58. Plard F, Gaillard JM, Bonenfant C, Hewison AJM, Delorme D, Cargnelutti B, Kjellander P, Nilsen EB, Coulson T (2013) Parturition date for a given female is highly repeatable within five roe deer populations. Biol Lett 9:20120841CrossRefPubMedPubMedCentralGoogle Scholar
  59. Plard F, Gaillard JM, Coulson T, Hewison AJM, Delorme D, Warnant C, Bonenfant C (2014) Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biol 12(4):e1001828CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pond CM (1977) The significance of lactation in the evolution of mammals. Evolution 31:177–199CrossRefPubMedGoogle Scholar
  61. Post E, Stenseth NC, Langvatn R, Fromentin JM (1997) Global climate change and phenotypic variation among red deer cohorts. Proc R Soc Lond B Biol Sci 264:1317–1324CrossRefGoogle Scholar
  62. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL Google Scholar
  63. Rees JW, Kainer RA, Davis RW (1966) Chronology of mineralization and eruption of mandibular teeth in mule deer. J Wildl Manag 30:629–631CrossRefGoogle Scholar
  64. Robinette WL, Jones DA, Rogers G, Gashwiler JS (1957) Notes of tooth development and wear for Rocky Mountain mule deer. J Wildl Manag 21:134–153CrossRefGoogle Scholar
  65. Robinson JJ, McDonald I, Fraser C, Crofts RMJ (1977) Studies on reproduction in prolific ewes. J Agric Sci 88:539–552CrossRefGoogle Scholar
  66. Sadleir RMFS (1987) Reproduction of female cervids. In: Wemmer CM (ed) Biology and management of the Cervidae. Smithsonian Institution Press, Washington, D.C., pp 123–144Google Scholar
  67. Smith BH (1989) Dental development as a measure of life history in primates. Evolution 43:683–688CrossRefPubMedGoogle Scholar
  68. Stewart KM, Bowyer RT, Dick BL, Johnson BK, Kie JG (2005) Density-dependent effects on physical condition and reproduction in North American elk: an experimental test. Oecologia 143:85–93CrossRefPubMedGoogle Scholar
  69. Stopher KV, Pemberton JM, Clutton-Brock TH, Coulson T (2008) Individual differences, density dependence and offspring birth traits in a population of red deer. Proc R Soc Lond B Biol Sci 275:2137–2145CrossRefGoogle Scholar
  70. Stopher KV, Bento A, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2014) Multiple pathways mediate the effects of climate change on maternal reproductive traits in a red deer population. Ecology 95:3124–3138CrossRefGoogle Scholar
  71. Symonds MRE, Mousalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  72. Taillon J, Brodeur V, Festa-Bianchet M, Côté SD (2012) Is mother condition related to offspring condition in migratory caribou (Rangifer tarandus) at calving and weaning? Can J Zool 90:393–402CrossRefGoogle Scholar
  73. Thenius E (1989) Zähne und Gebiß der Säugetiere. Walter de Gruyter, Berlin [in German]Google Scholar
  74. Toïgo C, Gaillard JM, Van Laere G, Hewison M, Morellet N (2006) How does environmental variation influence body mass, body size, and body condition? Roe deer as a case study. Ecography 29:301–308CrossRefGoogle Scholar
  75. Vanpé C, Gaillard JM, Morellet N, Kjellander P, Liberg O, Delorme D, Hewison M (2009) Age specific variation in male breeding success of a territorial ungulate species the European roe deer. J Mammal 90:661–665CrossRefGoogle Scholar
  76. Veitschegger K, Sánchez-Villagra MR (2016) Tooth eruption sequences in cervids and the effect of morphology, life history, and phylogeny. J Mamm Evol 23:251–263CrossRefGoogle Scholar
  77. White GC, Garrott RA, Bartmann RM, Carpenter LH, Alldredge AW (1987) Survival of mule deer in Northwest Colorado. J Wildl Manag 51:852–859CrossRefGoogle Scholar
  78. Wilson AJ, Festa-Bianchet M (2009) Maternal effects in wild ungulates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 83–103CrossRefGoogle Scholar
  79. Ziello C, Estrella N, Kostova M, Koch E, Menzel A (2009) Influence of altitude on phenology of selected plant species in the alpine region (1971–2000). Clim Res 39:227–234CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Italian National Institute for Environmental Protection and Research (ISPRA)Ozzano dell’Emilia (BO)Italy
  2. 2.Department of Veterinary MedicineUniversity of SassariSassariItaly

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