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Ecological factors affecting eruption timing of mandibular teeth in roe deer

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Abstract

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.

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References

  • 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 93–107

    Google Scholar 

  • Albon SD, Mitchell B, Staines BW (1983) Fertility and body mass in female red deer: a density-dependent relationship. J Anim Ecol 52:969–980

    Article  Google Scholar 

  • 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 15–21

    Chapter  Google Scholar 

  • 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]

    Article  Google Scholar 

  • Apollonio M, Mattioli L (2006) Il lupo in provincia di Arezzo. Editrice Le Balze, Montepulciano [in Italian]

    Google Scholar 

  • Apollonio M, Putman R, Andersen R (2010) Ungulate management in Europe in the XXI century. Cambridge University Press, Cambridge

    Google Scholar 

  • Barry RG (1981) Mountain weather and climate. Methuen, London

    Google Scholar 

  • 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):e0124698

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer-Verlag, New York

    Google Scholar 

  • Chapman DI, Chapman NG (1997) Fallow deer: their history, distribution and biology, 2nd edn. Coch-y-bonddu books, Machynl-leth

    Google Scholar 

  • 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 38:10–14

    Google Scholar 

  • Clutton-Brock TH, Price OF, Albon SD, Jewell PA (1992) Early development and population fluctuations in Soay sheep. J Anim Ecol 61:381–396

    Article  Google Scholar 

  • Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238

    Article  PubMed  Google Scholar 

  • 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 70:493–502

    Article  Google Scholar 

  • 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):1–10

    Google Scholar 

  • 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):e0175579

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 70:1541–1545

    Article  Google Scholar 

  • Gaillard JM, Delorme D, Jullien JM (1993a) Effects of cohort, sex, and birth date on body development of roe deer (Capreolus capreolus) fawns. Oecologia 94:57–61

    Article  PubMed  CAS  Google Scholar 

  • Gaillard JM, Delorme D, Jullien JM, Tatin D (1993b) Timing and synchrony of births in roe deer. J Mammal 74:738–744

    Article  Google Scholar 

  • 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 57:359–366

    Article  Google Scholar 

  • 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 60:29–36

    Article  Google Scholar 

  • 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 112:502–513

    Article  PubMed  Google Scholar 

  • Gaillard JM, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63

    Article  PubMed  CAS  Google Scholar 

  • 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 31:367–393

    Article  Google Scholar 

  • 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 67:767–773

    Article  Google Scholar 

  • 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 45:300–307

    Article  Google Scholar 

  • Garn S, Lewis AB, Kerewsky RS (1965) Genetic, nutritional, and maturational correlates of dental development. J Dent Res 44:228–242

    Article  Google Scholar 

  • 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 25:759–763

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 90:1981–1995

    Article  PubMed  Google Scholar 

  • Herring SW (1985) The ontogeny of mammalian mastication. Am Zool 25:339–349

    Article  Google Scholar 

  • Hewison AJM (1996) Variation in the fecundity of roe deer in Britain: effects of age and body weight. Acta Theriol 41:187–198

    Article  Google Scholar 

  • 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 239:573–581

    Article  Google Scholar 

  • Hillson S (2005) Teeth, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hobbs NT (1989) Linking energy balance to survival in mule deer: development and test of a simulation model. Wildl Monogr 101:1–39

    Google Scholar 

  • 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 12:71–76

    Article  Google Scholar 

  • Klein DR (1964) Range-related differences in growth of deer reflected in skeletal ratios. J Mammal 45:226–235

    Article  Google Scholar 

  • Langvatn R (1977) Criteria of physical condition, growth and development in Cervidae - suitable for routine studies. Nordic council for wildlife research, Stockholm

    Google Scholar 

  • Langvatn R, Albon SD (1986) Geographic clines in body weight of Norwegian red deer: a novel explanation to Bergmann’s rule? Holarct Ecol 9:285–293

    Google Scholar 

  • Langvatn R, Mysterud A, Stenseth NC (2004) Relationships in red deer Cervus elaphus mandibles. Acta Theriol 49:527–542

    Article  Google Scholar 

  • 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 7:439–451

    Article  Google Scholar 

  • Li J, Heap AD (2008) A review of spatial interpolation methods for environmental scientists. Geosci Aust 23:137

    Google Scholar 

  • Linnell JDC, Andersen R (1998) Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. J Zool 244:497–504

    Article  Google Scholar 

  • 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 262:83–89

    Article  Google Scholar 

  • Loison A, Langvatn R, Solberg E (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30

    Article  Google Scholar 

  • Lutz W (1993) Beitrag zur Zahn-und Unterkieferentwicklung bei Damwildkälbern aus einem großstädtischen Ballungsraum. Z Jagdwiss 39:73–86 [in German]

    Google Scholar 

  • 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 

  • 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 264:249–258

    Article  Google Scholar 

  • 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 15:213–224

    Article  PubMed  CAS  Google Scholar 

  • 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 88:3192–3201

    Article  PubMed  CAS  Google Scholar 

  • Oftedal OT (1984) Body size and reproductive strategy as correlates of milk energy output in lactating mammals. Acta Zool Fenn 171:183–186

    Google Scholar 

  • Patterson BR, Power VA (2002) Contributions of forage competition, harvest, and climate fluctuation to changes in population growth of northern white-tailed deer. Oecologia 130:62–71

    Article  PubMed  Google Scholar 

  • Pelliccioni ER, Scremin M, Toso S (2004) Early body development of roe deer Capreolus capreolus in a sub-Mediterranean ecosystem. Wildl Biol 10:107–113

    Article  Google Scholar 

  • 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 245:307–316

    Article  Google Scholar 

  • 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 269:747–753

    Article  Google Scholar 

  • 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 74:972–981

    Article  Google Scholar 

  • 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 112:565–572

    Article  Google Scholar 

  • 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 9:20120841

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):e1001828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pond CM (1977) The significance of lactation in the evolution of mammals. Evolution 31:177–199

    Article  PubMed  Google Scholar 

  • 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 264:1317–1324

    Article  CAS  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL https://www.R-project.org/

    Google Scholar 

  • Rees JW, Kainer RA, Davis RW (1966) Chronology of mineralization and eruption of mandibular teeth in mule deer. J Wildl Manag 30:629–631

    Article  Google Scholar 

  • Robinette WL, Jones DA, Rogers G, Gashwiler JS (1957) Notes of tooth development and wear for Rocky Mountain mule deer. J Wildl Manag 21:134–153

    Article  Google Scholar 

  • Robinson JJ, McDonald I, Fraser C, Crofts RMJ (1977) Studies on reproduction in prolific ewes. J Agric Sci 88:539–552

    Article  Google Scholar 

  • Sadleir RMFS (1987) Reproduction of female cervids. In: Wemmer CM (ed) Biology and management of the Cervidae. Smithsonian Institution Press, Washington, D.C., pp 123–144

    Google Scholar 

  • Smith BH (1989) Dental development as a measure of life history in primates. Evolution 43:683–688

    Article  PubMed  Google Scholar 

  • 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 143:85–93

    Article  PubMed  Google Scholar 

  • 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 275:2137–2145

    Article  Google Scholar 

  • 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 95:3124–3138

    Article  Google Scholar 

  • 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 65:13–21

    Article  Google Scholar 

  • 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 90:393–402

    Article  Google Scholar 

  • Thenius E (1989) Zähne und Gebiß der Säugetiere. Walter de Gruyter, Berlin [in German]

    Google Scholar 

  • 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 29:301–308

    Article  Google Scholar 

  • 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 90:661–665

    Article  Google Scholar 

  • Veitschegger K, Sánchez-Villagra MR (2016) Tooth eruption sequences in cervids and the effect of morphology, life history, and phylogeny. J Mamm Evol 23:251–263

    Article  Google Scholar 

  • White GC, Garrott RA, Bartmann RM, Carpenter LH, Alldredge AW (1987) Survival of mule deer in Northwest Colorado. J Wildl Manag 51:852–859

    Article  Google Scholar 

  • 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 83–103

    Chapter  Google Scholar 

  • 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 39:227–234

    Article  Google Scholar 

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Acknowledgments

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.

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  1. Italian National Institute for Environmental Protection and Research (ISPRA), via Ca’ Fornacetta, 9, I-40064, Ozzano dell’Emilia (BO), Italy

    Anna Maria De Marinis, Elisa Bottero & Marco Apollonio

  2. Department of Veterinary Medicine, University of Sassari, via Vienna 2, I-07100, Sassari, Italy

    Roberta Chirichella

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  1. Anna Maria De Marinis
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Correspondence to Roberta Chirichella.

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De Marinis, A.M., Chirichella, R., Bottero, E. et al. Ecological factors affecting eruption timing of mandibular teeth in roe deer. Eur J Wildl Res 64, 50 (2018). https://doi.org/10.1007/s10344-018-1211-0

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