Skip to main content
SpringerLink
Log in

Dental Eruption Series and Replacement Pattern in Miocene Prosantorhinus (Rhinocerotidae) as Revealed by Macroscopy and X-ray: Implications for Ontogeny and Mortality Profile

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

Fossil evidence of complete sequences of dental ontogeny in extinct mammals is rare but contains valuable information on the animal’s physiology, life history, and individual age. Here, we analyzed an exceptionally high number of juvenile dentaries at different developmental stages including highly fragile tooth germs of the extinct rhinoceros Prosantorhinus germanicus from the Miocene fossil lagerstätte Sandelzhausen in Germany. We used dental wear stages, eruption stages, and tooth germ development in order to reconstruct the tooth replacement pattern for P. germanicus. The results allow for the distinction of 11 dental eruption stages and document a tooth eruption sequence of (d2, d3), (d1, d4), m1, m2, p2, p3, p4, m3; a pattern identical to that reported for the extant African rhinoceros, Diceros bicornis. Moreover, our findings indicate that P. germanicus falls into the life history category of slow-growing, long-living mammals. The dental eruption stages of the fossil rhinoceros were correlated with data of living rhinoceroses in order to gain insight into the age-at-death distribution of P. germanicus at Sandelzhausen. The juvenile mortality profile of P. germanicus shows a trend of selective mortality at an inferred age range of about 3 months to 3 years. As this age range represents a life phase of increased natural risk of mortality, our findings indicate a gradual accumulation of corpses (attritional fossil assemblage). This result supports the interpretation of a taphocenosis found at the Sandelzhausen fossil site.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anders U, Koenigswald W von, Ruf I, Smith BH (2011) Generalized individual dental age stages for fossil and extant placental mammals. Paläontol Z 85:321–339

  • Anderson JL (1966) Tooth replacement and dentition of the black rhinoceros (Diceros bicornis Linn.). Lammergeyer 6:41–46

    Google Scholar 

  • Berger J, Cunningham C (1995) Predation, sensitivity, and sex: why female black rhinoceroses outlive males. Behav Ecol 6:57–64

    Article  Google Scholar 

  • Bigalke R, Steyn T, de Vos D, De Waard K (1950) Observations on a juvenile female square-lipped or white rhinoceros (Ceratotherium simum simum (Burch.)) in the National Zoological Gardens of South Africa. Proc Zool Soc Lond 120:519–528

    Article  Google Scholar 

  • Böhme M (2010) Ectothermic vertebrates (Actinopterygii, Allocaudata, Urodela, Anura, Crocodylia, Squamata) from the Miocene of Sandelzhausen (Germany, Bavaria) and their implications for environment reconstruction and palaeoclimate. Paläontol Z 84:3–41

    Article  Google Scholar 

  • Brain C, Forge O, Erb P (1999) Lion predation on black rhinoceros (Diceros bicornis) in Etosha National Park. Afr J Ecol 37:107–109

    Article  Google Scholar 

  • Caughley G (1966) Mortality patterns in mammals. Ecology 47:906–918

    Article  Google Scholar 

  • Cerdeño E (1996) Prosantorhinus, the small teleoceratine rhinocerotid from the Miocene of Western Europe. Geobios 29:111–124

    Article  Google Scholar 

  • Dittrich L (1972) Birth and growth of a male White rhinoceros Ceratotherium simum simum at Hanover Zoo. Internatl Zoo Yearbook 12:122–125

    Article  Google Scholar 

  • Dittrich L (1974) Beobachtungen zum Milchzahndurchbruch beim Spitzmaul- (Diceros bicornis) und Breitmaulnashorn (Ceratotherium simum). Säugetierk Mitt 22:289–295

    Google Scholar 

  • Fahlbusch V (1976) Die obermiozäne Wirbeltierfundstelle Sandelzhausen. Zbl Geol Paläont Teil II 5/6:255

    Google Scholar 

  • Fahlbusch V (2003) Die miozäne Fossil-Lagerstätte Sandelzhausen. Zitteliana A 43:109–122

    Google Scholar 

  • Fahlbusch V, Gall H, Schmidt-Kittler N (1972) Die obermiozäne Fossil-Lagerstätte Sandelzhausen. 2. Sediment und Fossilinhalt - Probleme der Genese und Ökologie. N Jb Geol Paläontol Mh 6:331–343

    Google Scholar 

  • Fortelius M (1985) Ungulate cheek teeth: developmental, functional, and evoutionary interrelations. Acta Zool Fenn 180:1–76

    Google Scholar 

  • Foster JB (1965) Mortality and ageing of black rhinoceros in east Tsavo Park, Kenya. E Afr Wild J 3:118–119

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Garutt NV (1994) Dental ontogeny of the woolly rhinoceros Coelodonta antiquitatis (BLUMENBACH, 1799). Cranium 11:37–48

    Google Scholar 

  • Goddard J (1966) Mating and courtship of the black rhinoceros in East Tsavo Park, Kenya. E Afr Wild J 3:118–119

    Google Scholar 

  • Goddard J (1970) Age criteria and vital statistics of a black rhinoceros population. E Afr Wild J 8:105–121

    Article  Google Scholar 

  • Godfrey LR, Samonds KE, Wright PC, King SJ (2005) Schultz’s unruly rule: dental developmental sequences and schedules in small-bodied, folivorous lemurs. Folia Primatol 76:77–99

    Article  PubMed  Google Scholar 

  • Groves C, Grubb P (2011) Ungulate Taxonomy. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Harvati K, Frost SR (2007) Dental eruption sequences in fossil colobines and the evolution of primate life histories. Internatl J Primatol 28:705–728

    Article  Google Scholar 

  • Heissig K (1968) Die Rhinocerotidae (Mammalia) aus der oberoligozänen Spaltenfüllung von Gaimersheim bei Ingoldstadt in Bayern und ihre phylogenetische Stellung. Ludwig-Maximilians-Universität, München

    Google Scholar 

  • Heissig K (1972) Die obermiozäne Fossil-Lagerstätte Sandelzhausen - 5. Rhinocerotidae (Mammalia) - Systematik und Ökologie. Mitt Bayer Staatssammlung Paläontol hist Geol 12:5781

    Google Scholar 

  • Hillman-Smith AKK, Groves CP (1994) Diceros bicornis. Mammal Species 455:1–8

    Article  Google Scholar 

  • Hillman-Smith AKK, Owen-Smith N, Anderson JL, Hall-Martin AJ, Selaladi JP (1986) Age estimation of the White rhinoceros (Ceratotherium simum). J Zool London 210:355–379

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Hitchins PM (1978) Age determination of the black rhinoceros (Diceros bicornis Linn.) in Zululand. S Afr J Wildl Res 8:71–80

    Google Scholar 

  • Hrabar H, Du Toit JT (2005) Dynamics of a protected black rhino (Diceros bicornis) population: Pilanesberg National Park, South Africa. Anim Conserv 8:259–267

    Article  Google Scholar 

  • Hutchins M, Kreger MD (2006) Rhinoceros behaviour: implications for captive management and conservation. Internatl Zoo Yearbook 40:150–173

    Article  Google Scholar 

  • Jordana X, Marin-Moratalla N, Moncunill-Sole B, Bover P, Alcover JA, Kohler M (2013) First fossil evidence for the advance of replacement teeth coupled with life history evolution along an anagenetic mammalian lineage. PLoS ONE 8:e70743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kindahl ME (1967) Some comparative aspects of the reduction of the premolars in the Insectivora. J Dent Res 46:805–808

    Article  CAS  PubMed  Google Scholar 

  • Klein RG (1982) Age (mortality) profiles as a means of distinguishing hunted species from scavenged ones in Stone Age archeological sites. Paleobiology 8:151–158

    Article  Google Scholar 

  • Klein RG, Cruz-Uribe K (1983) The computation of ungulate age (mortality) profiles from dental crown heights. Paleobiology 9:70–78

    Article  Google Scholar 

  • Koenigswald W von, Smith H, Arbor A, Keller T (2007) Supernumerary teeth in a subadult rhino mandible (Stephanorhinus hundsheimensis) from the middle Pleistocene of Mosbach in Wiesbaden (Germany). Paläontol Z 81:416–428

  • Kurtén B (1953) On the variation and population dynamics of fossil and recent mammal populations. Acta Zool Fenn 76:1–122

    Google Scholar 

  • Langer P (1988) The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution. Gustav Fischer Verlag, New York

    Google Scholar 

  • Langer P (2008) The phases of maternal investment in eutherian mammals. Zoology 111:148–162

    Article  PubMed  Google Scholar 

  • Laurie A (1982) Behavioural ecology of the Greater one-horned rhinoceros (Rhinoceros unicornis). J Zool London 196:307–341

    Article  Google Scholar 

  • Laurie WA, Lang EM, Groves CP (1983) Rhinoceros unicornis. Mammal Species 211:1

    Article  Google Scholar 

  • Lowe VPW (1967) Teeth as indicators of age with special reference to Red Deer (Cervus elaphus) of known age from Rhum. J Zool 152:137–153

    Article  Google Scholar 

  • Lubinski PM (2001) Estimating age and season of death of pronghorn antelope (Antilocapra Americana Ord) by means of tooth eruption and wear. Internatl J Osteoarchaeol 11:218–230

    Article  Google Scholar 

  • Luckett WP (1993) Ontogenetic staging of the mammalian dentition, and its value for assessment of homology and heterochrony. J Mammal Evol 1:269–282

    Article  Google Scholar 

  • Luo Z-X, Kielan-Jaworowska Z, Cifelli RL (2004) Evolution of dental replacement in mammals. Bull Carnegie Mus Nat Hist 36:159–175

    Article  Google Scholar 

  • Lyman RL (1994) Vertebrate Taphonomy. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mihlbachler MC (2003) Demography of late Miocene rhinoceroses (Teleoceras proterum and Ahelops malacorhinus) from Florida: linking mortality and sociality in fossil assemblages. Paleobiology 29:421–428

    Article  Google Scholar 

  • Miller RE (2003) Rhinoceridae (Rhinoceroses). In: Fowler ME, Miller RE (eds) Zoo and Wild Animal Medicine. Elsevier, Missouri, pp 558–569

    Google Scholar 

  • Morris P (1978) The use of teeth for estimating the age of wild animals. In: Butler PM, Joysey KA (eds) Development, Function and Evolution of Teeth. Academic Press, London, pp 483–494

    Google Scholar 

  • Moser M, Rössner GE, Göhlich UB, Böhme M, Fahlbusch V (2009) The fossil lagerstatte Sandelzhausen (Miocene; southern Germany): history of investigation, geology, fauna, and age. Paläontol Z 83:7–23

    Article  Google Scholar 

  • Owen R (1855) The Principle Forms of the Skeleton and the Teeth. Houlston & Stoneman, London

    Google Scholar 

  • Peter K (2002) Odontologie der Nashornverwandten (Rhinocerotidae) aus dem Miozän (MN 5) von Sandelzhausen (Bayern). Zitteliana 22:1–168

    Google Scholar 

  • Peyer B (1963) Die Zähne. Ihr Ursprung, ihre Geschichte und ihre Aufgabe. Springer-Verlag, Berlin

    Google Scholar 

  • Prothero DR, Guérin C, Manning E (1989) The history of the Rhinocerotoidea. In: Prothero DR, Schoch RM (eds) The Evolution of Perissodactyls. Oxford University Press, New York, pp 321–340

    Google Scholar 

  • Raposo-Amaral CE, Kobayashi GS, Almeida AB, Bueno DF, Rodrigues de Souza e Freitas F, Vulcano LC, Passos-Bueno MR, Alonso N (2010) Defeito ósseo alveolar em ratos para terapia celular. Estudo preliminar (Alveolar osseous defect in rat for cell therapy. Preliminary report). Acta Cir Bras 25:313–317

    PubMed  Google Scholar 

  • Ruscillo D (2006) Recent Advances in Ageing and Sexing Animal Bones. Oxbow Books, Oxford

    Google Scholar 

  • Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133

    Article  CAS  PubMed  Google Scholar 

  • Schmid W (2002) Ablagerungsmilieu, Verwitterung und Paläoböden feinklastischer Sedimente der oberen Süßwassermolasse Bayerns. Abh Bayer Akad Wiss Math-Naturw Klasse N F 172:1–247

    Google Scholar 

  • Schultz AH (1960) Age changes in primates and their modification in man. In: Tanner JM (ed) Human Growth. Pergamon Press, Oxford, pp 1–20

    Google Scholar 

  • Shpansky AV (2014) Juvenile remains of the “woolly rhinoceros” Coelodonta antiquitatis (Blumenbach 1799) (Mammalia, Rhinocerotidae) from the Tomsk Priob’e area (southeast Western Siberia). Quaternary Internatl 333:85–99

    Article  Google Scholar 

  • Smith BH (1994) Sequence of emergence of the permanent teeth in Macaca, Pan, Homo, and Australopithecus: its evolutionary significance. Am J Hum Biol 6:61–99

    Article  Google Scholar 

  • Smith BH (2000) ‘Schultz’s rule’ and the evolution of tooth emergence and replacement patterns in primates and ungulates. In: Teaford MF, Smith MM, Ferguson MWJ (eds) Development, Function and Evolution of Teeth. Cambridge University Press, Cambridge, pp 212–227

    Chapter  Google Scholar 

  • Tong H (2001) Age profiles of rhino fauna from the middle Pleistocene Nanjin Man Site, South China—explained by the rhino specimens of living species. Internatl J Osteoarchaeol 22:231–237

    Article  Google Scholar 

  • van Nievelt AFH, Smith KK (2005) To replace or not to replace: the significance of reduced functional tooth replacement in marsupial and placental mammals. Paleobiology 31:324–346

    Article  Google Scholar 

  • Van Valen L (1964) Age in two fossil horse populations. Acta Zool 45:93–106

    Article  Google Scholar 

  • Vera B, Cerdeño E (2014) Systematic revision of Antepithecus brachystephanus Ameghino, 1901, and dental eruption sequence in Eocene “notopithecines” (Notoungulata) from Patagonia. Geobios 47:60–74

    Article  Google Scholar 

  • Vigal CR, Machordom A (1985) Tooth eruption and replacement in the Spanish wild goat. Acta Theriol 19:305–320

    Article  Google Scholar 

  • Voorhies MR (1969) Taphonomy and population dynamics of an early Pliocene vertebrate fauna, Knox County, Nebraska. Univ Wyoming Spec Contrib Geol Spec Pap 1:1–69

    Google Scholar 

  • Ziegler AC (1971) A theory of the evolution of therian dental formulas and replacement patterns. Quart Rev Biol 46:226–249

    Article  Google Scholar 

Download references

Acknowledgments

Our gratitude goes to the late vertebrate palaeontologist Volker Fahlbusch who devoted an essential part of his life to the recovery and exploration of the Sandelzhausen fossils and site. The city of Mainburg, especially the then mayor Josef Egger, provided substantial support during excavations. Due to the committed excavation team and Mainburg residents the huge number of exceptional fossils were saved. The German Research Foundation (DFG) (Sonderforschungsbereich 53 “Paläoökologie”und GZ-4850/88/05), Stiftung zur Förderung der Wissenschaften, Wolf Klimatechnik GmbH, Sparkasse Kelheim, Deutsche Gleis und Tiefbau GmbH, Bosch-Siemens-Hausgeräte GmbH, Bayerische Akademie der Wissenschaften, Stadtsparkasse München, Pinsker Druck und Medien, Thyssen RÖRO, Ziegelwerk Leipfinger und Bader, VW-Werk, Elektrofirma Burger, Isar-Amper-Werke München gave financial support for excavation, preparation, and taxonomic as well as paleoecological research. We thank the radiological team of the Clinic for Small Animal Surgery at the Faculty of Veterinary Medicine of the Ludwig-Maximilians-Universität in Munich for producing the radiographs and CT scans. We thank G. Janssen (then Munich) for taking photographs of the fossils. We also acknowledge M. Krings (Munich) and S. Schneider (Cambridge) as well as two anonymous reviewers, whose helpful comments enhanced the quality of the manuscript.

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, Ludwig-Maximilians-Universität München, Richard-Wagner Straße 10, 80333, Munich, Germany

    Christine Böhmer, Kurt Heissig & Gertrud E. Rössner

  2. SNSB–Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner Straße 10, 80333, Munich, Germany

    Christine Böhmer, Kurt Heissig & Gertrud E. Rössner

  3. GeoBio-Center der Ludwig-Maximilians-Universität München, Richard-Wagner Straße 10, 80333, Munich, Germany

    Gertrud E. Rössner

Authors
  1. Christine Böhmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kurt Heissig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gertrud E. Rössner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine Böhmer.

Appendix

Appendix

Table 6 Prosantorhinus germanicus specimens measured in this study to evaluate dental wear
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Böhmer, C., Heissig, K. & Rössner, G.E. Dental Eruption Series and Replacement Pattern in Miocene Prosantorhinus (Rhinocerotidae) as Revealed by Macroscopy and X-ray: Implications for Ontogeny and Mortality Profile. J Mammal Evol 23, 265–279 (2016). https://doi.org/10.1007/s10914-015-9313-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-015-9313-x

Keywords

Search

Navigation