Generalized Individual Dental Age Stages for Fossil and Extant Placental Mammals

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Generalized individual dental age stages for fossil and extant placental mammals

Article in Paläontologische Zeitschrift · September 2011 DOI: 10.1007/s12542-011-0098-9

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Generalized individual dental age stages for fossil and extant placental mammals

Ulrike Anders • Wighart von Koenigswald • Irina Ruf • B. Holly Smith

Received: 20 August 2010 / Accepted: 7 February 2011 Springer-Verlag 2011

Abstract The traditional age stages for eutherian mam- vorgeschlagen, das auf dem Zahndurchbruch und der mals (infant, juvenile, adult, senile) can be difficult to Abrasion beruht. Sechs individuelle Altersstadien ‘‘indi- apply in the fossil record. Based on the tooth eruption and vidual dental age stages’’ (IDAS) werden definiert, die das wear of the cheek teeth we propose six ‘‘individual dental breite Spektrum der Placentalia abzudecken vermag. Die age stages’’ (IDAS) that can be applied to almost all fossil IDAS Stadien umfassen dabei die gesamte Lebensspanne and extant mammalian dentitions. The six stages of IDAS und korrelieren mit den neu definierten traditionellen cover the entire life span. Traditional terms can be corre- Bezeichnungen in folgender Weise: IDAS 0—pra¨natal, lated to the IDAS stages and thus redefined based on the IDAS 1—infantil, IDAS 2—juvenil, IDAS 3—adult, IDAS dentition: IDAS 0—prenatal, IDAS 1—infant, IDAS 2— 4—spa¨t adult und IDAS 5—senil. Daru¨ber hinaus erlaubt das juvenile, IDAS 3—adult, IDAS 4—late adult, and IDAS IDAS System, die La¨nge der Entwicklungsphasen ver- 5—senile. Furthermore IDAS enables comparison between schiedener Taxa, bis hin zu Ordnungen zu vergleichen und individuals, characterizing the mortality in monospecific damit zu charakterisieren. Ebenso bietet sich die Mo¨glich- populations, and even of entire communities composed of keit die Altersverteilung in fossilen Populationen fu¨r eine various species. The data obtained can be used for paleo- Art, aber auch fu¨r ganze Vergesellschaftungen in einer ecological interpretations. The varying duration of different Fundstelle zu vergleichen. Damit ero¨ffnet das IDAS-System stages in the IDAS pattern during the life history forms an Wege, Beitra¨ge zu verschiedenen palaöo¨kologischen Fragen additional way to characterize mammalian groups by zu liefern. development and wear of their dentition. Schlu¨sselwo¨rter Eutheria Á Altersstadien Á Bezahnung Á Keywords Eutheria Á Age stages Á Dentition Á Attrition Á Palaöo¨kologie Dental attrition Á Paleoecology

Kurzfassung Altersbestimmungen durch die traditionel- Introduction len Begriffe infantil, juvenil, adult oder senil kann fu¨r fossile Eutheria meist nur bedingt angewendet werden. Deswegen Classification of individual age of fossil and extant euthe- wird hier ein generell anwendbares Alterssystem (IDAS) rian mammals is important for ecological investigations and paleoecological reconstructions. Most aging schemes were established for wildlife management (e.g., Severing- & U. Anders ( ) Á W. von Koenigswald Á I. Ruf haus 1949; Gee et al. 2002) and for the understanding of Steinmann-Institut fu¨r Geologie, Mineralogie und Palaöntologie, Rheinische Friedrich-Wilhelms-Universita¨t Bonn, Nussallee 8, mammal populations in terms of life span, mortality, herd 53115 Bonn, Germany growth, and reaction to ecological factors (Severinghaus e-mail: [email protected] 1949; Rausch 1961; Lowe 1967; Morris 1972). The age of single individuals also has particular importance for B. H. Smith Museum of Anthropology, The University of Michigan, forensic identification in modern humans (e.g., Gustafson Ann Arbor, MI 48109-1107, USA 1950; Smith 1992). For the interpretation of fossils, 123 U. Anders et al. individual age can establish the pace of life history (Bro- species aging system for extant species. The great diversity mage and Dean 1985). in the dentition of placental mammals with reduction of The goal of most aging studies is to age the animal in several tooth positions limits the comparability to some years, whether based on fusion of the epiphyses or sutures degree, but slight modifications within the IDAS system in the skeleton (e.g., Brothwell 1972; Driesch 1976; allow including those taxa as well. These deviations from Knußman and Martin 1988;Sańchez-Villagra 2010) or size the normal IDAS system are new characteristics for the of horns in bovids and antlers in cervids (e.g., Fuller 1959; various mammalian groups. Finally, we redefine the tra- Chaplin and White 1969; Miura 1985). Others use char- ditional terms ‘‘prenatal’’, ‘‘infant’’, ‘‘juvenile’’, ‘‘adult’’, acters in the dentition, such as tooth eruption and wear ‘‘late adult’’, and ‘‘senile’’ for extant and fossil taxa with (e.g., Nostrand and Stephenson 1964; Gustafson 1950; the IDAS system based on tooth eruption and wear. Lowe 1967; Goddard 1970; Habermehl 1975, 1985; Louguet 2006; Magnell and Carter 2007; Greenfield and Arnold 2008; Munro et al. 2009; Kelley and Schwartz Materials and methods 2010) or the annual cementum layers on roots in teeth (e.g., Adams and Watkins 1967; Linhart and Knowlton 1967; For the definition of the six IDAS stages we use the fol- Reimers and Nordby 1968; Wolfe 1969; Crowe 1972; lowing characters: eruption of the deciduous and perma- Gasaway et al. 1978; Bodkin et al. 1997; Hamlin et al. nent dentition, first wear facets on molars, loss of 2000; Costello et al. 2004; Roksandic et al. 2009). These structured occlusal surface, and breakdown of the denti- age classifications are often very detailed and complex, but tion. Our study is based on a broad survey of placental applicable only to the species on which they are based, e.g., mammalian dentitions. The investigated species are almost Gazella gazella (Munro et al. 2009), Diceros bicornis all undomesticated to minimize possible human impact on (Goddard 1970) or a very close relative (e.g., Adam 1994). life span. For the design of the IDAS stages, but prior to Due to the great differences in maximum life span of testing and comparing the system on different species, mammals, establishing the age of an individual at death, information about tooth eruption and tooth wear was however, tells us little about its stage of life, and is only gathered from a large number of fossil and extant indi- meaningful with reference to some other events within the viduals from various orders (Lagomorpha, Rodentia, Arti- particular species. Even the classical terms juvenile, adult, odactyla, and Carnivora) (Appendix 1). In addition, we and senile may be poorly defined and difficult to compare investigated tooth eruption shortly after birth in serial between different species (see Table 1 below). histological sections of perinatal stages of seven rodent and For paleontological questions especially, the dentition is two lagomorph species (Appendix 1). Available informa- a useful base for aging, since dentitions are well docu- tion from various orders (Rodentia, Chiroptera, Scandentia, mented in the fossil record. Therefore, we propose a gen- Carnivora, Primates, Perissodactyla, Artiodactyla, and eralized system of IDAS (individual dental age stages) that Proboscidea) concerning tooth eruption, tooth wear, and is not based on years but on tooth eruption and tooth wear. life history (weaning, maturity, individual age, and maxi- By defining functional key points in our classification mum life span) were added from literature (Appendix 2). independent of calendar years, we hope to minimize the The resulting data are used to estimate the length of the effect of the great diversity in maximum life span and IDAS stages among different eutherian mammals. We then construct a standard useful to describe an individual or an correlate the duration of the various IDAS stages with assemblage. maximum life span (data from Nowak 1999; Weigl 2005). We are well aware that individual age determination Furthermore, mortality distributions of different fossil based on the IDAS system cannot be as precise as a single populations are identified based on the IDAS system.

Table 1 Correlation of the IDAS stages to age determinations of different species to illustrate the transferability of the IDAS system IDAS Common use but Schultz (primates) Knußmann 1988 (humans) Grau et al. 1970 Goddard 1970 rarely deﬁned (racoons) (rhinoceros) 1935 1960

0 Prenatal Fetus 1 Juvenile Infantile Young Infans I, II Class I–VI 2 Juvenile Juvenis Class VII–XI 3 Adult Adult Adult Adultus/matures Class I–III Class XII–XVI 4 Class IV Class XVII–XVIII 5 Senile Old Senilis Class V Class XIX–XX

123 Generalized individual dental age stages for fossil and extant placental mammals

Lastly, as an example for the mortality in a complex fossil • IDAS 2 (juvenile) covers the period from the first facets site, we construct the distribution of IDAS for individuals on the first molar to the fully erupted permanent of different orders from documentary photographs of the dentition. Ho¨wenegg assemblage (Tobien 1959; 1986;Hu¨nermann • IDAS 3 (adult) covers the period from full eruption of 1989; Bernor et al. 1997), representing an upper Miocene the dentition until the loss of the ‘‘inner profile’’ of the lake deposit in Germany. The included individuals are first molar (i.e., the occlusal surface is free of interior listed in Appendix 1. enamel and the enamel rim is not broken down). • IDAS 4 (late adult) lasts from the loss of the inner profile in the first molar until the loss of the inner Results and discussion profile in the second molar. • IDAS 5 (senile) covers from the loss of the inner profile Definition of individual dental age stages of the second molar to the complete breakdown of the dentition by wear and/or tooth loss. Based on fossil and recent material, data from literature, • These IDAS stages are ordered and meant to be and histological serial sections we propose six stages of mutually exclusive. They are applicable across species individual dental age (IDAS): with various tooth types (Fig. 1). • IDAS 0 (prenatal) comprises the prenatal stage of tooth development. Although IDAS 0 cannot be determined IDAS stages and life history in the teeth directly, we included it to characterize the prenatal stages. Especially in the fossil record this stage Definitions of IDAS stages are based on tooth eruption and needs independent evidence that the individual died wear because these dental characters are widely applicable before birth. to fossil individuals. Furthermore, these dental characters • IDAS 1 (infant) denotes the period from birth to the are also relevant in a biological context in most mamma- first attritional facets on the erupted first molar. lian species.

Fig. 1 Examples of IDAS stages 1–5 as applied to bunodont and selenodont species (left Sus scrofa; right Capreolus capreolus, both extant, Germany). Scale bar 1 cm 123 U. Anders et al.

IDAS 0 designates prenatal tooth development. most or all females will be reproducing in stage 3. In extant Although deciduous teeth are mineralized almost entirely eutherian mammals, the length of IDAS 3 demonstrates an in utero, the state of tooth eruption differs greatly at birth explicit variability in different taxa (e.g., bovids versus (Smith 2000; Gingerich et al. 2009). Some eutherians are cervids, see below). generally born without teeth, e.g., the carnivores, and IDAS 4 represents the functional reduction of the den- others erupt some teeth before birth or shortly afterwards, tition, covering the loss of structure in the first molar and notably in primates, artiodactyls, pinnipeds, and cavi- up to the time the second molar becomes worn out. It is a omorphs (Harman and Smith 1936; Kubota et al. 1961; period of transition to the beginning of the functional Habermehl 1975, 1985; Smith et al. 1994). Some early- breakdown of the entire dentition. In the life history of erupting teeth have special functions, notably the hooked most eutherian mammals, IDAS 4 is the late adult stage. incisors newborn bats use to cling to the mother’s fur IDAS 5 is defined by a more or less worn out tooth row during flight (Reeder 1953). IDAS 0 is rare in the fossil lacking the functional structures needed for effective food record but is known in several fetuses of ancestral horses grinding; single tooth positions may be already lost. Many (Tobien 1959; Franzen 2006) and an archaeocete whale individuals do not live until this stage in the wild because (Gingerich et al. 2009). of predators, diseases or, perhaps, the incapability to get In IDAS 1 the deciduous dentition dominates. We enough energy to survive. In herbivores the functional mark the end of IDAS 1 with the first attritional facets on efficiency of teeth is a key limiting factor to energy harvest the first molar because in biological terms it often marks as the loss of shearing blades or the loss of the blade the changeover to independent feeding, clearest for the sharpness reduces the grinding capacity of the dentition case of primates, where the eruption of the first permanent (Popowics and Fortelius 1997). However, extremely poor molar approximately equals the time of weaning (Smith dental conditions can occasionally be seen in some indi- 1991, 1992, 2000; Kelley and Smith 2003: Fig. 9). viduals. The Gombe female chimpanzee ‘‘Old Flo’’ is a Weaning young shortly before or shortly after the emer- striking example (Kilgore 1989). In a comparison of life gence of the first permanent molar appears to be wide- history, we can propose that IDAS 5 starts later in animals spread in ungulates as well (Smith, unpublished data). with hypsodont teeth, e.g., horses, than in animals with Thus the entire IDAS 1 period covers the time when brachydont teeth, e.g., suids. eutherian mammals learn to eat an adult diet while still supplemented with mother’s milk (Smith 2000). Some Applications of the IDAS system eutherian mammals, notably those born dentally super- precocious, may wean well after appearance of first The classical terms infant, juvenile, mature, adult, and molars, but the duration of IDAS 1 is rarely more than senile describe stages of life history that are underlain by 1 year in extant eutherian mammals, with exceptions for hormonal changes and behavior in addition to growth; they only the largest, very long-lived species e.g., rhinos, are also used by paleontologists to describe maturation of elephants, or hominoid primates including Homo sapiens hard tissues, especially dental eruption and wear stages. (Langer 2008). Thus, we correlate the IDAS stages to classic stages when During IDAS 2 the permanent dentition is established possible and to criteria established by studies of aging and subsequently comes into function, and deciduous teeth dentition (Table 1). On the one hand we observe that single are fully replaced. The last tooth to erupt differs in age classes can involve multiple IDAS stages (e.g., Schultz eutherian mammals and is often not the third molar (Smith 1935, 1960; Knußman and Martin 1988), on the other hand, 2000). A few of the placental mammals, for example, multiple age classes of these earlier studies can merge into elephants and hyraxes, show an extended tooth eruption one IDAS stage (e.g., Goddard 1970; Grau et al. 1970). and replacement continuing into adulthood or even IDAS stages should be general enough to fit into a wide throughout life (see Asher and Lehmann 2008). range of age classification studies. IDAS 3 is characterized by the use of the full permanent dentition; we mark its end with the loss of the occlusal IDAS stages of selected fossil individuals surface in the first molar. The stage IDAS 3 is commonly represented in literature because it includes the full per- The IDAS stages can be used to indicate the age of indi- manent dentition with all functional structures visible. It viduals of almost all orders of placental mammals. The appears that small to medium sized eutherian mammals fossil examples shown here are predominantly from start reproducing after completion of the dentition, thus paleoanthropology because they are well described and during IDAS 3 (Shigehara 1980; Smith 1992), although more familiar than many other mammalian fossils. Nev- more evidence is needed for such generalizations. ertheless, applicability to different placental mammalian Although some species begin in stage 2, we assume that orders is documented in the figures below. 123 Generalized individual dental age stages for fossil and extant placental mammals

Fig. 2 Tooth development in a fetal whale (Maiacetus inuus) from the Eocene of Pakistan, representing IDAS 0 (modiﬁed from Gingerich et al. 2009)

IDAS 0 is rare in the fossil record but is known in are already incorporated into the tooth row and in contact several fetuses of the horse Cromohipparion primigenius with their antagonists, but the permanent dentition is not from Ho¨wenegg (Tobien 1959, 1986), Propalaeotherium complete. As an additional example, a rhino mandible from (Eurohippus) parvulum from Messel (Franzen 2006, 2007), the Pleistocene, Stephanorhinus hundsheimensis, with a or the whale fetus of Maiacetus inuus from Pakistan slight dental abnormality was described from Mosbach (Gingerich et al. 2009) (Fig. 2). (Germany) as subadult, an undefined age stage (Koenigs- IDAS 1 includes one of the best known hominid fossils, wald et al. 2006). Although its deciduous teeth are the ‘‘Taung child,’’ which is the type of Australopithecus replaced, m3 is partially in the alveolus, showing that it africanus (Dart 1925). The teeth of the upper and lower jaw occupied IDAS 2 at death. Other examples of mammalian are well preserved. The first permanent molar has just individuals representing IDAS 2 are shown in Fig. 4. started to erupt and was not yet in function (Conroy and IDAS 3 is very common in the fossil record. Many Vannier 1987). Other mammalian examples that fit IDAS 1 dentitions figured in the paleontological literature represent are presented in Fig. 3. an early IDAS 3, since all morphological characters are IDAS 2 is represented by the Homo erectus fossil KNM- visible in this stage with limited abrasion showing the WT 15,000, the ‘‘Turkana boy’’ (Brown et al. 1985) who functional context. The lower hominid jaw from Mauer died in IDAS 2. The juvenile age of that individual is (Homo heidelbergensis) with all permanent teeth in func- shown by the unfinished tooth eruption of the third molars tion, somewhat worn, can be classified as IDAS 3 (Johanson and upper canines (Smith 1993). and Edgar 2000). A greater variety of individuals in IDAS 3 Another individual representing IDAS 2 is the most is shown in Fig. 5. complete primate skeleton from the Eocene of Messel, The duration of IDAS 4 in most species may be brief. Darwinius masillae. Although the cranium is compacted This stage is represented by the mandible Ehringsdorf F the stage of tooth replacement can be deduced from micro (Homo neanderthalensis) from Weimar-Ehringsdorf with CT scans (Franzen et al. 2009). The first and second molars the first molars worn out, whereas the second molars show

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Fig. 3 Examples of extant and fossil placental species from different Vypustek); d Gomphotherium angustidens (Miocene, Hofkirchen); orders in IDAS 1 with deciduous dentition and the M1/m1 not yet e Equus caballus (extant, Bonn); f Prosanthorhinus germanicus erupted. a Canis lupus (Recent, no data); b Crocuta spelaea (Late (Miocene, Sandelzhausen); g Sus scrofa (extant, Wachtberg-Villi- Pleistocene, Oberniesen); c Ursus spelaeus (Late Pleistocene, prott); h Capreolus capreolus (extant, Wolthausen) only moderate wear (Schwalbe 1914; Vlcˇek 1993). Other found near Koblenz (Germany). Elephants differ in their examples of individuals in stage IDAS 4 are given in Fig. 6. mode of tooth replacement from most eutherian mammals. IDAS 5 is exemplified by the Neanderthal skull ‘‘La However, it is possible to apply the IDAS system to ele- Ferassie 1’’ (Homo neanderthalensis) (Boule 1921; Puech phants at least in later stages. Based on the definition of 1981). The first and second molars in this individual are three deciduous premolars and three molars in elephants worn out. Another hominid example is the skull of La (Adam 1994; Louguet 2006), the very large third molar of Chapelle-aux-Saints where all cheek teeth are lost and the the individual from Koblenz is already heavily reduced by alveoli are almost closed (Boule 1921). Furthermore IDAS wear and the first and second molars are already lost 5 is represented by a skeleton of Mammuthus primigenius (Koenigswald 1989). That allows the classification to

123 Generalized individual dental age stages for fossil and extant placental mammals

Fig. 4 Examples of extant and fossil placental species from different e Anchitherium aurelianense (Miocene, Sandezhausen); f Stephano- orders in IDAS 2 with the permanent dentition not fully erupted yet. rhinus hundsheimensis (Middle Pleistocene, Mosbach); g Caenomeryx a Crocuta spelaea (Late Pleistocene, Villa Seckendorf); b Castor ﬁlholi (Oligocene, Gaimersheim); h Schizoporcus muenzenbergensis canadensis (extant, Wyoming); c Palaeolagus sp. (Eocene/Oligocene, (Miocene, Sandelzhausen) Nebraska); d Elephas trogontherii (Middle Pleistocene, Mosbach);

IDAS 5. Other individuals in stage IDAS 5 are shown in Fluctuations in population size or age structures have been Fig. 7. correlated to some parameters, e.g., climatic changes or seasonal events such as cubbing season (Kurte´n 1954). Fossil population dynamics expressed in the IDAS Stable populations are indicated by the dominance of indi- system viduals of reproductive age (Klein and Cruz-Uribe 1983). Prime reproductive age should be represented by IDAS 3. Population dynamics are important for interpreting the Catastrophic events as well as a time-averaged assemblage ecology of recent and fossil animals (Kurte´n 1953). of some duration can display a snapshot of a stable fossil

123 U. Anders et al.

Fig. 5 Examples of extant and fossil placental species from different Pleistocene, Swabian Alb); f Palaeolagus sp. (Eocene/Oligocene, orders in IDAS 3 with the fully erupted permanent dentition and only Nebraska); g Stromeriella franconica (Miocene, Wintershof-West); moderate wear. a Talpa europaea (extant, Tu¨bingen); b Megatherium h Dicerorhinus sp. (Early Pleistocene, Bru¨ggen); i Papio ursinus americanum (from Owen 1956); c Cynocephalus volans (extant, no (extant, Namibia); j Procervulus aurelianensis (Miocene, Wintershof- data); d Castor fiber (extant, Engure); e Dicrostonyx torquatus (Late West) population representing individuals from all age stages (Klein and Cruz-Uribe 1983). Such an overrepresentation (Klein and Cruz-Uribe 1983). In tests of the IDAS system to of young and old individuals (IDAS 1, 2 and 4, 5) is visible date on examples of different extinct species and localities in some cave bear sites where fewer individuals in IDAS 3 we find that IDAS 3 is dominant (Fig. 8a). are present. These observations are best explained by An overrepresentation of young or old individuals in a hibernation. More vulnerable individuals, such as the very fossil population is often correlated with difficult circum- young or even very old individuals, may not survive stances such as starvation, accidents, predators, or diseases through hibernation, dying in the caves (Grandal-D’An- that affect the most vulnerable members of a population glade and Vidal Romanı´ 1997; Stiner 1998).

123 Generalized individual dental age stages for fossil and extant placental mammals

Fig. 6 Examples of extant and fossil placental species from different sp. (Eocene/Oligocene, Nebraska); e Dicerorhinus hundsheimensis orders in IDAS 4 with the ﬁrst permanent molars having lost their (Pleistocene); f Hippopotamus amphibious (extant, Africa); g Camelus inner enamel structures on the occlusal surface. a Crocuta spelaea bacterianus (extant, Lanzerote), h Schizoporcus muenzenbergensis (Late Pleistocene, Sundweg); b Ursus spelaeus (Late Pleistocene, (Miocene, Sandelzhausen) Letmathe); c Cynomys ludovicianus (extant, Montana); d Palaeolagus

As another example, we applied the IDAS system to occurrence of IDAS 1 and 2 indicates that young and fossil cainotheres, extinct rabbit-sized ruminants from the therefore smaller individuals were more vulnerable victims Tertiary of Europe (Fig. 8b): Caenomeryx filholi from a of these birds of prey. fissure filling of Gaimersheim [late Oligocene (MP28), The IDAS system allows description of general patterns Bavaria, Germany], Cainotherium sp. from the freshwater of mortality and/or preservation represented at specific sites limestones from Saulcet [early Miocene (MN1), Allier, even if various species are involved. The lake deposits from France], and Cainotherium huerzeleri from the freshwater Ho¨wenegg (upper Miocene MN9, Hegau, Germany) are deposits of Steinberg near No¨rdlingen [middle Miocene famous for the mammalian skeletons preserved in full (MN6), Ries crater, Germany]. In Gaimersheim and Saul- articulation. At least two superimposed layers of carcasses cet, the IDAS stages show attributes of a stable population were observed (Tobien 1986;Hu¨nermann 1989; Bernor et al. with most individuals in IDAS 3. In the Steinberg fauna the 1997). To classify the Ho¨wenegg sample, we supplemented juvenile stages IDAS 1 and 2 are overrepresented. The the few published illustrations with unpublished photo doc- accumulation at Steinberg is most probably caused by birds umentation provided by R. Bernor and D. Wolf. In all, 46 of prey (Heizmann and Fahlbusch 1983). The preferential individuals representing Hippotherium, Aceratherium,

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Fig. 7 Examples of extant and fossil placental species from different Nebraska); c Mammuthus primigenius (Late Pleistocene, Polch); orders in IDAS 5 with the ﬁrst and second molars having lost their d Hyracodon nebrascensis (Oligocene, South Dakota); e Capreolus inner enamel structures on the occlusal surface. a Ursus spelaeus capreolus (extant, Unterschmeien); f Homo sapiens (Late Pleistocene, (Late Pleistocene, no data); b Palaeolagus sp. (Eocene/Oligocene, Bonn-Oberkassel)

Chalicotherium, Dorcatherium, Miotragocerus, and Mun- (IDAS pattern). Maximum life spans have been published tiacus could be classified into IDAS stages. Results show that for a wide range of extant species, e.g., by Finch (1990), young individuals are underrepresented and very old or Nowak (1999), Wilson and Ruff (1999), and Weigl (2005). senile individuals are missing at Ho¨wenegg (Fig. 8c). IDAS The length of the various IDAS measured in years differs 1 is represented only by a single Hippotherium and IDAS 2 significantly between taxa because of enormous differences by one Aceratherium, one Dorcatherium, and three indi- in maximum life span. Even if the length of the IDAS viduals of Miotragocerus. The bulk of individuals represent stages is plotted against the maximum life span (100%) IDAS 3 (38 individuals). The Hippotherium with one fetus significant differences occur within species and higher (IDAS 0) and the Miotragocerus with two fetuses both rep- taxonomic units (Figs. 9, 10). resent IDAS 3, indicating that this stage coincides with reproductive activity. There are no individuals representing Comparison of the IDAS pattern between cervids IDAS 4 or 5. Accordingly, the animals represented by the and bovids carcasses in the lake deposits of Ho¨wenegg were almost fully grown. Thus, the mammalian fauna of Ho¨wenegg does Cervids are compared with bovids in terms of their IDAS represent a specific—so far unidentified—selection, but not pattern relative to life span (Fig. 9). In cervids, IDAS 2 is a random sample from a stable population, which should relatively short, covering about 10% of life span and IDAS include a higher proportion of adolescents and seniles. 5 starts distinctly earlier than in bovids. In contrast, bovids enter IDAS 3 at around 20% of life span, and compared to Comparison of the relative length of the IDAS cervids, enter IDAS 4 and 5 very late. These differences are in various mammalian groups best explained by the hypsodonty of bovids. Because of their high crowned teeth, the occlusal profile is in function Mammalian orders can be characterized by the relative for a long time without constraint. Hypsodont teeth provide length of each IDAS compared to the maximum life span more material for wear since the teeth erupt over a long

123 Generalized individual dental age stages for fossil and extant placental mammals

Fig. 8 IDAS distribution from fossil populations of selected euthe- filholi, Cainotherium huerzeleri, Cainotherium sp.) of different rian species. a Single species (Hyotherium meissneri, Crocuta localities (Gaimersheim, Saulcet, Steinberg im Ries). c Species spelaea, Cervidae) in various fossil localities (Westtangente Ulm, composition and IDAS distribution at one locality (Ho¨wenegg) Villa Seckendorf). b IDAS distribution in cainotheres (Caenomeryx time (Koenigswald 1982). The expansion of hypsodonty to seen in Ovis and Gazella, may correlate to a particularly the deciduous dentition in bovids probably delays tooth abrasive food (Fig. 9). replacement. Thus, the permanent tooth row comes into We expect tooth replacement to be a more stable signal, function relatively later. whereas tooth wear should more easily differ, as it is more Duration of IDAS stages in cervids studied here is more influenced by external factors. We observed, however, variable than in the bovids. The variability is obvious some differences in juvenile stages based on tooth especially in later stages where different kinds of foods due replacement. Rangifer for example has a relatively long to various habitats can affect the brachydont dentition phase of IDAS 2 (about 14% of life span). In comparison, comparatively much. In cervids, the lower crowned teeth IDAS 2 is of short duration with about 6% of life span in lose their functionality distinctly earlier. Odocoileus and Capreolus and Odocoileus. Rangifer have the shortest IDAS 4 stages, which may be In cervids IDAS 5 is only valid for single individuals related to a more abrasive food. Some Rangifer populations (Fig. 9) because the maximum life spans are usually in Scandinavia have been observed in areas with a high records from captivity (e.g., zoo animals), and reaching this degree of sand in their food, which must lead to relatively mark may be very rare in the wild. If, however, we include high abrasion of the dentition (Bromeé-Skuncke 1952). the average life span (Fig. 9: vertical bars) as a percentage However, also in bovids a comparably shorter IDAS 3, as of the maximum life span, we can observe that the bulk of

123 U. Anders et al.

individuals die around the end of IDAS 4 (e.g., Capra, Ovis, Odocoileus, Capreolus, Cervus) or the beginning of IDAS 5 (e.g., Rupicapra, Bison, Alces, Rangifer, Dama) with the loss of the occlusal surface in the second molar. Despite individual variation, the trend for the mean of the average life span in bovids (*82%) is near to the maximum life span (100%). In contrast, cervids show a relatively short mean of average life spans (*54%). In summary, hypsodonty promotes the functionality of the dentition also in relatively old individuals, which allows the survival of the bulk of individuals for a longer time.

Comparison of IDAS pattern between orders

The IDAS system may also be used to compare species of different orders (Fig. 10), although differences in the IDAS Fig. 9 Percentage distribution of the single IDAS stages in some pattern may correlate with the mode of tooth replacement, bovid and cervid species relative to the maximum life span (100%). tooth types, or ecology. The vertical bars indicate the average life span of the species. The oblique edges at the end of the bars in IDAS 3 and 4 show the The time of tooth replacement (IDAS 1 and 2) covers a variation of these stages. Data from literature (Appendix 2). Asterisk shorter period or is totally reduced in some smaller indicates species with no or incomplete information for eruption and/ eutherian mammals such as eulipotyphlans (Erinaceus), or wear (represented by greater oblique edges) rodents (Castor, Rattus), and lagomorphs (Lepus) but is also shortened in carnivores (Canis, Felis, Procyon). In rodents and lagomorphs, many species are born with erupted permanent incisors, premolars, and even molars, e.g., Oryctolagus, Petromus, Octodon, Chinchilla (personal observations) and as observed in Cavia (Harman and Smith 1936; personal observations). Some rodent species even have no deciduous teeth when they are born (e.g., Rattus). The advantage of a short IDAS 1 and 2 is acceleration to a full functional dentition especially in species with a relatively short average life span (see Fig. 10, e.g., Rattus, Lepus). The short average life span in rodents and lagomorphs may arise from intrinsic factors (e.g., high met- abolic rate), as well as extrinsic factors (e.g., predation). Small bodied species have a higher mass-speciﬁc meta- bolic rate and also a higher mortality in the wild (Promi- slow and Harvey 1990). Thus, in these groups the wear of their teeth and the breakdown of the dentition is in all probability not the limiting factor for their life span. Unlike rodents and lagomorphs, carnivores are almost always born without any teeth, although tooth eruption begins shortly after birth. In this group the later IDAS stages 4 and 5 are the limiting factor for life span. The average life span in the included species is around the end of IDAS 4, correlating with the breakdown of the carnassials and the following molars (Fig. 10). Fig. 10 Percentage distribution of the single IDAS stages in repre- An elongation of the IDAS 1 and 2 is observed in some sentatives of different mammalian orders relative to the maximum life artiodactyls and perissodactyls. According to preliminary span (100%). The vertical bars indicate the average life span of the observations, an extended period of tooth replacement in species. The oblique edges at the end of the bars in IDAS 3 and 4 show the variation of these stages. Data from literature (Appendix 2). herbivores leads to an extended function of the occlusal Asterisks indicate species with no or incomplete information for proﬁle. In primates the juvenile stages last up to 30% of the eruption and/or wear (represented by greater oblique edges) maximum lifetime (Fig. 10). For primates the expanded 123 Generalized individual dental age stages for fossil and extant placental mammals

IDAS 1 and 2 relate to an extended youth that correlates the end of IDAS 1 coincides with the beginning of IDAS 3 with an enlarged brain, enhanced learning and sociality and the fully erupted dentition. IDAS 5 cannot be defined in (Harvey and Clutton-Brock 1985). these species because of the absent second and third molars. IDAS 3 can last very long in animals with more hyp- Although the system shows a wide applicability there sodont teeth as described above in bovids. Especially in are some species with specialized dentitions that cannot be species with euhypsodont teeth (e.g., lagomorphs), the included. Because of polydonty, reduced tooth formulae, occlusal surface persists in IDAS 3 for the whole life span. absent teeth, and in some cases horizontal tooth exchange, In these cases, the completion of the crown base is delayed species such as pinnipeds, whales, manatees, and toothless throughout the normal life expectancy (Koenigswald eutherians (e.g., anteaters) fall out of our system. In our 1982). study we have concentrated on the dentition of placental In other species, the late IDAS stages are more signifi- mammals. However, the system can be expanded to cover cant. IDAS 4, for example, covers a fairly long period in marsupials and even Mesozoic mammals. Although most Ovis and Diceros.InProcyon, Capreolus, and Sus IDAS 5 marsupial mammals have an increased number of molars lasts for a long time. But in terms of the average life span and special characteristics throughout eruption where only the bulk of individuals in these species will die earlier (see one premolar is replaced (Cifelli and de Muizon 1998; Van average life span in Fig. 10). In most species the average Nievelt and Smith 2005), the IDAS stages are defined by life span ends in IDAS 4. The functional occlusal surface is dental characteristics also occurring in these groups. The highly reduced in IDAS 5. In rare cases dental breakdown eruption of the first molar can be identified for IDAS 1. may reach the point at which not enough food can be Although marsupials do not replace all premolars, the processed to sustain the animal, e.g., as proposed for the dentition reaches an adult stage where the tooth replace- mammoth of Polch (Koenigswald 1989). But in some ment is completed, which defines the changeover from species many individuals can also survive until IDAS 5. IDAS 2 to IDAS 3. To define IDAS 3, 4, and 5 in mar- For example, due to the elongation of the third molar, the supials, criteria are much the same as for placental mam- functionality of the dentition of Sus can be preserved also mals. But as in eutherians some exceptions in marsupials in IDAS 5 for a long time. can be observed. In some kangaroo species due to the horizontal tooth exchange the last molar comes into func- Application of the IDAS system to specialized tion very late, which causes overlapping of the IDAS stages dentitions as observed in elephants. In Mesozoic mammals, the famous skeleton of the In eutherian mammals with reduced or expanded tooth dryolestid Henkelotherium guimarotae from the Upper formulae, slight adaptations to IDAS are necessary. Unu- Jurassic of Portugal has a fully developed dentition and all sual IDAS scores relative to life stages or overlapping deciduous teeth are shed (Krebs 1991). The attrition of the stages may point out more extreme or unusual adaptations. molars is minor. Thus, the individual can be attributed to In elephantids such as Elephas and Mammuthus, a hor- IDAS 3, although the tooth formula differs distinctly from izontal tooth replacement can be observed. The six cheek that of the eutherian mammals in having five upper and teeth (three milk premolars and three molars) follow each seven lower molars. other through their life and only one or two of them are in function at the same time (Adam 1994; Louguet 2006). Due to the horizontal tooth replacement, IDAS 2, 3, and 4 Conclusions overlap in a very specific way (Fig. 10). While the tooth replacement (IDAS 2) lasts until the third permanent molar Although variability in the dentition of placental mammals (M3/m3) comes into function, the first and second perma- is considerable, we have tried to establish a system that nent molars (M1/m1, M2/m2) erupt and are worn out compares mammalian taxa in terms of dental abrasion and (IDAS 3 and 4) before the end of IDAS 2. Only IDAS 1 functionality independently of their age in years and that and 5 can be clearly separated. This is an example of how can be applied to a wide range of taxa. The system of the analysis of IDAS stages can highlight special charac- individual dental age stages (IDAS) has the potential to teristics in the dentition. characterize extant as well as fossil individuals. Further- With some limitations even reduced dentitions can be more, IDAS can be used to classify members of extinct described in the IDAS system by relying on functional species into functional age groups, even if no extant rela- changes. For example, in spotted hyenas (Crocuta crocuta) tives are available from which the individual age in years the number of molars is reduced. Because there is no upper can be deduced. These functional age groups are also first molar, IDAS 1 and 2 can only be defined in the lower applicable with slight adaptations to species with expanded jaw. In the upper jaw only IDAS 1 can be identified. There, or reduced tooth formulae (e.g., elephants or hyenas). 123 U. Anders et al.

In summary, IDAS 0 represents the prenatal stage. IDAS Material used for mortality curves 1 covers the stage until the m1 shows first wear facets and many placental mammals are weaned. IDAS 1 and 2 Crocuta spelaea (Villa Seckendorff), n = 20 (SMNS: together, which cover the time until the entire dentition is 31334–31337, 31340, 31341, 31365, 31369–31378, 31380, in function, become a definition for ‘‘juvenile’’. IDAS 3 is 31404, 31406) hypothesized to be the time of maximum activity and Hyotherium meissneri (Westtangente Ulm), n = 22 prime reproduction in most eutherian mammals; it can be (SMNS: 44833–44839, 44841–44845, 44847, 44853, shown to be very common in the fossil record. IDAS 4 and 44854, 44859, 44865, 44884, 44888, 45125, 45395) IDAS 5 represent the ‘‘senile’’ stages of aging, where the Cervidae (Westtangente Ulm), n = 136 (SMNS: unnum- occlusal surface of the dentition is heavily worn with the bered specimen) loss of functional structures, leading eventually to com- Caenomeryx filholi (Geimersheim), n = 442 (BSPG: promised nutrition. Thus, the IDAS system provides stages 1952II186-190, 1002, 1003, 1008, 1010–1014, 1026, 1028, based on natural transitions in the dentition that can be used 1030, 1038, 1040, 1041, 1043–1046, 1048, 1051–1053, to gain insight into extant and fossil individuals and pop- 1055, 1059–1064, 1067, 1068, 1070–1078, 1080–1083, ulations in terms of morphology, dental functionality, 1086, 1087, 1089, 1094, 1096–1107, 1110–1117, biology, and ecology. 1120–1123, 1125–1127, 1129–1140, 1142, 1143, 1145, 1147, 1148, 1151, 1152, 1154, 1155, 1157–1159, 1161, Acknowledgments Establishing the IDAS system is based on a 1164, 1165, 1167–1169, 1171, 1172, 1174–1176, long-term study of materials from many collections. The authors 1178–1185, 1187, 1194–1197, 1200–1209, 1211–1213, express our cordial thanks to the numerous curators who facilitated access to collections in their care. This research was supported by the 1215–1219, 1221, 1224–1226, 1228–1241, 1243, 1244, Deutsche Forschungsgemeinschaft [DFG, German Research Foun- 1246–1251, 1253–1255, 1257, 1259, 1260, 1261, 1263, dation (KOE 627/36-1)] and is publication no. 22 of the DFG 1264, 1266–1269, 1271, 1272, 1274–1284, 1286–1288, Research Unit 771 ‘‘Function and performance enhancement in the 1290, 1291, 1295–1298, 1300–1305, 1307, 1309–1344, mammalian dentition—phylogenetic and ontogenetic impact on the masticatory apparatus’’. We are indebted to Prof. Dr. Ray Bernor, 1346, 1347, 1351–1355, 1357, 1358, 1361, 1362, Washington, for access to the photo documentation of the Ho¨wenegg 1365–1378, 1381–1390, 1392–1394, 1398–1400, fauna, established by Dominik Wolf. Thanks to Georg Oleschinski 1404–1406, 1409–1412, 1414–1418, 1501–1505, 1508, (Bonn) for providing several of the photos. 1509, 1511–1516, 1518–1525, 1528–1530, 1532, 1535, 1536, 1538, 1539, 1547, 1549, 1550, 1555, 1570–1593, 1595–1609, 1611, 1613–1617, 1619–1621, 1623, 1627, Appendix 1 1628, 1630–1631, 1632, 1635, 1636, 1639, 1641, 1643, 1651–1653, 1656, 1658, 1661, 1666, 1668, 1670, 1673, BSPG = Bayerische Staatsammlung Palaöntologie und 1675, 1677, 1679, 1680, 1690, 1692, 1693, 1695–1697, historische Geologie Mu¨nchen, Germany 1699–1701, 1703–1707, 1709–1718, 1954) HI = Heimatmuseum Immendingen, Germany Cainotherium huerzeleri (Steinberg im Ries), n = 10 HLMD = Hessisches Landesmuseum Darmstadt, (BSPG : 1970XVIII6991, 6992, 6994, 6996, 6997, 7012, Germany 7016–7018, 7092) NHMB = Naturhistorisches Museum Basel, Switzerland Cainotherium sp. (Saulcet, Allier), n = 420 (NHMB: SMNK = Staatliches Museum fu¨r Naturkunde Karlsruhe, unnumbered specimen). Germany SMNS = Staatliches Museum fu¨r Naturkunde Stuttgart, Material used for the Ho¨wenegg sample Germany ZSHT = Zoologische Sammlung Histologie Tu¨bingen, Aceratherium sp. [HLMD: Hoe 56-7, Hoe 56–67 (HLMD Germany. 490), Hoe Rhino I-1953 (I/53), one individual unnumbered; SMNK: F/1954 / t-pli12 (F/54), Hoe 25/55] Hippotherium primigenium [HLMD: Hoe 58-V1 (V/58), Materials used for IDAS stages Hoe 58-V2 (V/58), Hoe 54 (III/53), Hoe 488 (E/55), Hoe 492 54-F4-G1, Hoe 493 y59-5 y220 (Y/59), Hoe M55-1 Histological serial sections (ZSHT) (M/55), Hoe 479, E54 (E/54), Hoe 29–58; HI: Hoe 740/58; SMNK: Hoe 07–60, Hoe A (A/54), Hoe C (C/54), Hoe Lagomorpha—Lepus europaeus, Oryctolagus cuniculus 158, Hoe B (B/54), RLB 8574] Rodentia—Petromus typicus, Octodon degus, Chinchilla Chalicotherium sp. (HLMD: one individual unnumbered) sp., Cavia porcellus (listed under C. cobaya), Mesocricetus Miotragocerus sp. [HI: Hoe W/58, Hoe 92, two individuals auratus, Peromyscus maniculatus, Micromys minutus. unnumbered; SMNK: Hoe D1-54 (D/54), Hoe S-56 (S/56), 123 Generalized individual dental age stages for fossil and extant placental mammals

Hoe 44–56, Hoe 100-59, Hoe 122, Hoe Q1955, Hoe U44, moschatus—Allen 1913; Ovis aries—Greenfield and four individuals unnumbered; SMNS: four individuals Arnold 2008; Moran and O’Connor 1994; Capra hircus— unnumbered] Greenfield and Arnold 2008; Gazella gazelle—Munro et al. Dorcatherium sp. (SMNK: H/54) 2009; Cervus elaphus—Azorit et al. 2002;Lowe1967; Muntiak (SMNK: Hoe K55). Cervus canadensis—Quimby and Gaab 1957; Dama dama—Chaplin and White 1969; Odocoileus hemionus— Thomas and Bandy 1975; Rees et al. 1966; Robinette et al. Appendix 2 1957; Odocoileus virginianus—Gee et al. 2002; Ryel et al. 1961; Severinghaus 1949; Rangifer tarandus—Bergerud Selected literature on the dentition age relationship 1970; Bromeé-Skuncke 1951; Loison et al. 2001; Miller for specific mammalian species 1972; Sus domesticus—Bivin and McClure 1976; Rhom- berg 1932; Weaver et al. 1966, 1969; Sus scrofa—Magnell General Asher and Lehmann 2008; Baumann 1949; and Carter 2007; Matschke 1967; Wittmann 2004. Habermehl 1975, 1985; van Nievelt and Smith 2005; Proboscidea Proboscideans—Louguet 2006; Loxodonta Slaughter et al. 1974; Smith 2000; Spinage 1973. africana—Sikes 1966, 1968; Mammuthus primigenius— Rodentia Hystrix africaeaustralis—Aarde 1985; Rattus Adam 1994. sp.—Nishijima et al. 2007; Castor canadensis—Nostrand and Stephenson 1964; Niviventer coxingi—Yu and Lin 1999; Peromyscus maniculatus—Layne 1968. References Chiroptera Pteropus sp.—Giannini et al. 2006. Elephas Scandentia Tupaia glis Adam, K.D. 1994. Anomalien des Zahnwechsels bei —Shigehara 1980. primigenius aus dem Quarta¨r des Oberrheins. Stuttgarter Beit- Carnivora Procyon lotor—Grau et al. 1970; Ursus ra¨ge zur Naturkunde Ser. B. 211: 1–36. Adams, L., and S.G. Watkins. 1967. Annuli in tooth cementum americanus—Marks and Erickson 1966; Rausch 1961; indicate age in California ground squirrels. Journal of Wildlife Vulpes vulpes—Bro¨mel and Zettl 1974; Geiger et al. 1977; Management 31(4): 836–839. Stubbe 1965; Canis familiaris—Cahill and Marks 1982; Allen, J.A. 1913. Ontogenetic and other variations in muskoxen, with Martes martes—Habermehl and Ro¨ttcher 1967; Mustela a systematic review of the muskox group, recent and extinct. Memoires American Museum Natural History, N.S. 1(4): putorius—Habermehl and Ro¨ttcher 1967; Popowics 1998; 103–226. Panthera pardus—Stander 1997; Crocuta crocuta—Van Anemone, R.L., E.S. Watts, and D.R. Swindler. 1991. Dental Horn et al. 2003; Meles meles—Stubbe 1965. development of known-age chimpanzees, Pan troglodytes (Pri- mates, Pongidae). American Journal of Physical Anthropology Primates Primates—Schultz 1935; Smith et al. 1994; 86: 229–241. Homo—Smith 1984, 1991, 1992; Homo sapiens—Dean Asher, R.J., and T. Lehmann. 2008. Dental eruption in afrotherian mammals. BMC Biology 6(14): 1–11. and Wood 1981; Donachie and Walls 1995, 1996; Gus- Azorit, C., M. Analla, R. Carrasco, J.A. Calvo, and J. Munoz-Cobo. tafson 1950; Lovejoy 1985; Marks and Schroeder 1996; 2002. Teeth eruption pattern in red deer (Cervus elaphus Miles 1963, 2001; Molnar 1971; Moorrees et al. 1963; hispanicus) in southern Spain. Anales de Biologia 24: 107–114. Nagao 1992; Schour and Massler 1941; Scott 1979; Stav- Baumann, D.F. 1949. Die freilebenden Saügetiere der Schweiz. Bern: Pan troglodytes Verlag Hans Huber. rianos et al. 2008; Walker et al. 1991; — Bergerud, A.T. 1970. Eruption of permanent premolars and molars for Anemone et al. 1991; Dean and Wood 1981; Nissen and Newfoundland caribou. Journal of Wildlife Management 34(4): Riesen 1964; Smith et al. 2007; Welsch 1967; Gorilla 962–963. gorilla—Dean and Wood 1981; Kelley and Schwartz 2010; Bernor, L.B., H. Tobien, L.C. Hayek, and H. Mittmann. 1997. Hippotherium primigenium Pongo pygmaeus (Equidae, Mammalia) from the late Welsch 1967; —Dean and Wood 1981; Miocene of Ho¨wenegg. Andrias 10: 1–230. Kelley and Schwartz 2010 ; Welsch 1967; Macaca irus— Bivin, W.S., and R.C. McClure. 1976. Deciduous tooth chronology in Bowen and Koch 1970; Saguinus nigricollis—Chase and the mandible of the domestic pig. Journal of Dental Research Cooper 1969. 55(4): 591–597. Bodkin, J.L., J.A. Ames, R.J. Jameson, A.M. Johnson, and G.M. Perissodactyla Equus zebra—Penzhorn 1982; Equus Matson. 1997. Estimating age of sea otters with cementum layers caballus—Possmann Dias 2005; Equus burchelli—Spin- in the first premolar. Journal of Wildlife Management 61(3): 967–973. eage 1972; Rhinocerotidae—Louguet 2006; Diceros Boule, M. 1921. Les hommes fossiles–e´le´ments de palaeóntologie bicornis—Goddard 1970; Hitchins 1978. humaine. Paris: Masson et Cie. Bowen, W.H., and G. Koch. 1970. Determination of age in monkeys Artiodactyla Bison bison—Frison et al. 1976; Fuller (Macaca irius) on the basis of dental development. Laboratory 1959; Capra ibex—Ratti and Habermehl 1977; Ovibos Animals 4: 113–123.

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123 Pala¨ontol Z DOI 10.1007/s12542-011-0101-5

ERRATUM

Erratum to: Generalized individual dental age stages for fossil and extant placental mammals

Ulrike Anders • Wighart von Koenigswald • Irina Ruf • B. Holly Smith

Ó Springer-Verlag 2011

Erratum to: Pala¨ontol Z DOI 10.1007/s12542-011-0098-9

During processing of this article, inappropriate changes were made to Table 1 that rendered its content incompre- hensible. The correct version of the table is given here.

Table 1 Correlation of the IDAS Common Schultz Knußmann Grau 1970 Goddard 1970 IDAS stages to age use determinations of different (primates) 1988 (racoons) (rhinoceros) species to illustrate the but rarely defined (humans) transferability of the IDAS 1935 1960 system 0 prenatal fetus 1 infantile infans I, II class I-VI juvenile young 2 juvenile juvenis class VII-XI 3 class I-III class XII-XVI adultus/ adult adult 4 adult matures class IV class XVII-XVIII 5 senile old senilis class V class XIX-XX

The online version of the original article can be found under doi:10.1007/s12542-011-0098-9.

U. Anders (&) Á W. von Koenigswald Á I. Ruf Steinmann-Institut fu¨r Geologie, Mineralogie und Pala¨ontologie, Rheinische Friedrich-Wilhelms-Universita¨t Bonn, Nussallee 8, 53115 Bonn, Germany e-mail: [email protected]

B. H. Smith Museum of Anthropology, The University of Michigan, Ann Arbor, MI 48109-1107, USA 123

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