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Longevity and Life History of Cave Bears – a Review and Novel Data from Tooth Cementum and Relative Emergence of Permanent Dentition See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/323284525 Longevity and life history of cave bears – a review and novel data from tooth cementum and relative emergence of permanent dentition Article in Historical Biology · February 2018 DOI: 10.1080/08912963.2018.1441293 CITATIONS READS 13 615 4 authors, including: Christian Kolb Eli Amson Städtisches Naturkundliches Museum Göppingen State Museum of Natural History Stuttgart 14 PUBLICATIONS 278 CITATIONS 87 PUBLICATIONS 778 CITATIONS SEE PROFILE SEE PROFILE Marcelo R Sánchez-Villagra University of Zurich 374 PUBLICATIONS 7,264 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Convergent evolution of humeral and femoral functional morphology in slow arboreal mammals View project First Evidence of Convergent Lifestyle Signal in Reptile Skull Roof Microanatomy View project All content following this page was uploaded by Marcelo R Sánchez-Villagra on 22 February 2018. The user has requested enhancement of the downloaded file. HISTORICAL BIOLOGY, 2018 https://doi.org/10.1080/08912963.2018.1441293 Longevity and life history of cave bears – a review and novel data from tooth cementum and relative emergence of permanent dentition Kristof Veitscheggera,b , Christian Kolba, Eli Amsonc,d,e and Marcelo R. Sánchez-Villagraa aPaläontologisches Institut und Museum, Universität Zürich, Zürich, Switzerland; bNaturalis Biodiversity Center, Leiden, The Netherlands; cAG Morphologie und Formengeschichte, Institut für Biologie, Humboldt Universität, Berlin, Germany; dBild Wissen Gestaltung. Ein interdisziplinäres Labor, Humboldt Universität, Berlin, Germany; eMuseum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany ABSTRACT ARTICLE HISTORY Longevity and other life history variables are key to understanding evolutionary processes and the biology Received 6 December 2017 of extinct animals. For the past 20 years, the lifespan of cave bears received an increased interest. Studies Accepted 13 February 2018 focusing on incremental lines of tooth cementum resulted in detailed mortality patterns from different KEYWORDS localities. In this review, we summarise literature on age estimation as well as mortality of different Incremental lines; age European cave bear localities and present novel data on longevity from 94 teeth originating from 20 estimation; Schultz’s rule; European localities. Additionally, the relative tooth emergence pattern of the permanent dentition is heterochrony; Ursus spelaeus investigated under the Schultz’s rule framework of possible life history implications. For this, the known sequences of extant bear species are compared with the one of cave bears. Our results suggest that the typical duration of the life of cave bears was 19 years but data from literature show that in rare cases ages of up to 30–32 years were achieved. Additionally, we present the oldest known age for the Middle Pleistocene cave bear Ursus deningeri, 29 years. The tooth eruption pattern of cave bears exhibits a heterochronic shift that implies, under the assumption of Schulz’ rule, a slightly faster life history than closely related species. Cave bears as a study object for exploring questions questions of growth and life history evolution in the fossil about life history evolution record (Ehrenberg 1931; Kurtén 1958; Debeljak 1996a; Fosse and Crégut-Bonnoure 2014; Veitschegger 2017a, 2017b). Despite Exploring the biology and life history of extinct animals is a their close relationship to brown and polar bears (Noonan et crucial part to understand evolution and extinction in the fossil al. 2005; Bon et al. 2008; Krause et al. 2008; Knapp et al. 2009), record. Cave bears, crown group members of Ursidae (Noonan cave bears exhibited unique adaptations, ecologically clearly dis- et al. 2005; Bon et al. 2008; Krause et al. 2008; Knapp et al. tinguishing their niche of that of brown bears, with which they 2009), are abundantly recovered in Eurasian sediments from shared their habitat (Fortes et al. 2016). Additionally, their skull the Late Pleistocene (Rabeder et al. 2000). They went extinct growth trajectory as well as size increase differs clearly from that close to the end of the Pleistocene, around 27.800 -24.300 cal. of brown bears (Fosse and Crégut-Bonnoure 2014; Fuchs et al. years BP (Pacher and Stuart 2009; Baca et al. 2016), sharing the 2015). Two prominent characteristics of cave bears are their big fate of many other representatives of the last ice age megafauna body size (Christiansen 1999; Rabeder et al. 2000; Veitschegger (Barnosky et al. 2004). Cave bears were dependent on caves to 2017a) and adaptations to herbivorous diet (Bocherens 2015; survive the winters as well as to give birth to their offspring and Naito et al. 2016). However, even though herbivory is the most exhibited homing behaviour (Fortes et al. 2016). Thus, if death accepted hypothesis concerning the feeding ecology of cave bears occurred, their remains were located in an ideal setting for fossil (e.g. Rabeder et al. 2000; van Heteren et al. 2014; Bocherens 2015; preservation because of the less disturbed conditions in caves Naito et al. 2016), some studies suggest a more varied diet for (Rabeder et al. 2000). Consequently, many collections all over this species (Richards et al. 2008; Figueirido et al. 2009; Peigné Eurasia house teeth, skulls, and postcranial bones of cave bears et al. 2009; Robu et al. 2017). Here, we aim to summarise infor- of all different ontogenetic stages, even neonate individuals mation on cave bear longevity and life history as well as present (e.g. Ehrenberg 1931, 1964, 1973; Kurtén 1958; Debeljak 1996a; novel data, based on tooth cementum lines. We give an overview Rabeder et al. 2000; Tsoukala et al. 2006). This abundance, in of the current state of research on the lifespan of cave bears in addition to our knowledge of the phylogenetic position of cave the context of its extant relatives and with remarks to the fossil bears (Noonan et al. 2005; Bon et al. 2008; Krause et al. 2008; record. Additionally, we investigate tooth eruption sequences of Knapp et al. 2009), makes them an ideal subject for exploring cave bears and closely related species for life history implications. CONTACT Kristof Veitschegger [email protected] Supplemental data for this article can be accessed https://doi.org/10.1080/08912963.2018.1441293 © 2018 Informa UK Limited, trading as Taylor & Francis Group Published online 19 Feb 2018 .K. VEITSCHEGGER ET AL 2 Life history and longevity Owing to the ideal preservational conditions in caves and the abundance of fossil material, this method is also widely applied on The duration of the life of an organism until death, longev- cave bears (Debeljak 1996b, 2004, 2007, 2011, 2014; Torres et al. ity, is a fundamental aspect of evolution. A species’ lifespan is 2007; Holland 2013) and can even provide insight into the season associated with body mass (e.g. Speakman 2005; Healy et al. of death of these animals due to the different rates of cementum 2014) and shows correlations with life history traits (e.g. Rollo deposition in seasonal environments (Debeljak 2011, 2014). Thus, 2002; Metcalfe and Monaghan 2003; de Magalhães et al. 2007). the maximum longevity and even complete mortality curves are Nonetheless, there is a considerable amount of variation in lon- known for several localities (e.g. Debeljak 2004, 2007, 2011, 2014; gevity among organisms of comparable body masses (Healy et Torres et al. 2007; Holland 2013). To establish the individual age al. 2014). Longevity as a trait is not independent from phylog- based on cementum incremental lines the amount of lines is added eny, thus closer related species often exhibit similar lifespans (de to the age of the eruption of the respective tooth (Rausch 1969; Magalhães et al. 2007; Healy et al. 2014). Most bear species can Kaur et al. 2015). Additionally, in cave bears, it was proposed to live longer than 20 years and in zoos record ages of over 40 have start counting at the boundary between cementum and dentine in been reported (de Magalhães and Costa 2009; Hunter 2011). the lower first molar because of the difficulty in recognising the first However, it remains somewhat difficult to assess the longevity incremental line (Debeljak 2011; Holland 2013). Rausch (1969) in different ursid species. Even though lifespan is known for identified similar difficulties in canines of brown bears. In bears, all extant bear species, data often originate from animals that the first premolar and first molar are the most informative teeth lived and died in zoos and thus reflects more a possible maxi- as they appear early in ontogeny, usually within the first half year mum lifespan under protected conditions rather than life expec- after birth (Dittrich 1960; Marks and Erickson 1966). The lower tancy in the wild (de Magalhães and Costa 2009; Hunter 2011). first molar erupts in brown bears between four and five months and Additionally, in modern times, human intervention often leads to reaches its final position at an age of around 5.5 months (Dittrich death of older individuals, which have not reached their potential 1960). In polar bears eruption of m1 occurs slightly later. The onset life expectancy (Krofel et al. 2012; Zedrosser et al. 2013). Bears of eruption is around the 5th month and it is still erupting at an lack adaptation such as eusociality possibly extending lifespan age of 5.5 months (Dittrich 1960). American black bears have a (Williams and Shattuck 2015) but it was proposed that hiberna- longer documented period of eruption with the onset of lower first tion (or dormancy in the case of bears) might aid in achieving molar emergence occuring around 5.5 months and it reaches its longer lifespans (Wu and Storey 2016). final position at the beginning of the seventh month (Marks and Erickson 1966). However, in all species with available data, the first Tooth cementum and longevity in cave bears – molar is already in place when cement deposition should decrease background due to winter conditions (Debeljak 2011).
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