Publication Cover
Historical Biology
An International Journal of Paleobiology
Volume 33, 2021 - Issue 5
334
Views
7
CrossRef citations to date
0
Altmetric
Articles

The life history of European Middle Pleistocene equids: first insights from bone histology

ORCID Icon &
Pages 672-682 | Received 11 Jun 2019, Accepted 08 Aug 2019, Published online: 19 Aug 2019

References

  • Adam KD. 1954. Die mittelpleistozänen Faunen von Steinheim an der Murr (Württemberg). Quaternaria. 1:131–144.
  • Alberdi MT, Bonadonna FP. 1988. Equidae (Perissodactyla, Mammalia): extinctions subsequent to the climatic changes. Rev Española Paleontol. 3:39–43.
  • Alberdi MT, Ortiz-Jaureguizar E, Prado JL. 1998. A quantitative review of European stenonoid horses. J Paleontol. 72(2):371–387. doi:10.1017/S0022336000036350.
  • Alberdi MT, Prado JL, Ortiz-Jaureguizar E. 1995. Patterns of body size changes in fossil and living Equini (Perissodactyla). Biol J Linn Soc. 54:349–370.
  • Amprino R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement. Arch Biol. 58:315–330.
  • Amson E, Kolb C, Scheyer TM, Sánchez-Villagra MR. 2015. Growth and life history of Middle Miocene deer (Mammalia, Cervidae) based on bone histology. Comptes Rendus - Palevol. 14(8):637–645. doi:10.1016/j.crpv.2015.07.001.
  • Azzaroli A. 1983. Quaternary mammals and the “end-Villafranchian” dispersal event - A turning point in the history of Eurasia. Palaeogeogr Palaeoclimatol Palaeoecol. 44(1–2):117–139. doi:10.1016/0031-0182(83)90008-1.
  • Azzaroli A. 1992. Ascent and decline of monodactyl equids: a case for prehistoric overkill. Ann Zool Fennici. 28:151–163.
  • Blueweiss L, Fox H, Kudzma V, Nakashima D, Peters R, Sams S. 1978. Relationships between body size and some life history parameters. Oecologia. 37:257–272.
  • Bybee PJ, Lee AH, Lamm E-T. 2006. Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. J Morphol. 267:347–359. doi:10.1002/jmor.
  • Calder WAI. 1984. Size, function and life history. New York (NY): Dover Publications.
  • Calderón T, DeMiguel D, Arnold W, Stalder G, Köhler M. 2019. Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer. J Anat Online Ver. doi:10.1111/joa.13016.
  • Cantalapiedra JL, Prado JL, Hernández Fernández M, Alberdi MT. 2017. Decoupled ecomorphological evolution and diversification in Neogene-Quaternary horses. Science. 355(6325):627–630. doi:10.1126/science.aag1772.
  • Castanet J, Francillon-Vieillot H, Meunier F, de Ricqlès A. 1993. Bone and individual aging. In: Hall BK, editor. Bone: a Treatise. Vol. 7. Boca Raton: CRC Press; p. 245–283.
  • Castanet J. 2006. Time recording in bone microstructures of endothermic animals; functional relationships. Comptes Rendus - Palevol. 5(3–4):629–636. doi:10.1016/j.crpv.2005.10.006.
  • Castanet J, Croci S, Aujard F, Perret M, Cubo J, de Margerie E. 2004. Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J Zool. 263(1):31–39. doi:10.1017/S0952836904004844.
  • Chinsamy-Turan A. 2005. The microstructure of dinosaur bone. Deciphering biology with fine-scale techniques. Baltimore and London: The Johns Hopkins University Press.
  • Churcher C. 1993. Equus grevyi. Mamm Species. 453:1–9.
  • Cubo J, le Roy N, Martinez-Maza C, Montes L. 2012. Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology. 38(2):335–349. doi:10.5061/dryad.j2m25n82.
  • Damuth J. 1981. Population density and body size in mammals. Nature. 290:699–700.
  • Damuth J, MacFadden BJ. 1990. Body size in mammalian Paleobiology. Estimations and biological implications. Cambridge: Cambridge University Press.
  • de Margerie E, Cubo J, Castanet J. 2002. Bone typology and growth rate: testing and quantifying “Amprino’s rule” in the mallard (Anas platyrhynchos). Comptes Rendus - Biol. 325(3):221–230. doi:10.1016/S1631-0691(02)01429-4.
  • Eisenberg JF. 1990. The behavioral/ecological significance of body size in the Mammalia. In: Damuth J, MacFadden BJ, editors. Body size in mammalian Paleobiology. Estimations and biological implications. Cambridge: Cambridge University Press; p. 25–37.
  • Eisenmann V. 1979. Les métapodes d’Equus sensu lato (Mammalia, Périssodactyla). Geobios. 12(6):863–886. doi:10.1016/S0016-6995(79)80004-2.
  • Eisenmann V, Alberdi MT, de Giuli C, Staesche U. 1988. Studying fossil horses. Collected papers after the “New York international hipparion conference, 1981”. In: Woodburne M, Sondaar P, editors. Volume I: methodology. Leiden: E.J. Brill; p. 1 - 72.
  • Eisenmann V. 1991. Les chevaux quaternaires européens (Mammalia, Perissodactyla). Taille, typologie, biostratigraphie et taxonomie. Geobios. 24(6):747–759.
  • Erickson GM. 2005. Assessing dinosaur growth patterns: A microscopic revolution. Trends Ecol Evol. 20(12):677–684. doi:10.1016/j.tree.2005.08.012.
  • Erickson GM, Rogers KC, Yerby SA. 2001. Dinosaurian growth patterns and rapid avian growth rates. Nature. 412(6845):429–433. doi:10.1038/35086558.
  • Ernest SKM. 2003. Life history characteristics of placental nonvolant mammals. Ecology. 84(12):3402. doi:10.1890/11-1341.1.
  • Feh C, Munkhtuya B, Enkhbold S, Sukhbaatar T. 2001. Ecology and social structure of the Gobi khulan Equus hemionus subsp. in the Gobi B National Park, Mongolia. Biol Conserv. 101:51–61.
  • Forsten A. 1988. The small caballoid horse of the upper Pleistocene and Holocene. J Anim Breed Genet. 105(1–6):161–176. doi:10.1111/j.1439-0388.1988.tb00288.x.
  • Forsten A. 1991a. Size trends in Holarctic anchitherines (Mammalia, Equidae). J Paleontol. 65(1):147–159.
  • Forsten A. 1991b. Size decrease in Pleistocene-Holocene true or caballoid horses of Europe. Mammalia. 55(3):407–420. doi:10.1515/mamm.1991.55.3.407.
  • Forsten A. 1999. The horses (genus Equus) from the Middle Pleistocene of Steinheim, Germany. In: Haynes G, Klimowicz J, Reumer JWF, editors. Mammoths and the Mammoth fauna: studies of an extinct ecosystem. Vol. Deinsea 6. Rotterdam: Natural History Museum Rotterdam. p. 147–154.
  • Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY, Zylberberg L, de Ricqlès A. 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG, editor. Skeletal biomineralization: patterns, processes and evolutionary trends. New York (NY): Van Nostrand Reinhold; p. 471–530.
  • García-Martínez R, Marín-Moratalla N, Jordana X, Köhler M. 2011. The ontogeny of bone growth in two species of dormice: reconstructing life history traits. Comptes Rendus - Palevol. 10(5–6):489–498. doi:10.1016/j.crpv.2011.03.011.
  • Gosling LM, Muntifering J, Kolberg H, Uiseb K, King SRB. 2019. Equus zebra. IUCN Red List of Threat Species. 2019:p. e.T7960A45171906. http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T7960A45171906.en
  • Grubb P. 1981. Equus burchelli. Mamm Species. 157:1–9.
  • Guthrie RD. 2003. Rapid body size decline in Alaskan Pleistocene horses before extinction. Nature. 426(6963):169–171. doi:10.1038/nature02098.
  • Horner JR, de Ricqlès A, Padian K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology. 25(3):295–304. doi:10.1666/0094-8373(1999)025<0295:VIDSII>2.3.CO;2.
  • Huttenlocker AK, Woodward HN, Hall BK. 2013. The biology of bone. In: Padian K, Lamm E-T, editors. Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. Berkeley: University of California Press; p. 13–34.
  • Janis C. 2007. The horse series. In: Regal B, editor. Icons of Evolution. Westport: Greenwood Press; p. 251–280.
  • Jordana X, Marín-Moratalla N, Moncunill-Solé B, Nacarino-Meneses C, Köhler M. 2016. Ontogenetic changes in the histological features of zonal bone tissue of ruminants: a quantitative approach. Comptes Rendus - Palevol. 15(1–2):255–266. doi:10.1016/j.crpv.2015.03.008.
  • Kaczensky P, Lkhagvasuren B, Pereladova O, Hemami M, Bouskila A. 2015. Equus hemionus. IUCN Red List Threat Species; p. e.T7951A45. http://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T7951A45171204.en
  • Kahlke HD. 1975. The Macro-faunas of continental Europe during the Middle Pleistocene: stratigraphic sequence and problems of intercorrelation. In: Butzer KW, Isaac GL, editors. After the australopithecines. Stratigraphy, ecology, and culture change in the Middle Pleistocene. The Hague: Mouton Publishers; p. 309–374.
  • Kahlke RD, García N, Kostopoulos DS, Lacombat F, Lister AM, Mazza PPA, Spassov N, Titov VV. 2011. Western Palaearctic palaeoenvironmental conditions during the early and early Middle Pleistocene inferred from large mammal communities, and implications for hominin dispersal in Europe. Quat Sci Rev. 30(11–12):1368–1395. doi:10.1016/j.quascirev.2010.07.020.
  • Kahlke VH-D. 1961. Revision der Säugetierfaunen der klassischen deutschen Pleistozän-Fundstellen von Süßenborn, Mosbach und Taubach. Geologie. 10:493–532.
  • King SRB, Moehlman PD. 2016. Equus quagga. IUCN Red List Threat Species; p. e.T41013A45172424. http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T41013A45172424.en
  • Kleiber M. 1932. Body size and metabolism. Hilgardia. 6(11):315–353. doi:10.1017/CBO9781107415324.004.
  • Koenigswald WV, Smith BH, Keller T. 2007. Supernumerary teeth in a subadult rhino mandible (Stephanorhinus hundsheirnensis) from the middle Pleistocene of Mosbach in Wiesbaden (Germany). Paläontolog Z. 81:416–428.
  • Köhler M. 2010. Fast or slow? The evolution of life history traits associated with insular dwarfing. In: Pérez-Mellado V, Ramon C, editors. Islands and Evolution. Vol. 19. Maó: Institut Menorquí d’Estudis. Recerca; p. 261–280.
  • Köhler M, Marín-Moratalla N, Jordana X, Aanes R. 2012. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature. 487:358–361. doi:10.1038/nature11264.
  • Köhler M, Moyà-Solà S. 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc Natl Acad Sci USA. 106(48):20354–20358. doi:10.1073/pnas.0813385106.
  • Kolb C, Scheyer TM, Veischegger K, Van Den Hoek Ostende LW, Hayashi S, Sánchez-Villagra MR. 2015. Mammalian bone palaeohistology: a survey and new data with emphasis on island forms. Peer J. 3:e1358. doi:10.7717/peerj.1358.
  • Lamm E-T. 2013. Preparation and sectioning of specimens. In: Padian K, Lamm E-T, editors. Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. Berkeley: University of California Press; p. 55–160.
  • Lee AH, Huttenlocker AK, Padian K, Woodward HN. 2013. Analysis of growth rates. In: Padian K, Lamm E-T, editors. Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. Berkeley: University of California Press; p. 217–251.
  • Lindsay EH, Opdyke ND, Johnson NM. 1980. Pliocene dispersal of the horse Equus and late Cenozoic mammalian dispersal events. Nature. 287(5778):135–138. doi:10.1038/287135a0.
  • MacFadden BJ. 1986. Fossil horses from “Eohippus” (Hyracotherium) to Equus: scaling, Cope’s Law, and the evolution of body size. Paleobiology. 12(4):355–369. doi:10.1017/S0094837300003109.
  • MacFadden BJ. 1992. Fossil horses. Systematics, paleobiology, and evolution of the family Equidae. Cambridge: Cambridge University Press.
  • MacFadden BJ. 2005. Fossil horses - evidence for evolution. Science. 307:1728–1730. . doi:10.1126/science.1105458.
  • Marín-Moratalla N, Jordana X, García-Martínez R, Köhler M. 2011. Tracing the evolution of fitness components in fossil bovids under different selective regimes. Comptes Rendus - Palevol. 10(5–6):469–478. doi:10.1016/j.crpv.2011.03.007.
  • Marín-Moratalla N, Jordana X, Köhler M. 2013. Bone histology as an approach to providing data on certain key life history traits in mammals: implications for conservation biology. Mamm Biol. 78(6):422–429. doi:10.1016/j.mambio.2013.07.079.
  • Martínez-Maza C, Alberdi MT, Nieto-Diaz M, Prado JL. 2014. Life-history traits of the miocene Hipparion concudense (Spain) inferred from bone histological structure. PLoS One. 9(8):e103708. doi:10.1371/journal.pone.0103708.
  • Maul LC, Rekovets L, Heinrich W-D, Keller T, Storch G. 2000. Arvicola mosbachensis (Schmidtgen 1991) of Mosbach 2: a basic sample for the early evolution of the genus and a reference for further biostratigraphical studies. Senckenbergiana Lethaea. 80:129–147.
  • McHorse BK, Biewener AA, Pierce SE. 2017. Mechanics of evolutionary digit reduction in fossil horses (Equidae). Proc R Soc B Biol Sci. 284(1861):20171174. doi:10.1098/rspb.2017.1174.
  • McNab BK. 1990. The physiological significance of body size. In: Damuth J, MacFadden BJ, editors. Body size in mammalian Paleobiology. Estimations and biological implications. Cambridge: Cambridge University Press; p. 11–23.
  • Moehlman PD, Rubenstein DI, Kebede F. 2013. Equus grevyi. IUCN Red List Threat Species; p. e.T7950A21070406. doi:10.2305/IUCN.UK.2013-1.RLTS.T7950A21070406.en.
  • Moncunill-Solé B, Orlandi-Oliveras G, Jordana X, Rook L, Köhler M. 2016. First approach of the life history of Prolagus apricenicus (Ochotonidae, Lagomorpha) from Terre Rosse sites (Gargano, Italy) using body mass estimation and paleohistological analysis. Comptes Rendus - Palevol. 15(1–2):227–237. doi:10.1016/j.crpv.2015.04.004.
  • Nacarino-Meneses C, Jordana X, Köhler M. 2016a. Histological variability in the limb bones of the Asiatic wild ass and its significance for life history inferences. Peer J. 4(10):e2580. doi:10.7717/peerj.2580.
  • Nacarino-Meneses C, Jordana X, Köhler M. 2016b. First approach to bone histology and skeletochronology of Equus hemionus. Comptes Rendus - Palevol. 15(1–2):267–277. doi: 10.1016/j.crpv.2015.02.005.
  • Nacarino-Meneses C, Köhler M. 2018. Limb bone histology records birth in mammals. PLoS One. 13(6):e0198511.
  • Nitychoruk J, Bińka K, Hoefs J, Ruppert H, Schneider J. 2005. Climate reconstruction for the Holsteinian interglacial in Eastern Poland and its comparison with isotopic data from marine isotope stage 11. Quat Sci Rev. 24(5–6):631–644. doi:10.1016/j.quascirev.2004.07.023.
  • Nowak RM. 1999. Walker’s mammals of the world. Baltimore and London: The Johns Hopkins University Press.
  • Orlandi-Oliveras G, Jordana X, Moncunill-Solé B, Köhler M. 2016. Bone histology of the giant fossil dormouse Hypnomys onicensis (Gliridae, Rodentia) from Balearic Islands. Comptes Rendus - Palevol. 15(1–2):238–244. doi:10.1016/j.crpv.2015.05.001.
  • Orlandi-Oliveras G, Nacarino-Meneses C, Koufos GD, Köhler M. 2018. Bone histology provides insights into the life history mechanisms underlying dwarfing in hipparionins. Sci Rep. 8(1):17203. doi:10.1038/s41598-018-35347-x.
  • Orlando L. 2015. Equids. Curr Biol. 25:R973–R978. doi:10.1016/j.cub.2015.09.005.
  • Ortiz-Jaureguizar E, Alberdi MT. 2003. The pattern of body mass changes in the Hipparionini (Perissodactyla, Equidae) of the Iberian Peninsula during the Upper Miocene-Upper Pliocene. Coloquios Paleontol. 1:499–509.
  • Padian K, de Ricqlès A, Horner JR. 2001. Dinosaurian growth rates and bird origins. Nature. 412(6845):405–408. doi:10.1038/35086500.
  • Palkovacs EP. 2003. Explaining adaptive shifts in body size on islands: a life history approach. Oikos. 103(1):37–44. doi:10.1034/j.1600-0706.2003.12502.x.
  • Penzhorn BL. 1988. Equus zebra. Mamm Species. 314:1–7.
  • Peters RH. 1983. The ecological implications of body size. Cambridge: Cambridge University Press.
  • Pushkina D, Bocherens H, Ziegler R. 2014. Unexpected palaeoecological features of the Middle and Late Pleistocene large herbivores in southwestern Germany revealed by stable isotopic abundances in tooth enamel. Quat Int. 339–340:164–178. doi:10.1016/j.quaint.2013.12.033.
  • Roff DA. 1992. The evolution of life histories. Theory and analysis. New York: Chapman and Hall.
  • Roff DA. 2002. Life history evolution. Sunderland: Sinauer Associates.
  • Rubenstein D, Low Mackey B, Davidson Z, Kebede F, King SR. 2016. Equus grevyi. IUCN Red List Threat Species; p. e.T7950A89624491. http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T7950A89624491.en
  • Saarinen J, Eronen J, Fortelius M, Seppä H, Lister AM. 2016. Patterns of diet and body mass of large ungulates from the Pleistocene of Western Europe, and their relation to vegetation. Palaeontol Electron. 19(3):1–58.
  • Schöpke K, Stubbe A, Stubbe M, Batsaikhan N, Schafberg R. 2012. Morphology and variation of the Asiatic wild ass (Equus hemionus hemionus). Erforsch Biol Ressourcen Mongolei. 12:77–84.
  • Schulz E, Kaiser TM. 2013. Historical distribution, habitat requirements and feeding ecology of the genus Equus (Perissodactyla). Mamm Rev. 43(2):111–123. doi:10.1111/j.1365-2907.2012.00210.x.
  • Shoemaker L, Clauset A. 2014. Body mass evolution and diversification within horses (family Equidae). Ecol Lett. 17(2):211–220. doi:10.1111/ele.12221.
  • Silver IA. 1963. The aging of domestic animals. In: Brothwell D, Higgs E, editors. Science in Archaeology: a comprehensive survey of progress and research. New York: Basic Books; p. 250–268.
  • Simpson GG. 1953. The major features of evolution. New York: Columbia University Press.
  • Stanley SM. 1973. An explanation for Cope’s rule. Evolution (N Y). 27:1–26.
  • Stearns SC. 1992. The evolution of life histories. New York: Oxford University Press.
  • Stearns SC. 2000. Life history evolution: successes, limitations, and prospects. Naturwissenschaften. 87. 476–486.
  • Strömberg CAE. 2006. Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology. 32(2):236–258.
  • Turner-Walker G, Mays S. 2008. Histological studies on ancient bone. In: Pinhasi R, Mays S, editors. Advances in human paleopathology. Chichester: John Wiley & Sons, Ltd; p. 121–146.
  • Van Asperen EN. 2013. Position of the Steinheim interglacial sequence within the marine oxygen isotope record based on mammal biostratigraphy. Quat Int. 292:33–42. doi:10.1016/j.quaint.2012.10.045.
  • Western D. 1979. Size, life history and ecology in mammals. Afr J Ecol. 17(4):185–204. doi:10.1111/j.1365-2028.1979.tb00256.x.
  • Woodward HN, Padian K, Lee AH. 2013. Skeletochronology. In: Padian K, Lamm E-T, editors. Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. Berkeley: University of California Press; p. 195–215.
  • Woodward HN, Freedman Fowler EA, Farlow JO, Horner JR. 2015. Maiasaura, a model organism for extinct vertebrate population biology: a large sample statistical assessment of growth dynamics and survivorship. Paleobiology. 41(4):503–527. doi:10.1017/pab.2015.19.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.