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Bone histology, palaeobiology, and early diagenetic history of extinct equids from Turkey

Published online by Cambridge University Press:  06 November 2020

Carmen Nacarino-Meneses Open the ORCID record for Carmen Nacarino-Meneses [Opens in a new window] ,
Anusuya Chinsamy Open the ORCID record for Anusuya Chinsamy [Opens in a new window] ,
Serdar Mayda Open the ORCID record for Serdar Mayda [Opens in a new window] ,
Tanju Kaya Open the ORCID record for Tanju Kaya [Opens in a new window]  and
Ugur Cengiz Erismis
Carmen Nacarino-Meneses*
Affiliation:
University of Cape Town, Department of Biological Sciences, Private Bag X3, Rhodes Gift, Cape Town, 7700South Africa
Anusuya Chinsamy
Affiliation:
University of Cape Town, Department of Biological Sciences, Private Bag X3, Rhodes Gift, Cape Town, 7700South Africa
Serdar Mayda
Affiliation:
Ege University, Faculty of Science, Biology Department, Bornova, Izmir, 35100Turkey Ege University, Natural History Museum, Bornova, Izmir, 35100Turkey
Tanju Kaya
Affiliation:
Ege University, Natural History Museum, Bornova, Izmir, 35100Turkey
Ugur Cengiz Erismis
Affiliation:
Afyon Kocatepe University, Faculty of Science and Literature, Molecular Biology and Genetics Department, Afyonkarahisar, 03200Turkey
*
*Corresponding author at: E-mail address: [email protected] (C. Nacarino-Meneses).
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Abstract

Bone histology has proved to be a valuable tool to obtain information about the palaeobiology and early taphonomic history of fossil vertebrates. However, there are still many extinct taxa for which bone histology studies could be applied to deduce information about their life history and early diagenetic changes. Here, we partially fill this gap by studying bone microstructure and bone micropreservation in the third metapodia of Hipparion and Equus recovered from several Miocene, Pliocene, and Pleistocene localities in Turkey. Our histological analysis reveals that most of the bone cortices under study are composed of a well-vascularized fibrolamellar bone. Furthermore, we record the presence of compact coarse cancellous bone in a Hipparion metatarsal. In terms of histological preservation, our findings provide supporting evidence that differences in moisture, oxygen, and/or temperature during fossilisation at the different localities impacted the quality of bone preservation. Bacterial bioerosion was extensive in the samples, and we also identified a specific tunnelling morphology that we tentatively consider to be damage caused by freshwater algae. The present study provides novel insight into the palaeobiology and early diagenetic history of extinct horses from Turkey and sets the stage for further research in this area.

Keywords

EquidaeBone histologyPalaeobiologySkeletochronologyBioerosionDiagenesis
Type
Research Article
Information
Quaternary Research , Volume 100 , March 2021 , pp. 240 - 259
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Copyright
Copyright © University of Washington. Published by Cambridge University Press, 2020

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References

REFERENCES

Akgün, F., Kayseri, M.S., Akkiraz, M.S., 2007. Palaeoclimatic evolution and vegetational changes during the Late Oligocene-Miocene period in Western and Central Anatolia (Turkey). Palaeogeography, Palaeoclimatology, Palaeoecology 253, 56–90.CrossRefGoogle Scholar
Akkiraz, M.S., Akgün, F., Utescher, T., Bruch, A.A., Mosbrugger, V., 2011. Precipitation gradients during the Miocene in Western and Central Turkey as quantified from pollen data. Palaeogeography, Palaeoclimatology, Palaeoecology 304, 276–290.CrossRefGoogle Scholar
Alberdi, M.T., 1989. A review of Old World hipparionine horses. In: Prothero, D.R., Schoch, R. (Eds.), The Evolution of Perissodactyls. Oxford University Press, New York, pp. 234–261.Google Scholar
Alberdi, M.T., Bonadonna, F.P., 1988. Equidae (Perissodactyla, Mammalia): extinctions subsequent to the climatic changes. Revista Española de Paleontologia 3, 39–43.Google Scholar
Alberdi, M.T., Cerdeño, E., 2003. Sistemática y distribución de los perisodáctilos del Neógeno y Cuaternario. In: Jiménez Fuentes, E., Civis Llovera, J. (Eds.), Los Vertebrados Fósiles En La Historia de La Vida. Excavación, Estudio y Patrimonio. Aquilafuente, Ediciones Universidad de Salamanca, Salamanca, pp. 237–279.Google Scholar
Alberdi, M.T., Ortiz-Jaureguizar, E., Prado, J.L., 1998. A quantitative review of European stenonoid horses. Journal of Paleontology 72, 371–387.CrossRefGoogle Scholar
Alçiçek, M.C., Mayda, S., Alçiçek, H., 2012. Faunal and palaeoenvironmental changes in the Çal Basin, SW Anatolia: Implications for regional stratigraphic correlation of late Cenozoic basins. Comptes Rendus - Geoscience 344, 89–98.CrossRefGoogle Scholar
Amprino, R., 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Archives of Biology 58, 315–330.Google Scholar
Amson, E., Kolb, C., Scheyer, T.M., Sánchez-Villagra, M.R., 2015. Growth and life history of Middle Miocene deer (Mammalia, Cervidae) based on bone histology. Comptes Rendus - Palevol 14, 637–645.CrossRefGoogle Scholar
Antoine, P.-O., Saraç, G., 2005. Rhinocerotidae (Mammalia, Perissodactyla) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 601–632.Google Scholar
Atalay, Z., 1980. Muğla-Yatağan ve Yakın Dolayı Karasal Neojen'inin Stratigrafi Araştırması. Bulletin of the Geological Society of Turkey 23, 3–99.Google Scholar
Azzaroli, A., 1992. Ascent and decline of monodactyl equids: a case for prehistoric overkill. Annales Zoologici Fennici 28, 151–163.Google Scholar
Bao, V., Rachel, H., Bradley, W., Curry Rogers, K., 2009. Patterns of microbial bioerosion in bones from the Campanian Judith River Formation of Montana. In: Geological Society of America. Abstracts with Programs. p. 628.Google Scholar
Bell, L.S., Skinner, M.F., Jones, S.J., 1996. The speed of post mortem change to the human skeleton and its taphonomic significance. Forensic Science International 82, 129–140.CrossRefGoogle ScholarPubMed
Bernor, R.L., Göhlich, U.B., Harzhauser, M., Semprebon, G.M., 2017. The Pannonian C hipparions from the Vienna Basin. Palaeogeography, Palaeoclimatology, Palaeoecology 476, 28–41.CrossRefGoogle Scholar
Bernor, R.L., Kovar-Eder, J., Lipscomb, D., Rögl, F., Sen, S., Tobien, H., 1988. Systematic, Stratigraphic, and Paleoenvironmental Contexts of First-Appearing Hipparion in the Vienna Basin, Austria. Journal of Vertebrate Paleontology 8, 427–452.CrossRefGoogle Scholar
Bernor, R.L., Scott, R.S., Fortelius, M., Kappelman, J., Sen, S., 2003. Equidae (Perissodactyla). In: Fortelius, M., Kappelman, J., Sen, S., Bernor, R.L. (Eds.), The Geology and Paleontology of the Miocene Sinap Formation, Turkey. Columbia University Press, New York.Google Scholar
Bernor, R.L., Tobien, H., Woodburne, M.O., 1990. Patterns of Old World Hipparionine Evolutionary Diversification and Biogeographic Extension. In: Lindsay, E.H., Fahlbusch, V., Mein, P. (Eds.), European Neogene Mammal Chronology. Plenum Press, New York, pp. 263–319.CrossRefGoogle Scholar
Bhat, M.S., Chinsamy, A., Parkington, J., 2019. Long bone histology of Chersina angulata: Interelement variation and life history data. Journal of Morphology 280, 1881–1899.CrossRefGoogle ScholarPubMed
Bonar, L.C., Glimcher, M.J., 1970. Thermal denaturation of mineralized and demineralized bone collagens. Journal of Ultrasructure Research 32, 545–557.CrossRefGoogle ScholarPubMed
Boulbes, N., Mayda, S., Titov, V.V., Alçiçek, M.C., 2014. Les grands mammifères du Villafranchien supérieur des travertins du Bassin de Denizli (Sud-Ouest Anatolie, Turquie). Anthropologie. 118, 44–73.CrossRefGoogle Scholar
Boulbes, N., van Asperen, E.N., 2019. Biostratigraphy and Palaeoecology of European Equus. Frontiers in Ecology and Evolution 7, 301.CrossRefGoogle Scholar
Brönnimann, D., Portmann, C., Pichler, S.L., Booth, T.J., Röder, B., Vach, W., Schibler, J., Rentzel, P., 2018. Contextualising the dead—Combining geoarchaeology and osteo-anthropology in a new multi-focus approach in bone histotaphonomy. Journal of Archaeological Science 98, 45–58.CrossRefGoogle Scholar
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. Journal of Zoology 263, 31–39.CrossRefGoogle Scholar
Castanet, J., Francillon-Vieillot, H., Meunier, F., de Ricqlès, A., 1993. Bone and individual aging. In: Hall, B.K. (Ed.), Bone: A Treatise, Vol. 7. CRC Press, Boca Raton, pp. 245–283.Google Scholar
Child, A.M., 1995. Microbial taphonomy of archaeological bone. Studies in Conservation 40, 19–30.Google Scholar
Chinsamy-Turan, A., 2005. The microstructure of dinosaur bone. Deciphering biology with fine-scale techniques. The Johns Hopkins University Press, Baltimore and London.Google Scholar
Chinsamy-Turan, A., 2012. Forerunners of mammals: radiation, histology, biology. Indiana University Press, Bloomington.Google Scholar
Chinsamy-Turan, A., Ray, S., 2012. Bone histology of some Therocephalians and Gorgonopsians, and evidence of bone degradation by fungi. In: Chinsamy-Turan, A. (Ed.), Forerunners of Mammals: Radiation, Histology, Biology. Indiana University Press, Bloomington, pp. 199–222.Google Scholar
Chinsamy, A., Hanrahan, S.A., Neto, R.M., Seeley, M., 1995. A skeletochronological assessment of age in Angolosaurus skoogi, a lizard living in an aseasonal environment. Journal of Herpetology 29, 457–460.CrossRefGoogle Scholar
Chinsamy, A., Raath, M.A., 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana 29, 39–44.Google Scholar
Chinsamy, A., Valenzuela, N., 2008. Skeletochronology of the endangered side-neck turtles Podocnemis expansa. South African Journal of Science 104, 311–314.Google Scholar
Christol, J. de, 1832. Description d’Hipparion. Annales des Sciences et de l'Industrie du Midi de France 1, 180–181.Google Scholar
Currey, J.D., 2002. Bones. Structure and mechanics. Princeton University Press, Princeton.CrossRefGoogle Scholar
Dal Sasso, G., Maritan, L., Usai, D., Angelini, I., Artioli, G., 2014. Bone diagenesis at the micro-scale: Bone alteration patterns during multiple burial phases at Al Khiday (Khartoum, Sudan) between the Early Holocene and the II century AD. Palaeogeography, Palaeoclimatology, Palaeoecology 416, 30–42.CrossRefGoogle Scholar
Damann, F.E., Jans, M.M.E., 2017. Microbes, anthropology, and bones. In: Carte, D.O., Tomberlin, J.K., Benbow, M.E., Metcalf, J.L. (Eds.), Forensic Microbiology. John Wiley & Sons, Ltd, West Sussex, pp. 312–327.CrossRefGoogle Scholar
Davis, P.G., 1997. The Bioerosion of Bird Bones. International Journal of Osteoarchaeology 7, 388–401.3.0.CO;2-H>CrossRefGoogle Scholar
de Bonis, L., 2005. Carnivora (Mammalia) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 567–589.Google Scholar
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 - Biology 325, 221–230.CrossRefGoogle Scholar
Demirel, F.A., Mayda, S., 2014. A new Early Pleistocene mammalian fauna from Burdur Basin, SW Turkey. Russian Journal of Theriology 13, 55–63.CrossRefGoogle Scholar
de Ricqlès, A., 1975. Recherches paléohistologiques sur les os longs des tétrapodes VII.—Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des tétrapodes. Première partie, structures. Annales de Paléontologie (Vertébrés) 61, 51–129.Google Scholar
Eisenmann, V., Sondaar, P., 1998. Pliocene vertebrate locality of Çalta, Ankara, Turkey. 7. Hipparion. Geodiversitas 20, 409–439.Google Scholar
Enlow, D.H., 1962. A study of the post-natal growth and remodeling of bone. American Journal of Anatomy 110, 79–101.CrossRefGoogle Scholar
Enlow, D.H., Brown, S.O., 1956. A comparative histological study of fossil and recent bone tissues. Part I. Texas Journal of Science 8, 405–412.Google Scholar
Enlow, D.H., Brown, S.O., 1957. A comparative histological study of fossil and recent bone tissues. Part II. Texas Journal of Science 9, 186–214.Google Scholar
Enlow, D.H., Brown, S.O., 1958. A comparative histological study of fossil and recent bone tissues. Part III. Texas Journal of Science 10, 187–230.Google Scholar
Erismis, U.C., Chinsamy, A., 2010. Ontogenetic Changes in the Epiphyseal Cartilage of Rana (Pelophylax) caralitana (Anura: Ranidae). The Anatomical Record 293, 1825–1837.CrossRefGoogle Scholar
Erten, H., Sen, S., Özkul, M., 2005. Pleistocene mammals from travertine deposits of the Denizli basin (SW Turkey). Annales du Paléontologie 91, 267–278.CrossRefGoogle Scholar
Fernández-Jalvo, Y., Andrews, P., 2016. Atlas of Taphonomic Identifications. 1001+ Images of Fossil and Recent Mammal Bone Modification, Vertebrate Paleobiology and Paleoantropology Series. Springer, Dordrecht.CrossRefGoogle Scholar
Fernández-Jalvo, Y., Andrews, P., Pesquero, D., Smith, C., Marín-Monfort, D., Sánchez, B., Geigl, E.M., Alonso, A., 2010. Early bone diagenesis in temperate environments. Part I: Surface features and histology. Palaeogeography, Palaeoclimatology, Palaeoecology 288, 62–81.CrossRefGoogle Scholar
Forsten, A., 1988. Middle Pleistocene replacement of stenonid horses by caballoid horses - Ecological implications. Palaeogeography, Palaeoclimatology, Palaeoecology 65, 23–33.CrossRefGoogle Scholar
Forsten, A., 1989. Horse diversity through the ages. Biological Reviews 64, 279–304.CrossRefGoogle ScholarPubMed
Forsten, A., Kaya, T., 1995. The hipparions (Mammalia, Equidae) from Gülpınar (Çanakkale, Turkey). Paläontologische Zeitschrift 69, 491–501.CrossRefGoogle Scholar
Francillon-Vieillot, H., de Buffrénil, V., Castanet, J., Géraudie, J., Meunier, F.J., Sire, J.Y., Zylberberg, L., de Ricqlès, A., 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter, J.G. (Ed.), Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends. Van Nostrand Reinhold, New York, pp. 471–530.Google Scholar
Galligani, P., Sartori, J., Barrientos, G., 2019. Bacterial bioerosion in human and animal bones from subtropical environments (Northern Pampa/Middle Paraná River Basin, República Argentina). Journal of Archaeological Science: Reports 25, 561–574.CrossRefGoogle Scholar
Garcés, M., Cabrera, L., Agustí, J., Parés, J.M., 1997. Old world first appearance datum of “Hipparion” horses: Late Miocene large-mammal dispersal and global events. Geology 25, 19–22.2.3.CO;2>CrossRefGoogle Scholar
Garland, A.N., 1989. Microscopical analysis of fossil bone. Applied Geochemistry 4, 215–229.CrossRefGoogle Scholar
Garrone, M.C., Cerda, I.A., Tomassini, R.L., 2019. Ontogenetic variability in the limb bones histology of plains vizcacha (Lagostomus maximus, Chinchillidae, Rodentia): implications for life history reconstruction of fossil representatives. Historical Biology In press.Google Scholar
Geiger, M., Wilson, L.A.B., Costeur, L., Sánchez, R., Sánchez-Villagra, M.R., 2013. Diversity and body size in giant caviomorphs (Rodentia) from the northern Neotropics - A study of femoral variation. Journal of Vertebrate Paleontology 33, 1449–1456.CrossRefGoogle Scholar
Geraads, D., Gulec, E., Kaya, T., 2002. Sinotragus (Bovidae, mammalia) from Turkey and the Late Miocene Middle Asiatic Province. Neues Jahrbuch für Geologie und Paläontologie Monatshefte 8, 477–489.CrossRefGoogle Scholar
Guo, L., Riding, R., 1998. Hot-spring travertine facies and sequences, Late Pleistocene, Rapolano Terme, Italy. Sedimentology 45, 163–180.CrossRefGoogle Scholar
Hackett, C.J., 1981. Microscopical focal destruction (tunnels) in exhumed human bones. Medicine, Science and the Law 21, 243–265.CrossRefGoogle ScholarPubMed
Hanson, M., Cain, C.R., 2007. Examining histology to identify burned bone. Journal of Archaeological Science 34, 1902–1913.CrossRefGoogle Scholar
Haynes, S., Searle, J.B., Bretman, A., Dobney, K.M., 2002. Bone preservation and ancient DNA: The application of screening methods for predicting DNA survival. Journal of Archaeological Science 29, 585–592.CrossRefGoogle Scholar
Hedges, R.E.M., 2002. Bone diagenesis: An overview of processes. Archaeometry 44, 319–328.CrossRefGoogle Scholar
Hedges, R.E.M., Millard, A.R., Pike, A.W.G., 1995. Measurements and relationships of diagenetic alteration of bone from three archaeological sites. Journal of Archaeological Science 22, 201–209.CrossRefGoogle Scholar
Hilgen, F.J., Lourens, L.J., Van Dam, J.A., Beu, A.G., Boyes, A.F., Cooper, R.A., Krijgsman, W., Ogg, James G., Piller, W.E., Wilson, D.S., 2012. The Neogene Period. In: Gradstein, F.., Ogg, J.G, Schmitz, M., Ogg, G. (Eds.), The Geologic Time Scale, Elsevier, Amsterdam, pp. 923–978.CrossRefGoogle Scholar
Hollund, H.I., Jans, M.M.E., Collins, M.J., Kars, H., Joosten, I., Kars, S.M., 2012. What happened here? Bone histology as a tool in decoding the postmortem histories of archaeological bone from Castricum, The Netherlands. International Journal of Osteoarchaeology 22, 537–548.CrossRefGoogle Scholar
Huttenlocker, A.K., Woodward, H.N., Hall, B.K., 2013. The biology of bone. In: Padian, K., Lamm, E.-T. (Eds.), Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation. University of California Press, Berkeley, pp. 13–34.Google Scholar
Jans, M.M.E., 2005. Histological characterisation of diagenetic alteration of archaeological bone. Vrije Universiteit, Amsterdam.Google Scholar
Jans, M.M.E., 2008. Microbial bioerosion of bone—a review. In: Wisshak, M., Tapanila, L. (Eds.), Current Developments in Bioerosion. Erlangen Earth Conference Series. Springer-Verlag, Berlin, Heidelberg, pp. 397–413.CrossRefGoogle Scholar
Jans, M.M.E., Kars, H., Nielsen-Marsh, C.M., Smith, C.I., Nord, A.G., Arthur, P., Earl, N., 2002. In situ preservation of archaeological bone: a histological study within a multidisciplinary approach. Archaeometry 44, 343–352.CrossRefGoogle Scholar
Jans, M.M.E., Nielsen-Marsh, C.M., Smith, C.I., Collins, M.J., Kars, H., 2004. Characterisation of microbial attack on archaeological bone. Journal of Archaeological Science 31, 87–95.CrossRefGoogle Scholar
Jiménez-Moreno, G., Alçiçek, H., Alçiçek, M.C., van den Hoek Ostende, L., Wesselingh, F.P., 2015. Vegetation and climate changes during the late Pliocene and early Pleistocene in SW Anatolia, Turkey. Quaternary Research 84, 448–456.CrossRefGoogle Scholar
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, 255–266.CrossRefGoogle Scholar
Kahlke, R.D., García, N., Kostopoulos, D.S., Lacombat, F., Lister, A.M., Mazza, P.P.A., Spassov, N., Titov, V.V., 2011. Western Palaearctic palaeoenvironmental conditions during the Early and early Middle Pleistocene inferred from large mammal communities, and implications for hominin dispersal in Europe. Quaternary Science Reviews 30, 1368–1395.CrossRefGoogle Scholar
Kaya, O., 1981. Miocene reference section for the coastal parts of West Anatolia. Newsletters on Stratigraphy 10, 164–191.CrossRefGoogle Scholar
Kaya, O., Müller, E.D., Rückert-Ülkümen, N., Kaya, T., 1998. Biostratigraphic and Environmental Aspects of the Late Miocene-Early Pliocene Deposits in Develiköy (Manisa, Turkey). Mitteilungen der Bayerischen Staatssammlung für Paläontologie und historische Geologie 38, 3–7.Google Scholar
Kaya, T., Forsten, A., 1999. Late Miocene Ceratotherium and Hipparion (Mammalia, Perissodactyla) from Düzyayla (Hafik, Sivas), Turkey. Geobios 32, 743–748.CrossRefGoogle Scholar
Kaya, T., Geraads, D., Tuna, V., 2005a. A new Late Miocene mammalian fauna in the Karaburun Peninsula (W Turkey). Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen Band 236, 321–349.CrossRefGoogle Scholar
Kaya, T., Mayda, S., Saraç, G., 2005b. A new Late Miocene mammalian fauna from Bayat (Kütahya, Western Turkey). In: International Earth Sciences Colloquium on the Aegean Regions (IESCA 2005). pp. 62–63.Google Scholar
Kaya, T.T., Mayda, S., Kostopoulos, D.S., Alcicek, M.C., Merceron, G., Tan, A., Karakutuk, S., Giesler, A.K., Scott, R.S., 2012. Şerefköy-2, a new Late Miocene mammal locality from the Yatağan Formation, Muğla, SW Turkey. Comptes Rendus - Palevol 11, 5–12.CrossRefGoogle Scholar
Kayseri-Özer, M.S., Karadenizli, L., Akgün, F., Oyal, N., Saraç, G., Şen, Ş., Tunoğlu, C., Tuncer, A., 2017. Palaeoclimatic and palaeoenvironmental interpretations of the Late Oligocene, Late Miocene–Early Pliocene in the Çankırı-Çorum Basin. Palaeogeography, Palaeoclimatology, Palaeoecology 467, 16–36.CrossRefGoogle Scholar
Kazanci, N., Karadenizli, L., Seyitoǧlu, G., Sen, S., Alçiçek, M.C., Varol, B., Saraç, G., Hakyemez, Y., 2005. Stratigraphy and sedimentology of Neogene mammal bearing deposits in the Akkaşdaǧι area, Turkey. Geodiversitas 27, 527–551.Google Scholar
Kendall, C., Eriksen, A.M.H., Kontopoulos, I., Collins, M.J., Turner-Walker, G., 2018. Diagenesis of archaeological bone and tooth. Palaeogeography, Palaeoclimatology, Palaeoecology 491, 21–37.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Köhler, M., Moyà-Solà, S., 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proceedings of the National Academy of Science of the United States of America 106, 20354–20358.CrossRefGoogle Scholar
Kolb, C., Scheyer, T.M., Lister, A.M., Azorit, C., de Vos, J., Schlingemann, M., Rössner, G.E., Monaghan, N.T., Sánchez-Villagra, M.R., 2015a. Growth in fossil and extant deer and implications for body size and life history evolution. BMC Evolutionary Biology 15, 19.CrossRefGoogle Scholar
Kolb, C., Scheyer, T.M., Veitschegger, K., Forasiepi, A.M., Amson, E., Van der Geer, A.A.E., Van den Hoek Ostende, L.W., Hayashi, S., Sánchez-Villagra, M.R., 2015b. Mammalian bone palaeohistology: a survey and new data with emphasis on island forms. PeerJ 3, e1358.CrossRefGoogle Scholar
Kontopoulos, I., Nystrom, P., White, L., 2016. Experimental taphonomy: post-mortem microstructural modifications in Sus scrofa domesticus bone. Forensic Science International 266, 320–328.CrossRefGoogle ScholarPubMed
Kostopoulos, D.S., Saraç, G., 2005. Giraffidae (Mammalia, Artiodactyla) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 735–745.Google Scholar
Kostopoulos, D.S., Sen, S., 1999. Late Pliocene (Villafranchian) mammals from Sarikol Tepe, Ankara, Turkey. Mitteilungen der Bayerischen Staatssammlung für Paläontologie und historische Geologie 39, 165–202.Google Scholar
Koufos, G.D., Kostopoulos, D.S., 1994. The late Miocene mammal localities of Kemiklitepe, Turkey: 3. Equidae. Bulletin du Muséum National d'Histoire Naturelle 16, 41–80.Google Scholar
Koufos, G.D., Mayda, S., Kaya, T., 2018. New carnivoran remains from the Late Miocene of Turkey. PalZ 92, 131–162.CrossRefGoogle Scholar
Koufos, G.D., Vlachou, T.D., 2005. Equidae (Mammalia, Perissodactyla) from the late Miocene of Akkașdağı, Turkey. Geodiversitas 27, 633–705.Google Scholar
Lebatard, A.E., Alçiçek, M.C., Rochette, P., Khatib, S., Vialet, A., Boulbes, N., Bourlès, D.L., et al. , 2014. Dating the Homo erectus bearing travertine from Kocabaş (Denizli, Turkey) at at least 1.1 Ma. Earth and Planetary Science Letters 390, 8–18.CrossRefGoogle Scholar
Lees, S., 1989. Some characteristics of mineralised collagen. In: Hukins, D.W.L. (Ed.), Calcified Tissue. The Macmillan Press, LTD, Houndmills, pp. 153–173.CrossRefGoogle Scholar
Legendre, L.J., Botha-Brink, J., 2018. Digging the compromise: investigating the link between limb bone histology and fossoriality in the aardvark (Orycteropus afer). PeerJ 6, e5216.CrossRefGoogle Scholar
Lindsay, E.H., Opdyke, N.D., Johnson, N.M., 1980. Pliocene dispersal of the horse Equus and late Cenozoic mammalian dispersal events. Nature 287, 135–138.CrossRefGoogle Scholar
Liu, L., Kostopoulos, D.S., Fortelius, M., 2005. Suidae (Mammalia, Artiodactyla) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 715–733.Google Scholar
Lyras, G.A., Giannakopoulou, A., Lillis, T., van der Geer, A.A.E., 2019. Paradise lost: Evidence for a devastating metabolic bone disease in an insular Pleistocene deer. International Journal of Paleopathology 24, 213–226.CrossRefGoogle Scholar
Lyras, G.A., Giannakopoulou, A., Lillis, T., Veis, A., Papadopoulos, G.C., 2016. Bone lesions in a Late Pleistocene assemblage of the insular deer Candiacervus sp.II from Liko cave (Crete, Greece). International Journal of Paleopathology 14, 36–45.CrossRefGoogle Scholar
MacFadden, B.J., 1984. Systematics and phylogeny of Hipparion, Neohipparion, Nannippus, and Cormohipparion (Mammalia, Equidae) from the Miocene and Pliocene of the New World. Bulletin of the American Museum of Natural History 179, 1–196.Google Scholar
MacFadden, B.J., 1985. Patterns of phylogeny and rates of evolution in fossil horses: hipparions from the Miocene and Pliocene of North America. Paleobiology 11, 245–257.CrossRefGoogle Scholar
MacFadden, B.J., 1992. Fossil horses. Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge University Press, Cambridge.Google Scholar
MacFadden, B.J., 2005. Fossil Horses—Evidence for Evolution. Science 307, 1728–1730.CrossRefGoogle ScholarPubMed
Marchiafava, V., Bonucci, E., Ascenzi, A., 1974. Fungal osteoclasia: a model of dead bone resorption. Calcified Tissue Research 14, 195–210.CrossRefGoogle Scholar
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, 469–478.CrossRefGoogle Scholar
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. Mammalian Biology 78, 422–429.CrossRefGoogle Scholar
Martínez-Maza, C., Alberdi, M.T., Nieto-Diaz, M., Prado, J.L., 2014. Life-history traits of the Miocene Hipparion concudense (Spain) inferred from bone histological structure. PLoS One 9, e103708.CrossRefGoogle ScholarPubMed
Mayda, S., Sotnikova, M., Tesakov, A., Tan, A., Kaya, T., 2015. Miocene-Pliocene transitional mammalian fauna of Develi (Turkey). In: 61 st Annual Session of the Russian Paleontologica Society. April 13–17, 2015. Saint-Petersburg. Paleontological Society of the Russian Academy of Sciences. pp. 182–183.Google Scholar
Mayda, S., Titov, V.V., Tesakov, A., Göktaş, F., Alçiçek, M.C., 2013. Revision of Plio-Pleistocene mammalian faunas from Çobanisa area (Western Turkey). In: VIII All-Russian Conference on Quaternary Research: Fundamental Problems of Queaternary, Results and Main Trands of Future Studies. SSC RAS Publishers, Rostov-on-Don, p. 48.Google Scholar
Mayer, E.L., Hubbe, A., Botha-Brink, J., Ribeiro, A.M., Haddad-Martim, P.M., Neves, W., 2020. Diagenetic changes on bone histology of Quaternary mammals from a tropical cave deposit in southeastern Brazil. Palaeogeography, Palaeoclimatology, Palaeoecology 537, 109372.CrossRefGoogle Scholar
McFarlin, S.C., Terranova, C.J., Zihlman, A.L., Enlow, D.H., Bromage, T.G., 2008. Regional variability in secondary remodeling within long bone cortices of catarrhine primates: The influence of bone growth history. Journal of Anatomy 213, 308–324.CrossRefGoogle ScholarPubMed
Metcalf, J.L., Xu, Z.Z., Weiss, S., Lax, S., Treuren, W. Van, Hyde, E.R., Song, S.J., et al. , 2016. Microbial community assembly and metabolic function during mammalian corpse decomposition. Science 351, 158–162.CrossRefGoogle ScholarPubMed
Millard, A., 2001. The deterioration of bone. In: Brothwell, D.R., Pollard, A.M. (Eds.), Handbook of Archaeological Sciences. John Wiley & Sons, Ltd, Chichester, pp. 637–647.Google Scholar
Miszkiewicz, J.J., Louys, J., Beck, R.M.D., Mahoney, P., Aplin, K., O'Connor, S., 2020. Island rule and bone metabolism in fossil murines from Timor. Biological Journal of the Linnean Society 129, 570–586.CrossRefGoogle Scholar
Miszkiewicz, J.J., Louys, J., O'Connor, S., 2019. Microanatomical record of cortical bone remodeling and high vascularity in a fossil giant rat midshaft femur. The Anatomical Record 302, 1934–1940.CrossRefGoogle Scholar
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, 227–237.CrossRefGoogle Scholar
Montoya-Sanhueza, G., Chinsamy, A., 2017. Long bone histology of the subterranean rodent Bathyergus suillus (Bathyergidae): ontogenetic pattern of cortical bone thickening. Journal of Anatomy 230, 203–233.CrossRefGoogle ScholarPubMed
Morales, N.S., Catella, L., Oliva, F., Sarmiento, P.L., Barrientos, G., 2018. A SEM-based assessment of bioerosion in Late Holocene faunal bone assemblages from the southern Pampas of Argentina. Journal of Archaeological Science: Reports 18, 782–791.CrossRefGoogle Scholar
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. PeerJ 4, e2580.CrossRefGoogle Scholar
Nacarino-Meneses, C., Jordana, X., Köhler, M., 2016b. First approach to bone histology and skeletochronology of Equus hemionus. Comptes Rendus - Palevol 15, 267–277.CrossRefGoogle Scholar
Nacarino-Meneses, C., Köhler, M., 2018. Limb bone histology records birth in mammals. PLoS One 13, e0198511.CrossRefGoogle ScholarPubMed
Nacarino-Meneses, C., Orlandi-Oliveras, G., 2019. The life history of European Middle Pleistocene equids: first insights from bone histology. Historical Biology In press.Google Scholar
Nielsen-Marsh, C., Gernaey, A., Turner-Walker, G., Hedges, R., Pike, A.W.G., Collins, M., 2000. The chemical degradation of bone. In: Cox, M., Mays, S. (Eds.), Human Osteology: In Archaeology and Forensic Science. Cambridge University Press, Cambridge, pp. 439–454.Google Scholar
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, 238–244.CrossRefGoogle Scholar
Orlandi-Oliveras, G., Nacarino-Meneses, C., Koufos, G.D., Köhler, M., 2018. Bone histology provides insights into the life history mechanisms underlying dwarfing in hipparionins. Scientific Reports 8, 17203.CrossRefGoogle ScholarPubMed
Orlando, L., 2015. Equids. Current Biology R973–R978.CrossRefGoogle ScholarPubMed
Orlando, L., Ginolhac, A., Zhang, G., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., et al. , 2013. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78.CrossRefGoogle ScholarPubMed
Özkul, M., Kele, S., Gökgöz, A., Shen, C.C., Jones, B., Baykara, M.O., Fórizs, I., Németh, T., Chang, Y.W., Alçiçek, M.C., 2013. Comparison of the Quaternary travertine sites in the Denizli extensional basin based on their depositional and geochemical data. Sedimentary Geology 294, 179–204.CrossRefGoogle Scholar
Pesquero, M.D., Bell, L.S., Fernández-Jalvo, Y., 2018. Skeletal modification by microorganisms and their environments. Historical Biology 30, 882–893.CrossRefGoogle Scholar
Pfretzschner, H.-U., 2000. Microcracks and fossilization of Haversian bone. Neues Jahrbbuch für Geologie und Paläontologie - Abhandlungen 216, 413–432.CrossRefGoogle Scholar
Pfretzschner, H.U., 2004. Fossilization of Haversian bone in aquatic environments. Comptes Rendus - Palevol 3, 605–616.CrossRefGoogle Scholar
Pfretzschner, H.U., Tütken, T., 2011. Rolling bones—Taphonomy of Jurassic dinosaur bones inferred from diagenetic microcracks and mineral infillings. Palaeogeography, Palaeoclimatology, Palaeoecology 310, 117–123.CrossRefGoogle Scholar
Prado, J.L., Alberdi, M.T., 1996. A cladistic analysis of the tribe Equini. Palaeontology 39, 663–680.Google Scholar
Pueyo, E.L., Muñoz, A., Laplana, C., Parés, J.M., 2016. The Last Appearance Datum of Hipparion in Western Europe: magnetostratigraphy along the Pliocene–Pleistocene boundary in the Villarroya Basin (Northern Spain). International Journal of Earth Sciences 105, 2203–2220.CrossRefGoogle Scholar
Rausch, L., Alçiçek, H., Vialet, A., Boulbes, N., Mayda, S., Titov, V.V., Stoica, M., et al. , 2019. An integrated reconstruction of the early Pleistocene palaeoenvironment of Homo erectus in the Denizli Basin (SW Turkey). Geobios 57, 77–95.CrossRefGoogle Scholar
Rook, L., Bernor, R.L., Avilla, L.S., Cirilli, O., Flynn, L., Jukar, A., Sanders, W., Scott, E., Wang, X., 2019. Mammal Biochronology (Land Mammal Ages) Around the World From Late Miocene to Middle Pleistocene and Major Events in Horse Evolutionary History. Frontiers in Ecology and Evolution 7, 278.CrossRefGoogle Scholar
Rook, L., Cirilli, O., Bernor, R.L., 2017. A Late Occurring “Hipparion” from the middle Villafranchian of Montopoli, Italy (early Pleistocene; MN16b; ca. 2.5 Ma). Bolletino della Società Paleontologica Italiana 56, 333–339.Google Scholar
Sander, P.M., Andrássy, P., 2006. Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: What do they tell us about dinosaur physiology? Palaeontographica Abteilung A 277, 143–159.Google Scholar
Saraç, G., Kaya, T., Geraads, D., 2002. Ancylotherium pentelicum (Perissodactyla, Mammalia) from the Upper Miocene of central and western Turkey. Geobios 35, 241–251.CrossRefGoogle Scholar
Saraç, G., Sen, S., 2005. Chalicotheriidae (Mammalia, Perissodactyla) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 591–600.Google Scholar
Schoeninger, M.J., Moore, K.M., Murray, M.L., Kingston, J.D., 1989. Detection of bone preservation in archaeological and fossil samples. Applied Geochemistry 4, 281–292.CrossRefGoogle Scholar
Sen, S., 1990. Hipparion datum and its chronologic evidence in the Mediterranean area. In: Lindsay, E.H., Fahlbusch, V., Mein, P. (Eds.), European Neogene Mammal Chronology. Plenum Press, New York, pp. 495–505.CrossRefGoogle Scholar
Sen, S., de Bonis, L., Dalfes, N., Geraads, D., Koufos, G.D., 1994. Les gisements de mammifères du Miocène supérieur de Kemiklitepe, Turquie: 1. Stratigraphie et magnétostratigraphie. Bulletin du Muséum National d'Histoire Naturelle 16, 5–17.Google Scholar
Sen, S., Seyitoğlu, G., Karadenizli, L., Kazanci, N., Varol, B., Araz, H., 1998. Mammalian biochronology of Neogene deposits and its correlation with the lithostratigraphy in the Çankırı-Çorum Basin, central Anatolia, Turkey. Eclogae Geologicae Helvetiae 91, 307–320.Google Scholar
Seyitoğlu, G., Alçiçek, C.M., Işık, V., Alçiçek, H., Mayda, S., Varol, B., Yılmaz, I., Esat, K., 2009. The stratigraphical position of Kemiklitepe fossil locality (Eşme, Uşsak) revised: Implications for the Late Cenozoic sedimentary basin development and extensional tectonics in western Turkey. Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen 251, 1–15.CrossRefGoogle Scholar
Strömberg, C.A.E., 2006. Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology 32, 236–258.CrossRefGoogle Scholar
Tassy, P., 2005. Proboscideans (Mammalia) from the late Miocene of Akkaşdaǧι, Turkey. Geodiversitas 27, 707–714.Google Scholar
Tekkaya, I., Atalay, Z., Gürbüz, M., Ünay, E., Ermumcu, M., 1975. Çankırı-Kalecik bölgesi karasal Neojeninin biostratigrafi araştırması. Bulletin of the Geological Society of Turkey 18, 77–80.Google Scholar
Tomassini, R.L., Miño-Boilini, Á.R., Zurita, A.E., Montalvo, C.I., Cesaretti, N., 2015. Modificaciones fosildiagenéticas en Toxodon platensis Owen, 1837 (Notoungulata, Toxodontidae) del Pleistoceno Tardío de la provincia de Corrientes, Argentina. Rev. Mex. Ciencias Geológicas 32, 283–292.Google Scholar
Trueman, C.N., Martill, D.M., 2002. The long-term survival of bone: the role of bioerosion. Archaeometry 44, 371–382.CrossRefGoogle Scholar
Turner-Walker, G., 2012. Early bioerosion in skeletal tissues: Persistence through deep time. Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen 265, 165–183.CrossRefGoogle Scholar
Turner-Walker, G., 2019. Light at the end of the tunnels? The origins of microbial bioerosion in mineralised collagen. Palaeogeography, Palaeoclimatology, Palaeoecology 529, 24–38.CrossRefGoogle Scholar
Turner-Walker, G., 2008. The chemical and microbial degradation of bones and teeth. In: Pinhasi, R., Mays, S. (Eds.), Advances in Human Palaeopathology. John Wiley & Sons, Ltd, Chichester, pp. 3–29.Google Scholar
Turner-Walker, G., Jans, M.M.E., 2008. Reconstructing taphonomic histories using histological analysis. Palaeogeography, Palaeoclimatology, Palaeoecology 266, 227–235.CrossRefGoogle Scholar
Turner-Walker, G., Nielsen-Marsh, C.M., Syversen, U., Kars, H., Collins, M.J., 2002. Sub-micron Spongiform Porosity is the Major Ultra-structural Alteration Occurring in Archaeological Bone. International Journal of Osteoarchaeology 12, 407–414.CrossRefGoogle Scholar
Valli, A.M.F., 2005. Taphonomy of the late Miocene mammal locality of Akkaşdaǧι, Turkey. Geodiversitas 27, 793–808.Google Scholar
van Asperen, E.N., 2012. Late Middle Pleistocene horse fossils from northwestern Europe as biostratigraphic indicators. Journal of Archaeological Science 39, 1974–1983.CrossRefGoogle Scholar
van der Sluis, L.G., Hollund, H.I., Buckley, M., De Louw, P.G.B., Rijsdijk, K.F., Kars, H., 2014. Combining histology, stable isotope analysis and ZooMS collagen fingerprinting to investigate the taphonomic history and dietary behaviour of extinct giant tortoises from the Mare aux Songes deposit on Mauritius. Palaeogeography, Palaeoclimatology, Palaeoecology 416, 80–91.CrossRefGoogle Scholar
Veitschegger, K., Kolb, C., Amson, E., Scheyer, T.M., Sánchez-Villagra, M.R., 2018. Palaeohistology and life history evolution in cave bears, Ursus spelaeus sensu lato. PLoS One 13, e0206791.CrossRefGoogle ScholarPubMed
Walker, M.M., Louys, J., Herries, A.I.R., Price, G.J., Miszkiewicz, J.J., 2020. Humerus midshaft histology in a modern and fossil wombat. Australian Mammalogy In press.Google Scholar
White, L., Booth, T.J., 2014. The origin of bacteria responsible for bioerosion to the internal bone microstructure: Results from experimentally-deposited pig carcasses. Forensic Science International 239, 92–102.CrossRefGoogle ScholarPubMed
Woodburne, M.O., Bernor, R.L., 1980. On Superspecific Groups of Some Old World Hipparionine Horses. Journal of Paleontology 54, 1319–1348.Google Scholar
Woodward, H.N., Padian, K., Lee, A.H., 2013. Skeletochronology. In: Padian, K., Lamm, E.-T. (Eds.), Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation. University of California Press, Berkeley, pp. 195–215.Google Scholar
Woolley, M.R., Chinsamy, A., Govender, R., Bester, M.N., 2019. Microanatomy and histology of bone pathologies of extant and extinct phocid seals. Historical Biology In press.Google Scholar
Zedda, M., Sathe, V., Chakraborty, P., Palombo, M.R., Farina, V., 2020. A first comparison of bone histomorphometry in extant domestic horses (Equus caballus Linnaeus, 1758) and a Pleistocene Indian wild horse (Equus namadicus Falconer & Cautley, 1849). Integrative Zoology In press.Google Scholar
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