Advertisement

Dental microwear textures and dietary preferences of extant rhinoceroses (Perissodactyla, Mammalia)

  • Manon HullotEmail author
  • Pierre-Olivier Antoine
  • Manuel Ballatore
  • Gildas Merceron
Original Paper

Abstract

Rhinoceroses were conspicuous elements in Cenozoic ecosystems, and studying the ecological behavior of extant species might unravel the ecology of their fossil kin. Microwear as a short-term recorder may detect subtle variations in the diet. Dental microwear texture analysis (DMTA) is extensively used to infer paleodiets. Yet, regarding ungulates, most microwear studies have been conducted on artiodactyls, and more particularly on ruminants (i.e., foregut fermenters), which may not be good models for hindgut fermenters, such as rhinoceroses. Moreover, rhinoceroses display a specific enamel ultrastructure with vertical Hunter–Schreger bands and a peculiar mastication cycle likely to impact tooth response to wear. Here, we studied the DMTA of the five extant rhinoceros species (17 specimens of Ceratotherium simum, four of Dicerorhinus sumatrensis, 21 of Diceros bicornis, 14 of Rhinoceros sondaicus, and 5 of Rhinoceros unicornis) and built up the present dataset. In parallel, we also compiled a taxon-based dataset of consumed plants for each rhinoceros species. Accordingly, we propose to reclassify the Indian rhinoceros (Rhinoceros unicornis) from mixed-feeder to variable grazer. Significant discrepancies were found between grinding and shearing facets on molars and between species on a given facet. Plotting the percentage of anisotropic specimens against that of complex specimens for each species discriminated well the different diets on both facets. This unprecedented dataset on rhinoceros texture microwear confronted to detailed diets appears critical for future diet reconstruction of fossil rhinocerotoids.

Keywords

Enamel microstructure Diet Dental microwear texture analysis (DMTA) Mastication Megaherbivore Rhinoceros 

Notes

Acknowledgements

We are indebted to the curators of all the visited institutions for granting access to the collections they are in charge of: S. Jiquel, B. Marandat and A.-L. Charruault (University of Montpellier), D. Berthet and F. Vigouroux (Musée des Confluences de Lyon), F. Zachos and A. Bibl (Natuhistorisches Museum Wien), J. Lesur and V. Bouetel (Muséum National d’Histoire Naturelle, Paris), M. Lowe (University Museum of Zoology of Cambrige), and E. Gilissen (Musée Royal d’Afrique Centrale, Tervuren). We thank R. Araújo, the advice of whom greatly improved the statistics. We are grateful to E. Berlioz, C. Robinet, and A. Ramdarshan for fruitful discussions. We thank the editor and anonymous reviewers for their relevant remarks that helped in clarifying a previous version of the manuscript. This study was partly funded by the Project ANR TRIDENT (ANR-13-JSV7-0008-01, PI: G. Merceron).This is ISEM article 2019-043.

Authors’ contributions

MB and MH molded the specimens of the database; MH did the review of plant consumption by the living rhinoceroses, and POA and GM revised it; MH and GM analyzed the microwear data; and MH led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Supplementary material

13364_2019_427_MOESM1_ESM.xlsx (611 kb)
ESM 1 (XLSX 610 kb)
13364_2019_427_MOESM2_ESM.xlsx (221 kb)
ESM 2 (XLSX 220 kb)
13364_2019_427_MOESM3_ESM.docx (102 kb)
ESM 3 (DOCX 101 kb)

References

  1. Abrams K (2016) Dental microwear variation in Teleoceras fossiger (Rhinocerotidae) from the Miocene (Hemphillian) of Kansas, with consideration of masticatory processes and enamel microstructure. Master Thesis, Fort Hays State UniversityGoogle Scholar
  2. Ammann H (1985) Contributions to the ecology and sociology of the Javan rhinoceros (Rhinoceros sondaicus Desm., 1822). Inaugural Dissertation, University of Basel, SwitzerlandGoogle Scholar
  3. Antoine P-O (2002) Phylogénie et évolution des Elasmotheriina (Mammalia, Rhinocerotidae). Mém Mus natl Hist nat 188:1–359Google Scholar
  4. Antoine P-O (2012) Pleistocene and Holocene rhinocerotids (Mammalia, Perissodactyla) from the Indochinese Peninsula. C R Palevol 11:159–168CrossRefGoogle Scholar
  5. Antoine P-O, Downing KF, Crochet J-Y et al (2010) A revision of Aceratherium blanfordi Lydekker, 1884 (Mammalia: Rhinocerotidae) from the Early Miocene of Pakistan: postcranials as a key. Zool J Linnean Soc 160:139–194.  https://doi.org/10.1111/j.1096-3642.2009.00597.x CrossRefGoogle Scholar
  6. Ballatore M, Merceron G, Breda M (2017) Inferences on the diet of fossil European rhinoceroses: Palaeoecological inferences from the dental material of Pliocene to Early Pleistocene European rhinoceroses. Lambert Academic PublishingGoogle Scholar
  7. Bentaleb I, Langlois C, Martin C, Iacumin P, Carré M, Antoine PO, Duranthon F, Moussa I, Jaeger JJ, Barrett N, Kandorp R (2006) Rhinocerotid tooth enamel 18O/16O variability between 23 and 12 Ma in southwestern France. Compt Rendus Geosci 338:172–179CrossRefGoogle Scholar
  8. Berlioz E, Azorit C, Blondel C et al (2017) Deer in an arid habitat: dental microwear textures track feeding adaptability. Hystrix Ital J Mammal 28:222–230.  https://doi.org/10.4404/hystrix-28.2-12048 CrossRefGoogle Scholar
  9. Bhatta R (2011) Ecology and Conservation of Great Indian One horned Rhino Rhinoceros unicornis in Pobitora Wildlife Sanctuary Assam India. PhD Thesis, Gauhati UniversityGoogle Scholar
  10. Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910.  https://doi.org/10.1046/j.1420-9101.2002.00472.x CrossRefGoogle Scholar
  11. Boisserie J-R, Zazzo A, Merceron G, Blondel C, Vignaud P, Likius A, Mackaye HT, Brunet M (2005) Diets of modern and late Miocene hippopotamids: evidence from carbon isotope composition and micro-wear of tooth enamel. Palaeogeogr Palaeoclimatol Palaeoecol 221:153–174CrossRefGoogle Scholar
  12. Boyde A, Fortelius M (1986) Development, structure and function of rhinoceros enamel. Zool J Linnean Soc 87:181–214.  https://doi.org/10.1111/j.1096-3642.1986.tb01336.x CrossRefGoogle Scholar
  13. Brizuela MA, Detling JK, Cid MS (1986) Silicon concentration of grasses growing in sites with different grazing histories. Ecology 67:1098–1101.  https://doi.org/10.2307/1939834 CrossRefGoogle Scholar
  14. Brown DH, Lent PC, Trollope WSW, Palmer AR (2003) Browse selection of black rhinoceros (Diceros bicornis) in two vegetation types of the Eastern Cape Province, South Africa, with particular reference to Euphorbiaceae. Proceedings of the VIIth International Rangeland Congress, pp 508–512Google Scholar
  15. Buk KG (2004) Diet selection of and habitat suitability for black rhino in Augrabies Falls National Park, South Africa. Master Thesis, University of CopenhagenGoogle Scholar
  16. Buk KG, Knight MH (2010) Seasonal diet preferences of black rhinoceros in three arid South African National Parks. Afr J Ecol 48:1064–1075CrossRefGoogle Scholar
  17. Calandra I, Merceron G (2016) Dental microwear texture analysis in mammalian ecology. Mammal Rev 46:215–228.  https://doi.org/10.1111/mam.12063 CrossRefGoogle Scholar
  18. Calandra I, Labonne G, Schulz-Kornas E, Kaiser TM, Montuire S (2016) Tooth wear as a means to quantify intra-specific variations in diet and chewing movements. Sci Rep 6:34037.  https://doi.org/10.1038/srep34037 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cerdeño E (1998) Diversity and evolutionary trends of the family Rhinocerotidae (Perissodactyla). Palaeogeogr Palaeoclimatol Palaeoecol 141:13–34.  https://doi.org/10.1016/S0031-0182(98)00003-0 CrossRefGoogle Scholar
  20. Charles C, Jaeger J-J, Michaux J, Viriot L (2007) Dental microwear in relation to changes in the direction of mastication during the evolution of Myodonta (Rodentia, Mammalia). Naturwissenschaften 94:71–75.  https://doi.org/10.1007/s00114-006-0161-7 CrossRefPubMedGoogle Scholar
  21. Choong MF, Lucas PW, Ong JSY et al (1992) Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytol 121:597–610.  https://doi.org/10.1111/j.1469-8137.1992.tb01131.x CrossRefGoogle Scholar
  22. Codron D, Codron J, Lee-Thorp JA et al (2007) Diets of savanna ungulates from stable carbon isotope composition of faeces. J Zool 273:21–29.  https://doi.org/10.3389/fevo.2018.00191 CrossRefGoogle Scholar
  23. Coetzee CG (1970) The distribution of mammals in the Namib Desert and adjoining inland escarpment. Scient Pap Namib Desert Res Stn 40:23–36Google Scholar
  24. de Mendiburu F (2019) agricolae: Statistical Procedures for Agricultural Research. R package version 1.3-0. https://CRAN.R-project.org/package=agricolae
  25. Deka RJ, Sarma NK, Baruah KK (2003) Nutritional evaluation of the principal forages/feed consumed by Indian rhino (Rhinoceros unicornis) in Pobitora Wildlife Sanctuary and Assam State Zoo-cum-Botanical Garden, Assam. Zoos’ Print J 18:1043–1045CrossRefGoogle Scholar
  26. Dinerstein E (1991) Seed dispersal by greater one-horned rhinoceros (Rhinoceros unicornis) and the flora of Rhinoceros latrines. Mammalia 55:355–362.  https://doi.org/10.1515/mamm.1991.55.3.355 CrossRefGoogle Scholar
  27. Dinerstein E, Price L (1991) Demography and habitat use by greater one-horned rhinoceros in Nepal. J Wildl Manag 55:401–411.  https://doi.org/10.2307/3808968 CrossRefGoogle Scholar
  28. Domning DP, Emry RJ, Portell RW, Donovan SK, Schindler KS (1997) Oldest West Indian land mammal: rhinocerotoid ungulate from the Eocene of Jamaica. J Vertebr Paleontol 17:638–641.  https://doi.org/10.1080/02724634.1997.10011013 CrossRefGoogle Scholar
  29. Dudley CO (1997) The candelabra tree (Euphorbia ingens): a source of water for black rhinoceros in Liwonde National Park, Malawi. Koedoe 40:57–62.  https://doi.org/10.4102/koedoe.v40i1.263 CrossRefGoogle Scholar
  30. Emslie RH (1999) The feeding ecology of the black rhinoceros (Diceros bicornis minor) in Hluhluwe-Umfolozi Park, with special reference to the probable causes of the Hluhluwe population crash. PhD Thesis, University of StellenboschGoogle Scholar
  31. Emslie RH (2008) Rhino population sizes and trends. Pachyderm 44:88–95Google Scholar
  32. Emslie RH (2012) Ceratotherium simum. The IUCN Red List of Threatened Species 2012: e.T4185A16980466.  https://doi.org/10.2305/IUCN.UK.2012.RLTS.T4185A16980466.en. Downloaded on 28 February 2019
  33. Emslie RH, Adcock K (1994) Feeding ecology of black rhinoceros. In: Proceedings of the symposium Rhinos as game ranch animals. SAVA Wildlife Group, Onderstepoort. pp 65–81Google Scholar
  34. Evans GH (1904) The Asiatic two-horned rhinoceros (Rhinoceros sumatrensis). J Bombay Nat Hist Soc 16:160–161Google Scholar
  35. Fjellstad JI, Steinheim G (1996) Diet and habitat use of Greater Indian one horned Rhinoceros (Rhinoceros unicornis) and Asian elephant (Elephas maximus) during the dry season in Babai Valley, Royal Bardia National Park, Nepal. Master Thesis, Agricultural University of NorwayGoogle Scholar
  36. Flynn RW (1981) Distribution, ecology & conservation of the Sumatran rhinoceros in Malaysia. Prog Rep 1–33Google Scholar
  37. Fortelius M (1985) Ungulate cheek teeth : developmental, functional and evolutionary interrelations. Acta Zool Fenn 180:1–76Google Scholar
  38. Fox J and Weisberg S (2011) An {R} Companion to Applied Regression, 3rd edn.Sage PublicationsGoogle Scholar
  39. Gagnon M, Chew AE (2000) Dietary preferences in extant African Bovidae. J Mammal 81:490–511.  https://doi.org/10.1644/1545-1542(2000)081<0490:DPIEAB>2.0.CO;2 CrossRefGoogle Scholar
  40. Goddard J (1968) Food preferences of two black rhinoceros populations. East Afr Wildl J 6:1–18CrossRefGoogle Scholar
  41. Goddard J (1970) Food preferences of black rhinoceros in the Tsavo National Park. East Afr Wildl J 8:145–161.  https://doi.org/10.1111/j.1365-2028.1970.tb00837.x CrossRefGoogle Scholar
  42. Gordon IJ, Prins HHT (2008) The ecology of browsing and grazing. Springer, HeidelbergCrossRefGoogle Scholar
  43. Groves CP (1972) Ceratotherium simum. Mamm Species 1–6.  https://doi.org/10.2307/3503966
  44. Groves CP, Kurt F (1972) Dicerorhinus sumatrensis. Mamm Species 21:1–6.  https://doi.org/10.2307/3503818 CrossRefGoogle Scholar
  45. Groves CP, Leslie DM (2011) Rhinoceros sondaicus (Perissodactyla: Rhinocerotidae). Mamm Species 43:190–208.  https://doi.org/10.1644/887.1 CrossRefGoogle Scholar
  46. Groves CP, Fernando P, Robovskỳ J (2010) The sixth rhino: a taxonomic re-assessment of the critically endangered northern white rhinoceros. PLoS One 5:e9703CrossRefPubMedPubMedCentralGoogle Scholar
  47. Guérin C (1980) Les Rhinocéros (Mammalia, Perissodactyla) du Miocène terminal au Pleistocène supérieur en Europe occidentale. Comparaison avec les espèces actuelles. Doc Lab Géol Univ Lyon, Sci Terre 79:1–1184Google Scholar
  48. Hall-Martin AJ, Erasmus T, Botha BP (1982) Seasonal variation of diet and faeces composition of black rhinoceros Diceros bicornis in the Addo Elephant National Park. Koedoe 25:63–82CrossRefGoogle Scholar
  49. Hazarika BC, Saikia PK (2012) Food habit and feeding patterns of great Indian one-horned rhinoceros (Rhinoceros unicornis) in Rajiv Gandhi Orang National Park, Assam, India. ISRN Zoology 2012:1–11.  https://doi.org/10.5402/2012/259695 CrossRefGoogle Scholar
  50. Hedberg C, DeSantis LRG (2016) Dental microwear texture analysis of extant koalas: clarifying causal agents of microwear. J Zool 301:206–214.  https://doi.org/10.1111/jzo.12413 CrossRefGoogle Scholar
  51. Heller E (1913) The white rhinoceros: with thirty-one plates. Smithson Misc Collect 61:i, 1–56, pls. 1–31Google Scholar
  52. Hillman-Smith AKK, Groves CP (1994) Diceros bicornis. Mamm Species 455:1–8.  https://doi.org/10.2307/3504292 CrossRefGoogle Scholar
  53. Hillman-Smith AKK, Owen-Smith NR, Anderson JL et al (1986) Age estimation of the white rhinoceros (Ceratotherium simum). J Zool 210:355–377.  https://doi.org/10.1111/j.1469-7998.1986.tb.03639.x CrossRefGoogle Scholar
  54. Hitchins PM (1978) Age determination of the black rhinoceros (Diceros bicornis Linn.) in Zululand. S Afr J Wildl Res 8:71–80Google Scholar
  55. Hoffman JM, Fraser D, Clementz MT (2015) Controlled feeding trials with ungulates: a new application of in vivo dental molding to assess the abrasive factors of microwear. J Exp Biol 218:1538–1547.  https://doi.org/10.1242/jeb.118406 CrossRefPubMedGoogle Scholar
  56. Hoogerwerf A (1970) Udjung Kulon: the land of the last Javan rhinoceros. Brill, LeidenGoogle Scholar
  57. Hummel J, Findeisen E, Südekum K-H et al (2010) Another one bites the dust: faecal silica levels in large herbivores correlate with high-crowned teeth. Proc R Soc London B Bio 278:1742–1747.  https://doi.org/10.1098/rspb.2010.1939 CrossRefGoogle Scholar
  58. Joomun SC, Hooker JJ, Collinson ME (2008) Dental wear variation and implications for diet: an example from Eocene perissodactyls (Mammalia). Palaeogeogr Palaeoclimatol Palaeoecol 263:92–106.  https://doi.org/10.1016/j.palaeo.2008.03.001 CrossRefGoogle Scholar
  59. Joubert E, Eloff FC (1971) Notes on the ecology and behaviour of the black rhinoceros Diceros bicornis Linn. 1758 in South West Africa. Madoqua 1:5–53Google Scholar
  60. Kahlke R-D, Kaiser TM (2011) Generalism as a subsistence strategy: advantages and limitations of the highly flexible feeding traits of Pleistocene Stephanorhinus hundsheimensis (Rhinocerotidae, Mammalia). Quat Sci Rev 30:2250–2261.  https://doi.org/10.1016/j.quascirev.2099.12.012 CrossRefGoogle Scholar
  61. Kaiser TM, Brasch J, Castell JC, Schulz E, Clauss M (2009) Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics. Mamm Biol 74:425–437.  https://doi.org/10.1016/j.mambio.2008.09.003 CrossRefGoogle Scholar
  62. Kaiser TM, Müller DW, Fortelius M et al (2013) Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Rev 43:34–46CrossRefGoogle Scholar
  63. Kingdon J, Hoffmann M (2013) Mammals of Africa, carnivores, pangolins, equids and rhinoceroses, V. Bloomsbury Publishing, LondonGoogle Scholar
  64. Koenigswald WV, Holbrook LT, Rose KD (2011) Diversity and evolution of Hunter-Schreger band configuration in tooth enamel of perissodactyl mammals. Acta Palaeontol Pol 56:11–32CrossRefGoogle Scholar
  65. Konwar P, Saikia MK, Saikia PK (2009) Abundance of food plant species and food habits of Rhinoceros unicornis Linn. In: Pobitora Wildlife Sanctuary, Assam, India. J Threatened Taxa 1:457–460.  https://doi.org/10.11609/JoTT.o1640.457-60 CrossRefGoogle Scholar
  66. Krumbiegel I (1960) Die asiatischen Nashorne (Dicerorhinus Gloger und Rhinoceros Linné). Säugetierk Mitt 8:12–20Google Scholar
  67. Laurie WA (1982) Behavioural ecology of the greater one-horned rhinoceros (Rhinoceros unicornis). J Zool 196:307–341.  https://doi.org/10.1111/j.1469-7998.1982.tb03506.x CrossRefGoogle Scholar
  68. Laurie WA, Lang EM, Groves CP (1983) Rhinoceros unicornis. Mamm Species 211:1–6.  https://doi.org/10.2307/3504002 CrossRefGoogle Scholar
  69. Loose H (1975) Pleistocene Rhinocerotidae of W. Europe with reference to the recent two-horned species of Africa and SE Asia. Scr Geol 33:1–59Google Scholar
  70. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003.  https://doi.org/10.1111/j.1461-0248.2008.01229.x CrossRefPubMedGoogle Scholar
  71. Loutit BD, Louw GN, Seely MK (1987) First approximation of food preferences and the chemical composition of the diet of the desert-dwelling black rhinoceros, Diceros bicornis L. Madoqua 15:35–54Google Scholar
  72. Lydekker R (1907) The game animals of India, Burma, Malaya, and Tibet: being a new and revised edition of 'The great and small game of India, Burma, and Tibet'. Rowland Ward Limited, LondonGoogle Scholar
  73. Maas MC (1997) Enamel microstructure in notoungulates. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) Vertebrate paleontology in the neotropics : the Miocene fauna of La Venta, Colombia. Smithsonian Institution Scholarly Press, Washington, pp 319–334Google Scholar
  74. Martin C, Bentaleb I, Antoine P-O (2011) Pakistan mammal tooth stable isotopes show paleoclimatic and paleoenvironmental changes since the early Oligocene. Palaeogeogr Palaeoclimatol Palaeoecol 311:19–29.  https://doi.org/10.1016/j.palaeo.2011.07.010 CrossRefGoogle Scholar
  75. Mary PO, Solanki GS, Limboo D, Upadhaya K (1998) Observations on feeding and territorial behaviour of Indian rhino (Rhinoceros unicornis) in Kaziranga National Park, Assam, India. Tigerpaper 25:25–28Google Scholar
  76. Merceron G, Blondel C, Brunet M, Sen S, Solounias N, Viriot L, Heintz E (2004a) The Late Miocene paleoenvironment of Afghanistan as inferred from dental microwear in artiodactyls. Palaeogeogr Palaeoclimatol Palaeoecol 207:143–163CrossRefGoogle Scholar
  77. Merceron G, Viriot L, Blondel C (2004b) Tooth microwear pattern in roe deer (Capreolus capreolus L.) from Chizé (Western France) and relation to food composition. Small Rumin Res 53:125–132.  https://doi.org/10.1016/j.smallrumres.2003.10.002 CrossRefGoogle Scholar
  78. Merceron G, Escarguel G, Angibault J-M, Verheyden-Tixier H (2010) Can dental microwear textures record inter-individual dietary variations? PLoS One 5:e9542.  https://doi.org/10.1371/journal.pone.0009542 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Merceron G, Ramdarshan A, Blondel C, Boisserie JR, Brunetiere N, Francisco A, Gautier D, Milhet X, Novello A, Pret D (2016) Untangling the environmental from the dietary: dust does not matter. Proc R Soc Lond B 283:20161032.  https://doi.org/10.1098/rspb.2016.1032 CrossRefGoogle Scholar
  80. Metcalfe GTC (1961) Rhinoceros in Malaya and their future. Malayan Nat J Special Issue:183–193Google Scholar
  81. Mihlbachler MC, Beatty BL, Caldera-Siu A, Chan D, Lee R (2012) Error rates in dental microwear analysis using light microscopy. Palaeontol Electron 15:22.  https://doi.org/10.26879/298 CrossRefGoogle Scholar
  82. Mihlbachler MC, Campbell D, Ayoub M, Chen C, Ghani I (2016) Comparative dental microwear of ruminant and perissodactyl molars: implications for paleodietary analysis of rare and extinct ungulate clades. Paleobiology 42:98–116.  https://doi.org/10.1017/pab.2015.33 CrossRefGoogle Scholar
  83. Mihlbachler MC, Campbell D, Chen C, Ayoub M, Kaur P (2018) Microwear–mesowear congruence and mortality bias in rhinoceros mass-death assemblages. Paleobiology 44:131–154.  https://doi.org/10.1017/pab.2017.13 CrossRefGoogle Scholar
  84. Milliken T, Emslie RH, Talukdar B (2009) African and Asian rhinoceroses–status, conservation and trade. A report from the IUCN Species Survival Commission (IUCN/SSC) African and Asian Rhino Specialist Groups and TRAFFIC to the CITES Secretariat pursuant to Resolution Conf 9.14 (Rev. CoP14) and Decision 14.89. Report to CITES 15th meeting (Doha, March 2010), CoP 15 Doc.45.1A annex: 1–18Google Scholar
  85. Mukinya JG (1977) Feeding and drinking habitats of the black rhinoceros in Masai Mara Game Reserve. East Afr Wildl J 15:125–138CrossRefGoogle Scholar
  86. Muya SM, Oguge NO (2000) Effects of browse availability and quality on black rhino (Diceros bicornis michaeli Groves 1967) diet in Nairobi National Park, Kenya. Afr J Ecol 38:62–71CrossRefGoogle Scholar
  87. Owen-Smith NR (1988) Megaherbivores: the influence of very large body size on ecology. Cambridge University PressGoogle Scholar
  88. Percher AM, Romero A, Galbany J, Nsi Akoue G, Pérez-Pérez A, Charpentier MJE (2017) Buccal dental-microwear and dietary ecology in a free-ranging population of mandrills (Mandrillus sphinx) from southern Gabon. PLoS One 12:e0186870.  https://doi.org/10.1371/journal.pone.0186870 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Player IC, Feely JM (1960) A preliminary report on the square-lipped rhinoceros Ceratotherium simum simum. Lammergeyer 1:3–24Google Scholar
  90. Prothero DR, Guérin C, Manning E (1989) The history of the Rhinocerotoidea. In: Prothero DR, Schoch RM (eds) The evolution of Perissodactyls. Oxford University Press, New York, pp 321–340Google Scholar
  91. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
  92. Ramdarshan A, Blondel C, Gautier D, Surault J, Merceron G (2017) Overcoming sampling issues in dental tribology: insights from an experimentation on sheep. Palaeontol Electron 20:1–19.  https://doi.org/10.26879/762 CrossRefGoogle Scholar
  93. Rensberger JM, Koenigswald W v (1980) Functional and phylogenetic interpretation of enamel microstructure in rhinoceroses. Paleobiology 6:477–495CrossRefGoogle Scholar
  94. Rivals F, Takatsuki S, Albert RM, Macià L (2014) Bamboo feeding and tooth wear of three sika deer (Cervus nippon) populations from northern Japan. J Mammal 95:1043–1053CrossRefGoogle Scholar
  95. Rookmaaker K, Antoine P-O (2012) New maps representing the historical and recent distribution of the African species of rhinoceros: Diceros bicornis, Ceratotherium simum and Ceratotherium cottoni. Pachyderm 52:81–96Google Scholar
  96. Schenkel R, Schenkel-Hulliger L (1969) The Javan rhinoceros (Rh. sondaicus Desm.) in Udjung Kulon Nature Reserve. Its ecology and behavior. Acta Trop 26:97–135PubMedGoogle Scholar
  97. Schulz E, Calandra I, Kaiser TM (2013) Feeding ecology and chewing mechanics in hoofed mammals: 3D tribology of enamel wear. Wear 300:169–179.  https://doi.org/10.1016/j.wear.2013.01.115 CrossRefGoogle Scholar
  98. Scott JR (2012) Dental microwear texture analysis of extant African Bovidae. Mammalia 76:157–174.  https://doi.org/10.1515/mammalia-2011-0083 CrossRefGoogle Scholar
  99. Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A (2005) Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693–695.  https://doi.org/10.1038/nature03822 CrossRefPubMedGoogle Scholar
  100. Scott RS, Ungar PS, Bergstrom TS, Brown CA, Childs BE, Teaford MF, Walker A (2006) Dental microwear texture analysis: technical considerations. J Hum Evol 51:339–349.  https://doi.org/10.1016/j.jhevol.2006.04.006 CrossRefPubMedGoogle Scholar
  101. Scott RS, Teaford MF, Ungar PS (2012) Dental microwear texture and anthropoid diets. Am J Phys Anthropol 147:551–579.  https://doi.org/10.1002/ajpa.22007 CrossRefPubMedGoogle Scholar
  102. Smith GS, Nelson AB, Boggino EJ (1971) Digestibility of forages in vitro as affected by content of “silica.”. J Anim Sci 33:466–471CrossRefPubMedGoogle Scholar
  103. Tissier J, Becker D, Codrea V, Costeur L, Fărcaş C, Solomon A, Venczel M, Maridet O (2018) New data on Amynodontidae (Mammalia, Perissodactyla) from Eastern Europe: phylogenetic and palaeobiogeographic implications around the Eocene-Oligocene transition. PLoS One 13:e0193774.  https://doi.org/10.1371/journal.pone.0193774 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Tunstall T, Kock R, Vahala J, Diekhans M, Fiddes I, Armstrong J, Paten B, Ryder OA, Steiner CC (2018) Evaluating recovery potential of the northern white rhinoceros from cryopreserved somatic cells. Genome Res 28:780–788.  https://doi.org/10.1101/gr.227603.117 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Ungar PS, Scott JR, Steininger CM (2016) Dental microwear differences between eastern and southern African fossil bovids and hominins. S Afr J Sci 112:1–5.  https://doi.org/10.17159/sajs.2016/20150393 CrossRefGoogle Scholar
  106. Uno KT, Rivals F, Bibi F, Pante M, Njau J, de la Torre I (2018) Large mammal diets and paleoecology across the Oldowan–Acheulean transition at Olduvai Gorge, Tanzania from stable isotope and tooth wear analyses. J Hum Evol 120:76–91.  https://doi.org/10.1016/j.jhevol.2018.01.002 CrossRefPubMedGoogle Scholar
  107. van Gyseghem R (1984) Observations on the ecology and behaviour of the northern white rhinoceros (Ceratotherium simum cottoni). Z Säugetierkd 49:348–358Google Scholar
  108. van Lieverloo RJ, Schuiling BF, de Boer WF, Lent PC, de Jong CB, Brown D, Prins HHT (2009) A comparison of faecal analysis with backtracking to determine the diet composition and species preference of the black rhinoceros (Diceros bicornis minor). Eur J Wildl Res 55:505–515.  https://doi.org/10.1007/s10344-009-0264-5 CrossRefGoogle Scholar
  109. van Strien NJ (1986) The Sumatran rhinoceros Dicerorhinus sumatrensis (Fischer, 1814) in the Gunung Leuser National Park, Sumatra, Indonesia. Parey, HamburgGoogle Scholar
  110. Welker F, Smith GM, Hutson JM, Kindler L, Garcia-Moreno A, Villaluenga A, Turner E, Gaudzinski-Windheuser S (2017) Middle Pleistocene protein sequences from the rhinoceros genus Stephanorhinus and the phylogeny of extant and extinct Middle/Late Pleistocene Rhinocerotidae. PeerJ 5:e3033.  https://doi.org/10.7717/peerj.3033 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New YorkGoogle Scholar
  112. Willerslev E, Gilbert MTP, Binladen J, Ho SYW, Campos PF, Ratan A, Tomsho LP, da Fonseca RR, Sher A, Kuznetsova TV, Nowak-Kemp M, Roth TL, Miller W, Schuster SC (2009) Analysis of complete mitochondrial genomes from extinct and extant rhinoceroses reveals lack of phylogenetic resolution. BMC Evol Biol 9:95.  https://doi.org/10.1186/1471-2148-9-95 CrossRefPubMedPubMedCentralGoogle Scholar
  113. World Wildlife Fund (1982) Mystery of dead Javan rhinos remains. Malayan Nat 36:40Google Scholar
  114. Young TP, Evans MR (1993) Alpine vertebrates of Mount Kenya, with particular notes on the rock hyrax. J East Afr Nat Hist Soc Natl Mus 82:55–79Google Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2019

Authors and Affiliations

  1. 1.Institut des Sciences de l’Évolution, UMR5554, CNRS, IRDUniversité MontpellierMontpellierFrance
  2. 2.CollegnoItaly
  3. 3.Palevoprim UMR 7262, CNRSUniversité de PoitiersPoitiersFrance

Personalised recommendations