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

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.

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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 University

  2. Ammann H (1985) Contributions to the ecology and sociology of the Javan rhinoceros (Rhinoceros sondaicus Desm., 1822). Inaugural Dissertation, University of Basel, Switzerland

  3. Antoine P-O (2002) Phylogénie et évolution des Elasmotheriina (Mammalia, Rhinocerotidae). Mém Mus natl Hist nat 188:1–359

    Google Scholar 

  4. Antoine P-O (2012) Pleistocene and Holocene rhinocerotids (Mammalia, Perissodactyla) from the Indochinese Peninsula. C R Palevol 11:159–168

    Article  Google 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

    Article  Google 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 Publishing

  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 338:172–179

    Article  CAS  Google 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

    Article  Google 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 University

  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

    Article  Google 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 221:153–174

    Article  Google 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

    Article  Google 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

    Article  CAS  Google 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 508–512

  15. Buk KG (2004) Diet selection of and habitat suitability for black rhino in Augrabies Falls National Park, South Africa. Master Thesis, University of Copenhagen

  16. Buk KG, Knight MH (2010) Seasonal diet preferences of black rhinoceros in three arid South African National Parks. Afr J Ecol 48:1064–1075

    Article  Google 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

    Article  Google 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

    Article  CAS  PubMed  PubMed Central  Google 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

    Article  Google 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

    Article  CAS  PubMed  Google 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

    Article  Google 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

    Article  Google Scholar 

  23. Coetzee CG (1970) The distribution of mammals in the Namib Desert and adjoining inland escarpment. Scient Pap Namib Desert Res Stn 40:23–36

  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 18:1043–1045

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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 Stellenbosch

  31. Emslie RH (2008) Rhino population sizes and trends. Pachyderm 44:88–95

    Google 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 65–81

  34. Evans GH (1904) The Asiatic two-horned rhinoceros (Rhinoceros sumatrensis). J Bombay Nat Hist Soc 16:160–161

    Google 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 Norway

  36. Flynn RW (1981) Distribution, ecology & conservation of the Sumatran rhinoceros in Malaysia. Prog Rep 1–33

  37. Fortelius M (1985) Ungulate cheek teeth : developmental, functional and evolutionary interrelations. Acta Zool Fenn 180:1–76

    Google Scholar 

  38. Fox J and Weisberg S (2011) An {R} Companion to Applied Regression, 3rd edn.Sage Publications

  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

    Article  Google Scholar 

  40. Goddard J (1968) Food preferences of two black rhinoceros populations. East Afr Wildl J 6:1–18

    Article  Google 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

    Article  Google Scholar 

  42. Gordon IJ, Prins HHT (2008) The ecology of browsing and grazing. Springer, Heidelberg

    Google 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

    Article  Google Scholar 

  45. Groves CP, Leslie DM (2011) Rhinoceros sondaicus (Perissodactyla: Rhinocerotidae). Mamm Species 43:190–208. https://doi.org/10.1644/887.1

    Article  Google 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:e9703

    Article  CAS  PubMed  PubMed Central  Google 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 79:1–1184

    Google 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 25:63–82

    Article  Google 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

    Article  Google 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

    Article  Google Scholar 

  51. Heller E (1913) The white rhinoceros: with thirty-one plates. Smithson Misc Collect 61:i, 1–56, pls. 1–31

  52. Hillman-Smith AKK, Groves CP (1994) Diceros bicornis. Mamm Species 455:1–8. https://doi.org/10.2307/3504292

    Article  Google 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

    Article  Google Scholar 

  54. Hitchins PM (1978) Age determination of the black rhinoceros (Diceros bicornis Linn.) in Zululand. S Afr J Wildl Res 8:71–80

    Google 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

    Article  PubMed  Google Scholar 

  56. Hoogerwerf A (1970) Udjung Kulon: the land of the last Javan rhinoceros. Brill, Leiden

    Google 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

    Article  Google 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

    Article  Google 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 1:5–53

    Google 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

    Article  Google 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

    Article  Google 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 43:34–46

    Article  Google Scholar 

  63. Kingdon J, Hoffmann M (2013) Mammals of Africa, carnivores, pangolins, equids and rhinoceroses, V. Bloomsbury Publishing, London

    Google 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 56:11–32

    Article  Google 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

    Article  Google Scholar 

  66. Krumbiegel I (1960) Die asiatischen Nashorne (Dicerorhinus Gloger und Rhinoceros Linné). Säugetierk Mitt 8:12–20

    Google 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

    Article  Google Scholar 

  68. Laurie WA, Lang EM, Groves CP (1983) Rhinoceros unicornis. Mamm Species 211:1–6. https://doi.org/10.2307/3504002

    Article  Google 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 33:1–59

    Google 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

    Article  PubMed  Google 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 15:35–54

    Google 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, London

    Google 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 319–334

    Google 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

    Article  Google 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 25:25–28

    Google 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 207:143–163

    Article  Google 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

    Article  Google 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

    Article  CAS  PubMed  PubMed Central  Google 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

    Article  CAS  Google Scholar 

  80. Metcalfe GTC (1961) Rhinoceros in Malaya and their future. Malayan Nat J Special Issue:183–193

  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

    Article  Google 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

    Article  Google 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

    Article  Google 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: 1–18

  85. Mukinya JG (1977) Feeding and drinking habitats of the black rhinoceros in Masai Mara Game Reserve. East Afr Wildl J 15:125–138

    Article  Google 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 38:62–71

    Article  Google Scholar 

  87. Owen-Smith NR (1988) Megaherbivores: the influence of very large body size on ecology. Cambridge University Press

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Player IC, Feely JM (1960) A preliminary report on the square-lipped rhinoceros Ceratotherium simum simum. Lammergeyer 1:3–24

    Google 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 321–340

    Google 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

    Article  Google Scholar 

  93. Rensberger JM, Koenigswald W v (1980) Functional and phylogenetic interpretation of enamel microstructure in rhinoceroses. Paleobiology 6:477–495

    Article  Google 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 95:1043–1053

    Article  Google 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 52:81–96

    Google 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 26:97–135

    CAS  PubMed  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  CAS  PubMed  Google 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

    Article  PubMed  Google 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

    Article  PubMed  Google Scholar 

  102. Smith GS, Nelson AB, Boggino EJ (1971) Digestibility of forages in vitro as affected by content of “silica.”. J Anim Sci 33:466–471

    Article  CAS  PubMed  Google 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

    Article  CAS  PubMed  PubMed Central  Google 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

    Article  CAS  PubMed  PubMed Central  Google 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

    Article  Google 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

    Article  PubMed  Google Scholar 

  107. van Gyseghem R (1984) Observations on the ecology and behaviour of the northern white rhinoceros (Ceratotherium simum cottoni). Z Säugetierkd 49:348–358

    Google 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

    Article  Google Scholar 

  109. van Strien NJ (1986) The Sumatran rhinoceros Dicerorhinus sumatrensis (Fischer, 1814) in the Gunung Leuser National Park, Sumatra, Indonesia. Parey, Hamburg

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. World Wildlife Fund (1982) Mystery of dead Javan rhinos remains. Malayan Nat 36:40

    Google 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 82:55–79

    Google Scholar 

Download references

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.

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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.

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Correspondence to Manon Hullot.

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Hullot, M., Antoine, P., Ballatore, M. et al. Dental microwear textures and dietary preferences of extant rhinoceroses (Perissodactyla, Mammalia). Mamm Res 64, 397–409 (2019). https://doi.org/10.1007/s13364-019-00427-4

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Keywords

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