Hard plant tissues do not contribute meaningfully to dental microwear: evolutionary implications

Affiliations


Abstract

Reconstructing diet is critical to understanding hominin adaptations. Isotopic and functional morphological analyses of early hominins are compatible with consumption of hard foods, such as mechanically-protected seeds, but dental microwear analyses are not. The protective shells surrounding seeds are thought to induce complex enamel surface textures characterized by heavy pitting, but these are absent on the teeth of most early hominins. Here we report nanowear experiments showing that the hardest woody shells - the hardest tissues made by dicotyledonous plants - cause very minor damage to enamel but are themselves heavily abraded (worn) in the process. Thus, hard plant tissues do not regularly create pits on enamel surfaces despite high forces clearly being associated with their oral processing. We conclude that hard plant tissues barely influence microwear textures and the exploitation of seeds from graminoid plants such as grasses and sedges could have formed a critical element in the dietary ecology of hominins.

Conflict of interest statement

The authors declare no competing interests.


Figures


Similar articles

Dental microwear texture analysis shows within-species diet variability in fossil hominins.

Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A.Nature. 2005 Aug 4;436(7051):693-5. doi: 10.1038/nature03822.PMID: 16079844

The diet of the first Europeans from Atapuerca.

Pérez-Pérez A, Lozano M, Romero A, Martínez LM, Galbany J, Pinilla B, Estebaranz-Sánchez F, Bermúdez de Castro JM, Carbonell E, Arsuaga JL.Sci Rep. 2017 Feb 27;7:43319. doi: 10.1038/srep43319.PMID: 28240290 Free PMC article.

Dental evidence for the diets of Plio-Pleistocene hominins.

Ungar PS.Am J Phys Anthropol. 2011;146 Suppl 53:47-62. doi: 10.1002/ajpa.21610.PMID: 22101687 Review.

Brief communication: Dental microwear and diet of Homo naledi.

Ungar PS, Berger LR.Am J Phys Anthropol. 2018 May;166(1):228-235. doi: 10.1002/ajpa.23418. Epub 2018 Feb 5.PMID: 29399788

The diets of early hominins.

Ungar PS, Sponheimer M.Science. 2011 Oct 14;334(6053):190-3. doi: 10.1126/science.1207701.PMID: 21998380 Review.


Cited by

Changing perspectives on early hominin diets.

Teaford MF, Ungar PS, Grine FE.Proc Natl Acad Sci U S A. 2023 Feb 14;120(7):e2201421120. doi: 10.1073/pnas.2201421120. Epub 2023 Feb 6.PMID: 36745809

Biomimicking Nature-Inspired Design Structures-An Experimental and Simulation Approach Using Additive Manufacturing.

Patil AY, Hegde C, Savanur G, Kanakmood SM, Contractor AM, Shirashyad VB, Chivate RM, Kotturshettar BB, Mathad SN, Patil MB, Soudagar MEM, Fattah IMR.Biomimetics (Basel). 2022 Nov 3;7(4):186. doi: 10.3390/biomimetics7040186.PMID: 36412714 Free PMC article.

Mechanical compensation in the evolution of the early hominin feeding apparatus.

Ledogar JA, Senck S, Villmoare BA, Smith AL, Weber GW, Richmond BG, Dechow PC, Ross CF, Grosse IR, Wright BW, Wang Q, Byron C, Benazzi S, Carlson KJ, Carlson KB, Pryor McIntosh LC, van Casteren A, Strait DS.Proc Biol Sci. 2022 Jun 8;289(1976):20220711. doi: 10.1098/rspb.2022.0711. Epub 2022 Jun 15.PMID: 35703052

Macrowear effects of external quartz abrasives of different size and concentration in rabbits (Oryctolagus cuniculus).

Martin LF, Ackermans NL, Richter H, Kircher P, Hummel J, Codron D, Clauss M, Hatt JM.J Exp Zool B Mol Dev Evol. 2022 Dec;338(8):586-597. doi: 10.1002/jez.b.23104. Epub 2021 Nov 23.PMID: 34813148 Free PMC article.

Grit your teeth and chew your food: Implications of food material properties and abrasives for rates of dental microwear formation in laboratory Sapajus apella (Primates).

Teaford MF, Ross CF, Ungar PS, Vinyard CJ, Laird MF.Palaeogeogr Palaeoclimatol Palaeoecol. 2021 Dec 1;583:110644. doi: 10.1016/j.palaeo.2021.110644. Epub 2021 Sep 20.PMID: 34764513 Free PMC article.


KMEL References


References

  1.  
    1. Grine FE, Sponheimer M, Ungar PS, Lee-Thorp J, Teaford MF. Dental microwear and stable isotopes inform the paleoecology of extinct hominins. Am. J. Phys. Anthropol. 2012;148:285–317. doi: 10.1002/ajpa.22086. - DOI - PubMed
  2.  
    1. Sponheimer M, et al. Isotopic evidence of early hominin diets. Proc. Natl. Acad. Sci. 2013;110:10513–10518. doi: 10.1073/pnas.1222579110. - DOI
  3.  
    1. Ungar PS, Sponheimer M. The diets of early hominins. Science. 2011;334:190–193. doi: 10.1126/science.1207701. - DOI - PubMed
  4.  
    1. Dominy NJ, Vogel ER, Yeakel JD, Constantino P, Lucas PW. Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evol. Biol. 2008;35:159–175. doi: 10.1007/s11692-008-9026-7. - DOI
  5.  
    1. Smith AL, et al. The feeding biomechanics and dietary ecology of Paranthropus boisei. Anat. Rec. 2015;298:145–167. doi: 10.1002/ar.23073. - DOI - PMC - PubMed
  6.  
    1. Constantino PJ, et al. Tooth chipping can reveal the diet and bite forces of fossil hominins. Biol. Lett. 2010;6:826–829. doi: 10.1098/rsbl.2010.0304. - DOI - PMC - PubMed
  7.  
    1. Constantino PJ, et al. Adaptation to hard-object feeding in sea otters and hominins. J. Hum. Evol. 2011;61:89–96. doi: 10.1016/j.jhevol.2011.02.009. - DOI - PubMed
  8.  
    1. Constantino PJ, Lucas PW, Lee JJ-W, Lawn BR. The influence of fallback foods on great ape tooth enamel. Am. J. Phys. Anthropol. 2009;140:653–660. doi: 10.1002/ajpa.21096. - DOI - PubMed
  9.  
    1. Rabenold D, Pearson OM. Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei. PLoS One. 2011;6:e28379. doi: 10.1371/journal.pone.0028379. - DOI - PMC - PubMed
  10.  
    1. Berthaume M, et al. The effect of early hominin occlusal morphology on the fracturing of hard food items. Anat. Rec. 2010;293:594–606. doi: 10.1002/ar.21130. - DOI - PubMed
  11.  
    1. Kay RF. The functional adaptations of primate molar teeth. Am. J. Phys. Anthropol. 1975;43:195–216. doi: 10.1002/ajpa.1330430207. - DOI - PubMed
  12.  
    1. Lucas, P. W. Dental Functional Morphology: How TeethWork. (Cambridge University Press, 2004).
  13.  
    1. Scott RS, et al. Dental microwear texture analysis: technical considerations. J. Hum. Evol. 2006;51:339–349. doi: 10.1016/j.jhevol.2006.04.006. - DOI - PubMed
  14.  
    1. Henry AG, et al. The diet of Australopithecus sediba. Nature. 2012;487:90–93. doi: 10.1038/nature11185. - DOI - PubMed
  15.  
    1. Scott RS, Teaford MF, Ungar PS. Dental microwear texture and anthropoid diets. Am. J. Phys. Anthropol. 2012;147:551–579. doi: 10.1002/ajpa.22007. - DOI - PubMed
  16.  
    1. Lucas PW, et al. Mechanisms and causes of wear in tooth enamel: Implications for hominin diets. J. R. Soc. Interface. 2013;10:20120923. doi: 10.1098/rsif.2012.0923. - DOI - PMC - PubMed
  17.  
    1. van Casteren A, et al. Evidence that metallic proxies are unsuitable for assessing the mechanics of microwear formation and a new theory of the meaning of microwear. R. Soc. Open Sci. 2018;5:171699. doi: 10.1098/rsos.171699. - DOI - PMC - PubMed
  18.  
    1. Lucas PW, et al. Structure and scale of the mechanics of mammalian dental enamel viewed from an evolutionary perspective. Evol. Dev. 2016;18:54–61. doi: 10.1111/ede.12169. - DOI - PubMed
  19.  
    1. Lucas PW, et al. Evolutionary optimization of material properties of a tropical seed. J. R. Soc. Interface. 2011;9:34–42. doi: 10.1098/rsif.2011.0188. - DOI - PMC - PubMed
  20.  
    1. Atkins AG, Liu JH. Toughness and the transition between cutting and rubbing in abrasive contacts. Wear. 2007;262:146–159. doi: 10.1016/j.wear.2006.04.002. - DOI
  21.  
    1. Hua L-C, Brandt ET, Meullenet J-F, Zhou Z-R, Ungar PS. Technical note: An in vitro study of dental microwear formation using the BITE Master II chewing machine. Am. J. Phys. Anthropol. 2015;158:769–775. doi: 10.1002/ajpa.22823. - DOI - PubMed
  22.  
    1. Agrawal KR, Lucas PW, Bruce IC. The effects of food fragmentation index on mandibular closing angle in human mastication. Arch. Oral Biol. 2000;45:577–584. doi: 10.1016/S0003-9969(00)00019-4. - DOI - PubMed
  23.  
    1. Reed DA, Ross CF. The influence of food material properties on jaw kinematics in the primate, Cebus. Arch. Oral Biol. 2010;55:946–962. doi: 10.1016/j.archoralbio.2010.08.008. - DOI - PubMed
  24.  
    1. Veenendaal EM, Ernst WHO, Modise GS. Reproductive effort and phenology of seed production of savanna grasses with different growth form and life history. Vegetatio. 1996;123:91–100. doi: 10.1007/BF00044891. - DOI
  25.  
    1. Smil, V. Energy in Nature and Society: General Energetics of Complex Systems. (The MIT Press, 2008).
  26.  
    1. Pontzer H. The crown joules: energetics, ecology, and evolution in humans and other primates. Evol. Anthropol. 2017;26:12–24. doi: 10.1002/evan.21513. - DOI - PubMed
  27.  
    1. Froehle AW, Schoeninger MJ. Intraspecies variation in BMR does not affect estimates of early hominin total daily energy expenditure. Am. J. Phys. Anthropol. 2006;131:552–559. doi: 10.1002/ajpa.20475. - DOI - PubMed
  28.  
    1. Jarvey JC, Low BS, Pappano DJ, Bergman TJ, Beehner JC. Graminivory and fallback foods: annual diet profile of geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. Int. J. Primatol. 2018;39:105–126. doi: 10.1007/s10764-018-0018-x. - DOI
  29.  
    1. Post DG. Feeding behavior of yellow baboons (Papio cynocephalusin) the Amboseli National Park, Kenya. Int. J. Primatol. 1982;3:403–430. doi: 10.1007/BF02693741. - DOI
  30.  
    1. Jolly CJ. The Seed-Eaters: A new model of hominid differentiation based on a baboon analogy. Man. 2009;5:5–26. doi: 10.2307/2798801. - DOI
  31.  
    1. Lee JJ-W, et al. Properties of tooth enamel in great apes. Acta Biomater. 2010;6:4560–4565. doi: 10.1016/j.actbio.2010.07.023. - DOI - PubMed
  32.  
    1. Lucas PW, Lowrey TK, Pereiras BP, Sarafis V, Kuhn W. The Ecology of Mezzetia leptopoda (Hk. f. et Thoms.) Oliv. (Annonaceae) seeds as viewed from a mechanical prospective. Funct. Ecol. 1991;5:545–553. doi: 10.2307/2389637. - DOI
  33.  
    1. Lucas PW, et al. The role of dust, grit and phytoliths in tooth wear. Ann. Zool. Fennici. 2014;51:143–152. doi: 10.5735/086.051.0215. - DOI