Advertisement

International Journal of Primatology

, Volume 33, Issue 3, pp 598–610 | Cite as

Measuring the Toughness of Primate Foods and its Ecological Value

  • Peter W. Lucas
  • Lynn Copes
  • Paul J. Constantino
  • Erin R. Vogel
  • Janine Chalk
  • Mauricio Talebi
  • Mariana Landis
  • Mark Wagner
Article

Abstract

The mechanical properties of plant foods play an important role in the feeding process, being one of many criteria for food acceptance or rejection by primates. One of the simplest justifications for this statement is the general finding that primates tend to avoid foods with high fiber. Although fiber is largely tasteless, odorless, and colorless, it imparts texture, a sensation in the mouth related to the physical properties of foods. All primates encounter such mechanical resistance when they bite into plant food, and studies on humans show that an incisal bite facilitates quick oral assessment of a property called toughness. Thus, it is feasible that primates make similar assessments of quality in this manner. Here, we review methods of measuring the toughness of primate foods, which can be used either for making general surveys of the properties of foods available to primates or for establishing the mechanisms that protect these foods from the evolved form of the dentition.

Keywords

Fiber content Methods Plant cell walls Primate feeding toughness 

References

  1. Agrawal, K. R., & Lucas, P. W. (2003). Mechanics of the first bite. Proceedings of the Royal Society B, 270, 1277–1282.PubMedCrossRefGoogle Scholar
  2. Agrawal, K. R., Ang, K. Y., Sui, Z., Tan, H. T. W., & Lucas, P. W. (2008). Methods of ingestion and incisal designs. In J. D. Irish & G. C. Nelson (Eds.), Technique and application in dental anthropology (pp. 349–363). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  3. Ang, K. Y., Lucas, P. W., & Tan, H. T. W. (2006). Incisal orientation and biting efficiency. Journal of Human Evolution, 50, 663–672.PubMedCrossRefGoogle Scholar
  4. Ang, K. Y., Lucas, P. W., & Tan, H. T. W. (2008). A novel way of measuring the fracture toughness of leaves and other thin films using a single inclined razor blade. The New Phytologist, 177, 830–837.PubMedCrossRefGoogle Scholar
  5. Aranwela, N., Sanson, G., & Read, J. (1999). Methods of assessing leaf-fracture properties. The New Phytologist, 144, 369–383.CrossRefGoogle Scholar
  6. Ashby, M. F., Evans, A. G., Fleck, N. A., Hutchinson, J. W., Wadley, H. N. G., & Gibson, L. G. (2000). Metal foams: A design guide. Boston: Butterworth-Heinemann.Google Scholar
  7. Atkins, A. G., & Mai, Y.-W. (1979). On the guillotining of materials. Journal of Materials Science, 14, 2747–2754.CrossRefGoogle Scholar
  8. Atkins, A. G., & Mai, Y.-W. (1985). Elastic and plastic fracture. Chichester: Ellis Horwood.Google Scholar
  9. Byrne, R. W., & Byrne, J. M. E. (1993). Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): Variability and standardization. American Journal of Primatology, 31, 241–261.CrossRefGoogle Scholar
  10. Chai, H., Lee, J. J.-W., Constantino, P., Lucas, P. W., & Lawn, B. R. (2009). Remarkable resilience of teeth. Proceedings of the National Academy of Sciences of the USA, 106, 7289–7293.PubMedCrossRefGoogle Scholar
  11. Chapman, C. A., Chapman, L. J., Naughton-Treves, L., Lawes, M. J., & McDowell, L. R. (2004). Predicting folivorous primate abundance: Validation of a nutritional model. American Journal of Primatology, 65, 55–69.CrossRefGoogle Scholar
  12. Choong, M. F., Lucas, P. W., Ong, J. Y. S., Pereira, B. P., Tan, H. T. W., & Turner, I. M. (1992). Leaf fracture toughness and sclerophylly: Their correlations and ecological implications. The New Phytologist, 121, 597–610.CrossRefGoogle Scholar
  13. Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical rainforest. Ecological Monographs, 53, 209–233.CrossRefGoogle Scholar
  14. Coley, P. D., & Kursar, T. A. (1996). Anti-herbivore defenses of young tropical leaves: physiological constraints and ecological trade-offs. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical forest plant ecophysiology (pp. 305–336). New York: Chapman & Hall.CrossRefGoogle Scholar
  15. Constantino, P. J., Markham, K. & Lucas, P. W. (in press). Tooth chipping as a tool to reconstruct primate diets. International Journal of Primatology. Google Scholar
  16. Deane, A. (2009). First contact: Understanding the relationship between hominoid incisor curvature and diet. Journal of Human Evolution, 56, 263–274.PubMedCrossRefGoogle Scholar
  17. Dominy, N. J. (2004). Color as an indicator of food quality to anthropoid primates: Ecological evidence and an evolutionary scenario. In C. Ross & R. F. Kay (Eds.), Anthropoid origins: New visions (pp. 615–644). New York: Kluwer Academic.CrossRefGoogle Scholar
  18. Dominy, N. J., Vogel, E. R., Yeakel, J. D., Constantino, P., & Lucas, P. W. (2008). Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evolutionary Biology, 35, 159–175.CrossRefGoogle Scholar
  19. Edwards, C., Read, J., & Sanson, G. (2000). Characterising sclerophylly: Some mechanical properties of leaves from heath and forest. Oecologia, 123, 158–167.CrossRefGoogle Scholar
  20. Elgart-Berry, A. (2004). Fracture toughness of mountain gorilla (Gorilla gorilla beringei) food plants. American Journal of Primatology, 62, 275–285.PubMedCrossRefGoogle Scholar
  21. Evans, A. G. (1990). Perspective on the development of high-toughness ceramics. Journal of the American Ceramic Society, 73, 187–206.CrossRefGoogle Scholar
  22. Ganzhorn, J. U. (1992). Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia, 91, 540–547.CrossRefGoogle Scholar
  23. Gibson, L. J., Ashby, M. F., & Easterling, K. E. (1988). The structure and mechanics of the iris leaf. Journal of Materials Science, 23, 3041–3048.CrossRefGoogle Scholar
  24. Goh, S. M., Charalambides, M. N., & Williams, J. G. (2003). Mechanical properties and sensory texture assessment of cheeses. Journal of Texture Studies, 34, 181–201.CrossRefGoogle Scholar
  25. Goh, S. M., Charalambides, M. N., & Williams, J. G. (2005). On the mechanics of wire cutting of cheese. Engineering Fracture Mechanics, 72, 931–946.CrossRefGoogle Scholar
  26. Gordon, J. E. (1978). Structures: Or why things don't fall down. London: Penguin.CrossRefGoogle Scholar
  27. Gordon, J. E., & Jeronimidis, G. (1974). Work of fracture. Nature, 252, 116.CrossRefGoogle Scholar
  28. Henry, D., Macmillan, R., & Simpson, R. (1996). Measurement of the shear and tensile fracture properties of leaves of pasture grasses. Australian Journal of Agricultural Research, 47, 587–603.CrossRefGoogle Scholar
  29. Hill, D. A., & Lucas, P. W. (1996). Toughness and fiber content of major leaf foods of wild Japanese macaques (Macaca fuscata yakui) in Yakushima. American Journal of Primatology, 38, 221–231.CrossRefGoogle Scholar
  30. Hylander, W. L., Johnson, K. R., & Crompton, A. W. (1992). Muscle force recruitment and biomechanical modelling: An analysis of masseter muscle function during mastication in Macaca fascicularis. American Journal of Physical Anthropology, 88, 365–387.PubMedCrossRefGoogle Scholar
  31. Jeronimidis, G. (1980). The fracture behavior of wood and the relations between toughness and morphology. Proceedings of the Royal Society B: Biological Sciences, 208, 447–460.CrossRefGoogle Scholar
  32. Kamyab, I., Chakrabarti, S., & Williams, J. G. (1998). Cutting cheese with wire. Journal of Materials Science, 33, 2763–2770.CrossRefGoogle Scholar
  33. Kay, R. F. (1975). The functional adaptations of primate molar teeth. American Journal of Physical Anthropology, 42, 195–215.CrossRefGoogle Scholar
  34. Keckes, K., Burgert, I., Frühmann, K., Müller, M., Kölln, K., Hamilton, M., et al. (2003). Cell-wall recovery after irreversible deformation of wood. Nature Materials, 2, 810–813.PubMedCrossRefGoogle Scholar
  35. Khan, A. A., & Vincent, J. F. V. (1993). Anisotropy in the fracture properties of apple flesh as investigated by crack-opening tests. Journal of Materials Science, 28, 45–51.CrossRefGoogle Scholar
  36. Khan, A. A., & Vincent, J. F. V. (1996). Mechanical damage induced by controlled freezing in apple and potato. Journal of Texture Studies, 27, 143–157.CrossRefGoogle Scholar
  37. Lawn, B. R. (1993). Fracture of brittle solids (2nd ed.). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  38. Lucas, P. W. (2004). Dental functional morphology. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  39. Lucas, P. W., & Pereira, B. (1990). Estimation of the fracture toughness of leaves. Functional Ecology, 4, 819–822.CrossRefGoogle Scholar
  40. Lucas, P. W., Choong, M. F., Tan, H. T. W., Turner, I. M., & Berrick, A. J. (1991). The fracture toughness of the leaf of the dicotyledon Calophyllum inophyllum L. (Guttiferae). Philosophical Transactions of the Royal Society B: Biological Sciences, 334, 95–106.CrossRefGoogle Scholar
  41. Lucas, P. W., Tan, H. T. W., & Cheng, P. Y. (1997). The toughness of secondary cell wall and woody tissue. Philosophical Transactions of the Royal Society B: Biological Sciences, 352, 341–352.CrossRefGoogle Scholar
  42. Lucas, P. W., Turner, I. M., Dominy, N. J., & Yamashita, N. (2000). Mechanical defences to herbivory. Annals of Botany, 86, 913–920.CrossRefGoogle Scholar
  43. Lucas, P. W., Constantino, P., Wood, B. A., & Lawn, B. R. (2008). Dental enamel as a dietary indicator in mammals. Bioessays, 30, 374–285.PubMedCrossRefGoogle Scholar
  44. Lucas, P. W., Constantino, P. J., Chalk, J., Ziscovici, C., Wright, B. W., Fragaszy, D. M., et al. (2009). Indentation as a technique to assess the mechanical properties of fallback foods. American Journal of Physical Anthropology, 140, 643–652.PubMedCrossRefGoogle Scholar
  45. Lucas, P. W., Osorio, D., Yamashita, N., Prinz, J. F., Dominy, N. J., & Darvell, B. W. (2011). Dietary analysis I: Physics. In J. Setchell & D. Curtis (Eds.), Field and laboratory methods in primatology (2nd ed., pp. 237–254). Cambridge, UK: Cambridge University Press.Google Scholar
  46. Milton, K. (1991). Pectin content of neotropical plant parts. Biotropica, 23, 90–92.CrossRefGoogle Scholar
  47. Oates, J. F., Whitesides, G. H., Davies, A. G., Waterman, P. G., Green, S. M., Dasilva, G., et al. (1990). Determinants of variation in tropical forest primate biomass: New evidence from West Africa. Ecology, 71, 328–343.CrossRefGoogle Scholar
  48. Onoda, Y., Schieving, F., & Anten, N. P. R. (2008). Effects of light and nutrient availability on leaf mechanical properties of Plantago major: A conceptual approach. Annals of Botany, 101, 727–736.PubMedCrossRefGoogle Scholar
  49. Onoda, Y., et al. (2011). Global patterns of leaf mechanical properties. Ecology Letters, 14, 301–312.PubMedCrossRefGoogle Scholar
  50. Osborn, J. W., Baragar, F. A., & Grey, P. (1987). The functional advantage of proclined incisors in man. In D. E. Russell, J. P. Santoro & D. Sigognean-Russell (Eds.), Teeth revisited: Proceedings of VII International Symposium on Dental Morphology. Memoirs du Musee National d’Histoire Naturelle, Paris (Serie C), 53, 445–458.Google Scholar
  51. Paphangkorakit, J., & Osborn, J. W. (1997). The effect of pressure on a maximum incisal bite force in a man. Archives of Oral Biology, 42, 11–17.PubMedCrossRefGoogle Scholar
  52. Paphangkorakit, J., & Osborn, J. W. (1998). Effects on human maximum bite force of biting on a softer or harder object. Archives of Oral Biology, 43, 833–839.PubMedCrossRefGoogle Scholar
  53. Read, J., & Sanson, G. D. (2003). Characterizing sclerophylly: The mechanical properties of a diverse range of leaf types. The New Phytologist, 160, 81–99.CrossRefGoogle Scholar
  54. Sanson, G. (2006). The biomechanics of browsing and grazing. American Journal of Botany, 93, 1531–1545.PubMedCrossRefGoogle Scholar
  55. Sui, Z. Q., Agrawal, K. R., Corke, H., & Lucas, P. W. (2006). Biting efficiency in relation to incisal angulation. Archives of Oral Biology, 51, 491–497.PubMedCrossRefGoogle Scholar
  56. Teaford, M. F., Lucas, P. W., Ungar, P. S., & Glander, K. E. (2006). Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata). American Journal of Physical Anthropology, 129, 99–104.PubMedCrossRefGoogle Scholar
  57. Tonooka, R. (2001). Leaf-folding behavior for drinking water by wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea. Animal Cognition, 4, 325–334.CrossRefGoogle Scholar
  58. van Soest, P. J. (1994). Nutritional ecology of the ruminant. Ithaca, NY: Cornell University Press.Google Scholar
  59. Vincent, J. F. V. (1990). Fracture in plants. Advances in Botanical Research, 17, 235–282.CrossRefGoogle Scholar
  60. Vincent, J. F. V. (1992). Biomechanics—materials: A practical approach. Oxford: IRL Press.Google Scholar
  61. Vincent, J. F. V., Jeronimidis, G., Khan, A. A., & Luyten, H. (1991). The wedge fracture test: A new method for measurement of food texture. Journal of Texture Studies, 22, 45–57.CrossRefGoogle Scholar
  62. Vincent, J. F. V., Saunders, D. E. J., & Beyts, P. (2002). The use of stress intensity factor to quantify “hardness” and “crunchiness” objectively. Journal of Texture Studies, 33, 149–159.CrossRefGoogle Scholar
  63. Vogel, E. R., van Woerden, J. T., Lucas, P. W., Utami Atmoko, S. S., & van Schaik, C. P. (2008). Functional ecology and evolution of hominoid enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. Journal of Human Evolution, 55, 60–74.PubMedCrossRefGoogle Scholar
  64. Vogel, E. R., Haag, L., Parker, G. G., Mitra-Setia, T., van Schaik, C. P., & Dominy, N. (2009). Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. American Journal of Physical Anthropology, 140, 716–726.PubMedCrossRefGoogle Scholar
  65. Williams, S. H., Wright, B. W., van den Truong, Daubert, C. R., & Vinyard, C. J. (2005). Mechanical properties of foods used in experimental studies of primate masticatory function. American Journal of Primatology, 67, 329–346.PubMedCrossRefGoogle Scholar
  66. Wrangham, R., Conklin, N. L., Chapman, C. A., & Hunt, K. D. (1991). The significance of fibrous foods for Kibale Forest chimpanzees. Philosophical Transactions of the Royal Society B: Biological Sciences, 334, 171–178.CrossRefGoogle Scholar
  67. Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949–970.CrossRefGoogle Scholar
  68. Wright, B. W. (2005). Craniodental biomechanics and dietary toughness in the genus Cebus. Journal of Human Evolution, 48, 473–492.PubMedCrossRefGoogle Scholar
  69. Wright, I. J., & Cannon, K. (2001). Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Functional Ecology, 15, 351–359.CrossRefGoogle Scholar
  70. Wright, W., & Illius, A. W. (1995). A comparative study of the fracture properties of 5 grasses. Functional Ecology, 9, 269–278.CrossRefGoogle Scholar
  71. Wright, B. W., Ulibarri, L., O’Brien, J., Sadler, B., Prodhan, R., Covert, H. H., et al. (2008). It’s tough out there: Variation in the toughness of ingested leaves and feeding behavior among four Colobinae in Vietnam. International Journal of Primatology, 29, 1455–1466.CrossRefGoogle Scholar
  72. Yamashita, N. (2003). Food procurement and tooth use in two sympatric lemur species. American Journal of Physical Anthropology, 121, 125–133.PubMedCrossRefGoogle Scholar
  73. Yamashita, N., Vinyard, C. J., & Tan, C. L. (2009). Primate food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 139, 368–291.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Peter W. Lucas
    • 1
  • Lynn Copes
    • 2
  • Paul J. Constantino
    • 3
  • Erin R. Vogel
    • 4
  • Janine Chalk
    • 5
  • Mauricio Talebi
    • 6
  • Mariana Landis
    • 7
  • Mark Wagner
    • 8
  1. 1.Department of Bioclinical Sciences, Faculty of DentistryKuwait UniversitySafatKuwait
  2. 2.School of Human Evolution and Social ChangeArizona State UniversityTempeUSA
  3. 3.Department of Biological SciencesCollege of ScienceHuntingtonUSA
  4. 4.Department of AnthropologyRutgers, The State University of New JerseyNew BrunswickUSA
  5. 5.Center for the Advanced Study of Hominid Paleobiology, Department of AnthropologyThe George Washington UniversityWashingtonUSA
  6. 6.Departamento de Ciencias BiologicasUniversidade Federal de São PauloDiademaBrazil
  7. 7.Pró-Muriqui Association, Parque Estadual Carlos BotelhoSão Miguel ArcanjoBrazil
  8. 8.School of Engineering and Applied ScienceThe George Washington UniversityWashingtonUSA

Personalised recommendations