Telemetry System for Assessing Jaw-Muscle Function in Free-ranging Primates

Abstract

In vivo laboratory-based studies describing jaw-muscle activity and mandibular bone strain during mastication provide the empirical basis for most evolutionary hypotheses linking primate masticatory apparatus form to diet. However, the laboratory data pose a potential problem for testing predictions of these hypotheses because estimates of masticatory function and performance recorded in the laboratory may lack the appropriate ecological context for understanding adaptation and evolution. For example, in laboratory studies researchers elicit rhythmic chewing using foods that may differ significantly from the diets of wild primates. Because the textural and mechanical properties of foods influence jaw-muscle activity and the resulting strains, chewing behaviors studied in the laboratory may not adequately reflect chewing behaviors of primates feeding in their natural habitats. To circumvent this limitation of laboratory-based studies of primate mastication, we developed a system for recording jaw-muscle electromyograms (EMGs) from free-ranging primates so that researchers can conduct studies of primate jaw-muscle function in vivo in the field. We used the system to record jaw-muscle EMGs from mantled howlers (Alouatta palliata) at Hacienda La Pacifica, Costa Rica. These are the first EMGs recorded from a noncaptive primate feeding in its natural habitat. Further refinements of the system will allow long-term EMG data collection so that researchers can correlate jaw-muscle function with food mechanical properties and behavioral observations. In addition to furthering understanding of primate feeding biology, our work will foster improved adaptive hypotheses explaining the evolution of primate jaw form.

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References

  1. Agrawal, K. R., Lucas, P. W., Bruce, I. C., & Prinz, J. F. (1998). Food properties that influence neuromuscular activity during human mastication. Journal of Dental Research, 77, 1931–1938.

    PubMed  CAS  Google Scholar 

  2. Bock, W. J. (1980). The definition and recognition of biological adaptation. American Zoologist, 20, 217–227.

    Google Scholar 

  3. Bock, W. J., & von Wahlert, G. (1965). Adaptation and the form-function complex. Evolution; International Journal of Organic Evolution, 19, 269–299. doi:10.2307/2406439.

    Google Scholar 

  4. Bouvier, M. (1986). A biomechanical analysis of mandibular scaling in Old World monkeys. American Journal of Physical Anthropology, 69, 473–482. doi:10.1002/ajpa.1330690406.

    Article  Google Scholar 

  5. Bouvier, M., & Hylander, W. L. (1981). Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). Journal of Morphology, 167, 1–12. doi:10.1002/jmor.1051670102.

    PubMed  Article  CAS  Google Scholar 

  6. Daegling, D. J. (1993). The relationship of in vivo bone strain to mandibular corpus morphology in Macaca fascicularis. Journal of Human Evolution, 25, 247–269. doi:10.1006/jhev.1993.1048.

    Article  Google Scholar 

  7. Daegling, D. J. (2001). Biomechanical scaling of the hominoid mandibular symphysis. Journal of Morphology, 250, 12–23. doi:10.1002/jmor.1055.

    PubMed  Article  CAS  Google Scholar 

  8. Elgart-Berry, A. (2004). Fracture toughness of mountain gorilla (Gorilla gorilla beringei) food plants. American Journal of Primatology, 62, 275–285. doi:10.1002/ajp.20021.

    PubMed  Article  Google Scholar 

  9. Foster, K. D., Woda, A., & Peyron, M. A. (2006). Effect of texture of plastic and elastic model foods on the parameters of mastication. Journal of Neurophysiology, 95, 3469–3479. doi:10.1152/jn.01003.2005.

    PubMed  Article  CAS  Google Scholar 

  10. Glander, K. E. (2006). Average body weight for mantled howling monkeys (Alouatta pallilata): An assessment of average values and variability. In A. Estrada, P. A. Garber, M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates (pp. 247–263). New York: Springer.

    Google Scholar 

  11. Glander, K. E., Fedigan, L. M., Fedigan, L., & Chapman, C. (1991). Field methods for capture and measurement of three monkey species in Costa Rica. Folia Primatologica, 57, 70–82.

    Article  CAS  Google Scholar 

  12. Gursky, S. (1998). Effects of radio transmitter weight on a small nocturnal primate. American Journal of Primatology, 46, 145–155. doi:10.1002/(SICI)1098-2345(1998)46:2<145::AID-AJP4>3.0.CO;2-W.

    PubMed  Article  CAS  Google Scholar 

  13. Horio, T., & Kawamura, Y. (1989). Effects of texture of food on chewing patterns in the human subject. Journal of Oral Rehabilitation, 16, 177–183. doi:10.1111/j.1365-2842.1989.tb01331.x.

    PubMed  Article  CAS  Google Scholar 

  14. Hylander, W. L. (1977). In vivo bone strain in the mandible of Galago crassicaudatus. American Journal of Physical Anthropology, 46, 309–326. doi:10.1002/ajpa.1330460212.

    PubMed  Article  CAS  Google Scholar 

  15. Hylander, W. L. (1979a). Functional significance of primate mandibular form. Journal of Morphology, 160, 223–240. doi:10.1002/jmor.1051600208.

    PubMed  Article  CAS  Google Scholar 

  16. Hylander, W. L. (1979b). Mandibular function in Galago crassicaudatus and Macaca fascicularis: an in vivo approach to stress analysis of the mandible. Journal of Morphology, 159, 253–296. doi:10.1002/jmor.1051590208.

    PubMed  Article  CAS  Google Scholar 

  17. Hylander, W. L. (1984). Stress and strain in the mandibular symphysis of primates: a test of competing hypotheses. American Journal of Physical Anthropology, 64, 1–46. doi:10.1002/ajpa.1330640102.

    PubMed  Article  CAS  Google Scholar 

  18. Hylander, W. L. (1985). Mandibular function and biomechanical stress and scaling. American Zoologist, 25, 315–330.

    Google Scholar 

  19. Hylander, W. L., & Johnson, K. R. (1994). Jaw muscle function and wishboning of the mandible during mastication in macaques and baboons. American Journal of Physical Anthropology, 94, 523–547. doi:10.1002/ajpa.1330940407.

    PubMed  Article  CAS  Google Scholar 

  20. Hylander, W. L., Johnson, K. R., & Crompton, A. W. (1987). Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. American Journal of Physical Anthropology, 72, 287–314. doi:10.1002/ajpa.1330720304.

    PubMed  Article  CAS  Google Scholar 

  21. Hylander, W. L., Johnson, K. R., & Crompton, A. W. (1992). Muscle force recruitment and biomechanical modeling: an analysis of masseter muscle function during mastication in Macaca fascicularis. American Journal of Physical Anthropology, 88, 365–387. doi:10.1002/ajpa.1330880309.

    PubMed  Article  CAS  Google Scholar 

  22. Hylander, W. L., Ravosa, M. J., Ross, C. F., & Johnson, K. R. (1998). Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force. American Journal of Physical Anthropology, 107, 257–271. doi:10.1002/(SICI)1096-8644(199811)107:3<257::AID-AJPA3>3.0.CO;2-6.

    PubMed  Article  CAS  Google Scholar 

  23. Hylander, W. L., Ravosa, M. J., Ross, C. F., Wall, C. E., & Johnson, K. R. (2000). Symphyseal fusion and jaw-adductor muscle force: an EMG study. American Journal of Physical Anthropology, 112, 469–492. doi:10.1002/1096-8644(200008)112:4<469::AID-AJPA5>3.0.CO;2-V.

    PubMed  Article  CAS  Google Scholar 

  24. Hylander, W. L., Wall, C. E., Vinyard, C. J., Ross, C., Ravosa, M. R., Williams, S. H., et al. (2005). Temporalis function in anthropoids and strepsirrhines: an EMG study. American Journal of Physical Anthropology, 128, 35–56. doi:10.1002/ajpa.20058.

    PubMed  Article  Google Scholar 

  25. Kinzey, W. G., & Norconk, M. A. (1990). Hardness as a basis of fruit choice in two sympatric primates. American Journal of Physical Anthropology, 81, 5–15. doi:10.1002/ajpa.1330810103.

    PubMed  Article  CAS  Google Scholar 

  26. Kinzey, W. G., & Norconk, M. A. (1993). Physical and chemical properties of fruits and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. International Journal of Primatology, 14, 207–226. doi:10.1007/BF02192632.

    Article  Google Scholar 

  27. Lambert, J. E., Chapman, C. A., Wrangham, R. W., & Conklin-Brittain, N. L. (2004). Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125, 363–368. doi:10.1002/ajpa.10403.

    PubMed  Article  Google Scholar 

  28. Mioche, L., Bourdiol, P., Martin, J. F., & Noel, Y. (1999). Variations in human masseter and temporalis muscle activity related to food texture during free and side-imposed mastication. Archives of Oral Biology, 44, 1005–1012. doi:10.1016/S0003-9969(99)00103-X.

    PubMed  Article  CAS  Google Scholar 

  29. Møller, E. (1966). The chewing apparatus. Acta Physiologica Scandinavica, 69, 9–212.

    Google Scholar 

  30. Ottenhoff, F. A., van der Bilt, A., van der Glas, H. W., Bosman, F., & Abbink, J. H. (1996). The relationship between jaw elevator muscle surface electromyogram and simulated food resistance during dynamic condition in humans. Journal of Oral Rehabilitation, 23, 270–279. doi:10.1111/j.1365-2842.1996.tb00852.x.

    PubMed  Article  CAS  Google Scholar 

  31. Overdorff, D. J., & Strait, S. G. (1998). Seed handling by three prosimian primates in southeastern Madagascar: implications for seed dispersal. American Journal of Primatology, 45, 69–82. doi:10.1002/(SICI)1098-2345(1998)45:1<69::AID-AJP6>3.0.CO;2-U.

    PubMed  Article  CAS  Google Scholar 

  32. Ravosa, M. J. (1996). Jaw morphology and function in living and fossil Old World monkeys. International Journal of Primatology, 17, 909–932. doi:10.1007/BF02735294.

    Article  Google Scholar 

  33. Strait, S. G. (1993). Differences in occlusal morphology and molar size in frugivores and faunivores. Journal of Human Evolution, 25, 471–484. doi:10.1006/jhev.1993.1062.

    Article  Google Scholar 

  34. Taylor, A. B. (2002). Masticatory form and function in the African apes. American Journal of Physical Anthropology, 117, 133–156. doi:10.1002/ajpa.10013.

    PubMed  Article  Google Scholar 

  35. 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. doi:10.1002/ajpa.20225.

    PubMed  Article  CAS  Google Scholar 

  36. Thompson, C., Jackson, E., Stimpson, C., & Vinyard, C. (2007). Assessing how experimental and surgical manipulations during in vivo laboratory research influence chewing speed in tufted capuchins (Cebus apella). American Journal of Physical Anthropology, (Supplement 44), 231.

  37. Vinyard, C. J., Wall, C. E., Williams, S. H., & Hylander, W. L. (2003). Comparative functional analysis of skull morphology of tree-gouging primates. American Journal of Physical Anthropology, 120, 153–170. doi:10.1002/ajpa.10129.

    PubMed  Article  Google Scholar 

  38. Vinyard, C. J., Yamashita, N., & Tan, C. (2004). Maximum bite forces among three sympatric Hapalemur species at Ranomafana National Park, Madagascar. Journal of Morphology, 260, 338.

    Google Scholar 

  39. Vinyard, C. J., Yamashita, N., & Tan, C. Linking laboratory and field approaches in studying the evolutionary physiology of biting in bamboo lemurs. International Journal of Primatology, in press.

  40. Williams, S. H., Wall, C. E., Vinyard, C. J., & Hylander, W. L. (2002). A biomechanical analysis of skull form in gum-harvesting galagids. Folia Primatologica, 73, 197–209. doi:10.1159/000065429.

    Article  Google Scholar 

  41. Williams, S., Wright, B., Truong, V., Daubert, C., & Vinyard, C. (2005). Mechanical properties of foods used in experimental studies of primate masticatory function. American Journal of Primatology, 67, 329–346. doi:10.1002/ajp.20189.

    PubMed  Article  Google Scholar 

  42. Woda, A., Foster, K., Mishellany, A., & Peyron, M. A. (2006). Adaptation of healthy mastication to factors pertaining to the individual or to the food. Physiology & Behavior, 89, 28–35. doi:10.1016/j.physbeh.2006.02.013.

    Article  CAS  Google Scholar 

  43. Wright, B. W. (2005). Craniodental biomechanics and dietary toughness in the genus Cebus. Journal of Human Evolution, 48, 473–492. doi:10.1016/j.jhevol.2005.01.006.

    PubMed  Article  Google Scholar 

  44. Yamashita, N. (1998). Functional dental correlates of food properties in five Malagasy lemur species. American Journal of Physical Anthropology, 106, 169–188. doi:10.1002/(SICI)1096-8644(199806)106:2<169::AID-AJPA5>3.0.CO;2-L.

    PubMed  Article  CAS  Google Scholar 

  45. Yamashita, N. (2002). Diets of two lemur species in different microhabitats in Beza Mahafaly Special Reserve, Madagascar. International Journal of Primatology, 23, 1025–1051. doi:10.1023/A:1019645931827.

    Article  Google Scholar 

  46. Yamashita, N., Vinyard, C., & Tan, C. (2004). Food properties and jaw performance in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, (Supplement 38), 213.

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Acknowledgments

We thank Randy Ford and Margaret Clarke for assistance in the field and Stephan Schmidheiny and the Board of Directors of Hacienda La Pacifica for their permission to work on Hacienda La Pacifica and for their continued support and help. We also like to thank Drs. Nancy Stevens and Kristian Carlson for the invitation to contribute to this issue. The National Science Foundation (BCS-0507074, DBC-9118876, and SBR-9601766) and the Ohio University Research Committee supported our research.

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Correspondence to Susan H. Williams.

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Williams, S.H., Vinyard, C.J., Glander, K.E. et al. Telemetry System for Assessing Jaw-Muscle Function in Free-ranging Primates. Int J Primatol 29, 1441 (2008). https://doi.org/10.1007/s10764-008-9292-3

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Keywords

  • Alouatta
  • electromyography
  • mastication
  • telemetry