International Journal of Primatology

, Volume 33, Issue 3, pp 588–597 | Cite as

Thermal Imaging of Aye-Ayes (Daubentonia madagascariensis) Reveals a Dynamic Vascular Supply During Haptic Sensation

  • Gillian L. MoritzEmail author
  • Nathaniel J. Dominy


Infrared thermography (IRT) is used to visualize and estimate variation in surface temperatures. Applications of IRT to animal research include studies of thermofunctional anatomy, ecology, and social behavior. IRT is especially amenable to investigations of the somatosensory system because touch receptors are highly vascularized, dynamic, and located near the surface of the skin. The hands of aye-ayes (Daubentonia madagascariensis) are thus an inviting subject for IRT because of the prominent middle digit that functions as a specialized haptic sense structure during percussive and probative foraging. It is a vital sensory tool that is expected to feature a high density of dermal mechanoreceptors that radiate heat and impose thermal costs under cool temperatures. Here we explore this premise by acquiring IRT images of 8 aye-ayes engaged in a variety of passive and probative behaviors. We found that the middle digit was typically 2.3°C cooler than other digits when the metacarpophalangeal (MP) joint was extended, and that it warmed an average of 2.0°C when the MP joint was flexed during active touching behavior. These changes in digital surface temperature, which were sometimes as much 6.0°C, stand in sharp contrast with the profoundly invariant temperatures of the other digits. Although the physiological mechanisms behind these temperature changes are unknown, they appear to reveal a uniquely dynamic vascular supply.


Infrared imaging Mechanoreceptors Stenosis Stenotic kinking Thermography 



We thank E. R. Vogel and J. Chalk for the opportunity to contribute to the present special issue of IJP and to 3 anonymous reviewers for comments. For access to animals and images and for logistical and technical support, we thank A. J. Cunningham, M. Dye, J. A. Estes, K. E. Glander, D. M. Haring, H. Horblit, E. T. Hughes, R. Icard, T. L. Kivell, T. S. Kraft, E. C. Krakauer, C. MacDonald, M. N. Muchlinski, A. Pace, M. A. Ramsier, R. Schopler, C. V. Williams, T. M. Williams, A. D. Yoder, and S. Zehr. We received funding from the California Institute for Quantitative Biosciences, Center for Biomolecular Science and Engineering, UC-Santa Cruz, the David and Lucile Packard Foundation (2007–31754), and the Science, Technology, Engineering, Policy, and Society (STEPS) Institute for Innovation in Environmental Research, UC-Santa Cruz. This is DLC publication #1208.


  1. Ancrenaz, M., Lackman-Ancrenaz, I., & Mundy, N. (1994). Field observations of aye-ayes (Daubentonia madagascariensis) in Madagascar. Folia Primatologica, 62, 22–36.CrossRefGoogle Scholar
  2. Andriamasimanana, M. (1994). Ecoethological study of free-ranging aye-ayes (Daubentonia madagascariensis) in Madagascar. Folia Primatologica, 62, 37–45.CrossRefGoogle Scholar
  3. Brain, C., & Mitchell, D. (1999). Body temperature changes in free-ranging baboons (Papio hamadryas ursinus) in the Namib Desert, Namibia. International Journal of Primatology, 20, 585–598.CrossRefGoogle Scholar
  4. Cartmill, M. (1974). Daubentonia, Dactylopsila, woodpeckers and klinorhynchy. In R. D. Martin, G. A. Doyle, & A. C. Walker (Eds.), Prosimian biology (pp. 655–670). Gloucester: Duckworth.Google Scholar
  5. Cena, K., & Clark, J. A. (1973). Thermographic measurements of the surface temperatures of animals. Journal of Mammalogy, 54, 1003–1007.PubMedCrossRefGoogle Scholar
  6. Dehnhardt, G., Mauck, B., & Hyvarinen, H. (1998). Ambient temperature does not affect the tactile sensitivity of mystacial vibrissae in harbour seals. Journal of Experimental Biology, 201, 3023–3029.PubMedGoogle Scholar
  7. Dewasmes, G., & Telliez, F. (2000). Tactile arousal threshold of sleeping king penguins in a breeding colony. Journal of Sleep Research, 9, 255–259.PubMedCrossRefGoogle Scholar
  8. Dominy, N. J. (2009). Evolution of sensory receptor specializations in the glabrous skin. In L. R. Squire (Ed.), Encyclopedia of neuroscience, vol. 4 (pp. 39–42). Oxford: Academic Press.CrossRefGoogle Scholar
  9. Erickson, C. J. (1991). Percussive foraging in the aye-aye, Daubentonia madagascariensis. Animal Behaviour, 41, 793–801.CrossRefGoogle Scholar
  10. Erickson, C. J. (1995). Feeding sites for extractive foraging by the aye-aye, Daubentonia madagascariensis. American Journal of Primatology, 35, 235–240.CrossRefGoogle Scholar
  11. Erickson, C. J. (1998). Cues for prey location by aye-ayes (Daubentonia madagascariensis). Folia Primatologica, 69, 35–40.CrossRefGoogle Scholar
  12. Erickson, C. J., Nowicki, S., Dollar, L., & Goehring, N. (1998). Percussive foraging: Stimuli for prey location by aye-ayes (Daubentonia madagascariensis). International Journal of Primatology, 19, 111–122.CrossRefGoogle Scholar
  13. Fundin, B. T., Pfaller, K., & Rice, F. L. (1997). Different distributions of the sensory and autonomic innervation among the microvasculature of the rat mystacial pad. Journal of Comparative Neurology, 389, 545–568.PubMedCrossRefGoogle Scholar
  14. George, J. S., Lewine, J. D., Goggin, A. S., Dyer, R. B., & Flynn, E. R. (1993). IR thermal imaging of a monkey's head: Local temperature changes in response to somatosensory stimulation. Advances in Experimental Medicine and Biology, 333, 125–136.PubMedGoogle Scholar
  15. Gibson, K. R. (1986). Cognition, brain size and the extraction of embedded food resources. In J. G. Else & P. C. Lee (Eds.), Primate ontogeny, cognition and social behaviour (pp. 93–103). Cambridge: Cambridge University Press.Google Scholar
  16. Glander, K. E., Vinyard, C. J., Williams, S. H., & Teaford, M. F. (2011). Thermal imaging and iButtons: A novel use of two technologies to quantify the daily thermal profiles of wild howlers (Alouatta palliata) and their habitats at La Pacifica, Costa Rica. American Journal of Physical Anthropology, 144(Suppl. 52), 143.Google Scholar
  17. Hoffmann, J. N., Montag, A. G., & Dominy, N. J. (2004). Meissner corpuscles and somatosensory acuity: The prehensile appendages of primates and elephants. Anatomical Record, 281A, 1138–1147.Google Scholar
  18. Iwano, T. (1991). The usage of the digits of a captive aye-aye (Daubentonia madagascariensis). African Study Monographs, 12, 87–98.Google Scholar
  19. Iwano, T., & Iwakawa, C. (1988). Feeding behaviour of the aye-aye (Daubentonia madagascariensis) on nuts of ramy (Canarium madagascariensis). Folia Primatologica, 50, 136–142.CrossRefGoogle Scholar
  20. Jouffroy, F. K. (1975). Osteology and myology of the lemuriform postcranial skeleton. In I. Tattersall & R. W. Sussman (Eds.), Lemur biology (pp. 149–192). New York: Plenum Press.CrossRefGoogle Scholar
  21. Kaufman, J. A., Ahrens, E. T., Laidlaw, D. H., Zhang, S., & Allman, J. M. (2005). Anatomical analysis of an aye-aye brain (Daubentonia madagascariensis, Primates: Prosimii) combining histology, structural magnetic resonance imaging, and diffusion-tensor imaging. Anatomical Record, 287A, 1026–1037.CrossRefGoogle Scholar
  22. Kivell, T. L., Schmitt, D., & Wunderlich, R. E. (2010). Hand and foot pressures in the aye-aye (Daubentonia madagascariensis) reveal novel biomechanical trade-offs required for walking on gracile digits. Journal of Experimental Biology, 213, 1549–1557.PubMedCrossRefGoogle Scholar
  23. Krakauer, E., Lemelin, P., & Schmitt, D. (2002). Hand and body position during locomotor behavior in the aye-aye (Daubentonia madagascariensis). American Journal of Primatology, 57, 105–118.PubMedCrossRefGoogle Scholar
  24. Lhota, S., Jůnek, T., Bartoš, L., & Kuběna, A. A. (2008). Specialized use of two fingers in free-ranging aye-ayes (Daubentonia madagascariensis). American Journal of Primatology, 70, 786–795.PubMedCrossRefGoogle Scholar
  25. Lhota, S., Jůnek, T., & Bartoš, L. (2009). Patterns and laterality of hand use in free-ranging aye-ayes (Daubentonia madagascariensis) and a comparison with captive studies. Journal of Ethology, 27, 419–428.CrossRefGoogle Scholar
  26. Mauck, B., Eysel, U., & Dehnhardt, G. (2000). Selective heating of vibrissal follicles in seals (Phoca vitulina) and dolphins (Sotalia fluviatilis guianensis). Journal of Experimental Biology, 203, 2125–2131.PubMedGoogle Scholar
  27. Mauck, B., Bilgmann, K., Jones, D. D., Eysel, U., & Dehnhardt, G. (2003). Thermal windows on the trunk of hauled-out seals: Hot spots for thermoregulatory evaporation? Journal of Experimental Biology, 206, 1727–1738.PubMedCrossRefGoogle Scholar
  28. McCafferty, D. J. (2007). The value of infrared thermography for research on mammals: Previous applications and future directions. Mammal Review, 37, 207–223.CrossRefGoogle Scholar
  29. McCafferty, D. J., Gilbert, C., Paterson, W., Pomeroy, P. P., Thompson, D., Currie, J. I., et al. (2011). Estimating metabolic heat loss in birds and mammals by combining infrared thermography with biophysical modelling. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 158, 337–345.CrossRefGoogle Scholar
  30. Milliken, G. W., Ward, J. P., & Erickson, C. J. (1991). Independent digit control in foraging by the aye-aye (Daubentonia madagascariensis). Folia Primatologica, 56, 219–224.CrossRefGoogle Scholar
  31. Muchlinski, M. N. (2008). The relationship between the infraorbital foramen, infraorbital nerve, and maxillary mechanoreception: Implications for interpreting the paleoecology of fossil mammals based on infraorbital foramen size. Anatomical Record, 291A, 1221–1226.Google Scholar
  32. Muchlinski, M. N. (2010). Ecological correlates of infraorbital foramen area in primates. American Journal of Physical Anthropology, 141, 131–141.PubMedGoogle Scholar
  33. Nakayama, K., Goto, S., Kuraoka, K., & Nakamura, K. (2005). Decrease in nasal temperature of rhesus monkeys (Macaca mulatta) in negative emotional state. Physiology & Behavior, 84, 783–790.CrossRefGoogle Scholar
  34. Owen, R. (1863). Monograph on the aye-aye (Chiromys madagascariensis, Cuvier). London: Taylor and Francis.Google Scholar
  35. Oxnard, C. E. (1981). The uniqueness of Daubentonia. American Journal of Physical Anthropology, 54, 1–21.CrossRefGoogle Scholar
  36. Perry, G. H., & Dominy, N. J. (2009). Evolution of the human pygmy phenotype. Trends in Ecology & Evolution, 24, 218–225.CrossRefGoogle Scholar
  37. Petter, J. J., & Peyrieras, A. (1970). Nouvelle contribution a l'etude d'un lemurien Malagache, le aye-aye (Daubentonia madagascariensis E. Geoffroy). Mammalia, 34, 167–193.CrossRefGoogle Scholar
  38. Pollock, J. I., Constable, I. D., Mittermeier, R. A., Ratsirarson, J., & Simons, H. (1985). A note on the diet and feeding behavior of the aye-aye Daubentonia madagascariensis. International Journal of Primatology, 6, 435–447.CrossRefGoogle Scholar
  39. Rundus, A. S., Owings, D. H., Joshi, S. S., Chinn, E., & Giannini, N. (2007). Ground squirrels use an infrared signal to deter rattlesnake predation. Proceedings of the National Academy of Sciences of the USA, 104, 14372–14376.PubMedCrossRefGoogle Scholar
  40. Schmid, J. (2011). Thermoregulation and energetics. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology: A practical guide (2nd ed., pp. 339–351). Cambridge: Cambridge University Press.Google Scholar
  41. Soligo, C. (2005). Anatomy of the hand and arm in Daubentonia madagascariensis: A functional and phylogenetic outlook. Folia Primatologica, 76, 262–300.CrossRefGoogle Scholar
  42. Sterling, E. J. (1994). Aye-ayes: Specialists on structurally defended resources. Folia Primatologica, 62, 142–154.CrossRefGoogle Scholar
  43. Sterling, E. J., & McCreless, E. E. (2006). Adaptations in the aye-aye: A review. In L. Gould & M. L. Sauther (Eds.), Lemurs: Ecology and adaptation (pp. 159–184). New York: Springer.Google Scholar
  44. Sterling, E. J., & Povinelli, D. J. (1999). Tool use, aye-ayes, and sensorimotor intelligence. Folia Primatologica, 70, 8–16.CrossRefGoogle Scholar
  45. Sterling, E. J., Dierenfeld, E. S., Ashbourne, C. J., & Feistner, A. T. C. (1994). Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatologica, 62, 115–124.CrossRefGoogle Scholar
  46. Šumbera, R., Zelová, J., Kunc, P., Knížková, I., & Burda, H. (2007). Patterns of surface temperatures in two mole-rats (Bathyergidae) with different social systems as revealed by IR-thermography. Physiology & Behavior, 92, 526–532.CrossRefGoogle Scholar
  47. Tattersall, G. J., & Cadena, V. (2010). Insights into animal temperature adaptations revealed through thermal imaging. Imaging Science Journal, 58, 261–268.CrossRefGoogle Scholar
  48. Tattersall, G. J., Andrade, D. V., & Abe, A. S. (2009). Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science, 325, 468–470.PubMedCrossRefGoogle Scholar
  49. Ward, S., & Slater, P. J. B. (2005). Heat transfer and the energetic cost of singing by canaries Serinus canaria. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 191, 953–964.PubMedCrossRefGoogle Scholar
  50. Weissenböck, N. M., Weiss, C. M., Schwammer, H. M., & Kratochvil, H. (2010). Thermal windows on the body surface of African elephants (Loxodonta africana) studied by infrared thermography. Journal of Thermal Biology, 35, 182–188.CrossRefGoogle Scholar
  51. West, P. M., & Packer, C. (2002). Sexual selection, temperature, and the lion's mane. Science, 297, 1339–1343.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate Program in Ecology and Evolutionary BiologyDartmouth CollegeHanoverUSA
  2. 2.Department of Biological SciencesDartmouth CollegeHanoverUSA
  3. 3.Department of AnthropologyDartmouth CollegeHanoverUSA

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