Thermal Imaging of Aye-Ayes (Daubentonia madagascariensis) Reveals a Dynamic Vascular Supply During Haptic Sensation
- 443 Downloads
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.
KeywordsInfrared 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.
- 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
- 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
- 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
- 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
- Iwano, T. (1991). The usage of the digits of a captive aye-aye (Daubentonia madagascariensis). African Study Monographs, 12, 87–98.Google Scholar
- 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
- 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
- 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
- Owen, R. (1863). Monograph on the aye-aye (Chiromys madagascariensis, Cuvier). London: Taylor and Francis.Google Scholar
- 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
- 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