ArticlePDF Available

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


Abstract and Figures

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 ayeayes (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.
Content may be subject to copyright.
Thermal Imaging of Aye-Ayes (Daubentonia
madagascariensis) Reveals a Dynamic Vascular
Supply During Haptic Sensation
Gillian L. Moritz &Nathaniel J. Dominy
Received: 11 April 2011 / Accepted: 27 October 2011 / Published online: 8 January 2012
#Springer Science+Business Media, LLC 2012
Abstract 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.
Keywords Infrared imaging .Mechanoreceptors .Stenosis .Stenotic kinking .
Int J Primatol (2012) 33:588597
DOI 10.1007/s10764-011-9575-y
G. L. Moritz (*)
Department of Biological Sciences, Graduate Program in Ecology and Evolutionary Biology,
Dartmouth College, Hanover, NH 03755, USA
N. J. Dominy
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA
N. J. Dominy
Department of Anthropology, Dartmouth College, Hanover, NH 03755, USA
Infrared thermography (IRT) is used to visualize and estimate variation in surface
temperatures based on the physical laws of radiative transfer. For animals, surface
temperatures vary as a function of vascular dilation and the emissivity of heat from
skin, feathers, or fur (Fig. 1a). In the 1960s, the applications of IRT to animal
research faced a variety of practical limitations, such as the need for large, liquid
nitrogen-cooled detectors (Cena and Clark 1973; McCafferty et al. 2011). As a
result, IRT was conceived mainly as noninvasive means of detecting disease among
captive animals. At close range (<1 m), specific sites of heat transfer can point to the
location and extent of infection. In other studies, IRT was employed at greater
distances (>1000 m) to census wild populations (McCafferty 2007). By the 1990s,
the development of handheld, electronically cooled cameras eased portability
constraints and fueled a wider consideration of the energy costs faced by
endothermic animals. As a result, the applications of IRT to animal research have
surged in recent years to include studies of thermofunctional anatomy, ecology, and
social behavior (Šumbera et al. 2007; Tattersall and Cadena 2010). For example, the
thermal costs of sexual selection have been explored in species ranging from
canaries to lions (Ward and Slater 2005; West and Packer 2002). IRT is therefore an
established methodology that is undergoing a rapid and exciting practical expansion;
yet, research applications focused on nonhuman primates are few (George et al.
1993; Glander et al. 2011; Nakayama et al. 2005).
Active Touch, the Haptic Sense
IRT has also informed studies of the senses. It is especially amenable to the
somatosensory system because touch receptors are highly vascularized, dynamic,
and located near the surface of the skin (Fundin et al.1997). For pinnipeds, haptic
(active touch) perception with vibrissae can result in striking thermal increases of the
Fig. 1 a Thermograph of a man after 30 min of walking in the Bwindi Impenetrable National Park,
Uganda (ambient conditions= 19.7°C; relative humidity =97.4%). Evaporative cooling of the skin surface
(mean temperature= 30.3°C) reveals vasodilation and elevated surface temperatures of the perforating
branches of the thoracic and thoracoacromial arteries (range =31.032.2°C). bThermograph of a Steller's
sea lion (Eumetopias jubatus) in Santa Cruz, CA (ambient conditions= 14.4°C; relative humidity =85.0%).
A rich arterial supply to the underlying mechanoreceptors of the whiskers results in a conspicuous thermal
window; the mean mystacial surface temperature is 25.0°C, whereas the overall mean surface temperature
is 21.8°C.
Thermography of Vascular Supply of Aye-Ayes 589
mystacial skin (Fig. 1b). Such a thermal window or surface area associated with
disproportionate heat loss due to increased peripheral blood flow (Mauck et al. 2003;
Weissenböck et al.2010)is a testament to the adaptive value of whiskers (cf.
Muchlinski 2008,2010). The benefits of active touch for detecting prey must offset
the cost of reduced heat retention in cold water (Dehnhardt et al. 1998; Mauck et al.
2000). Similarly, the egg-incubating feet of sleeping penguins (Aptenodytes
patagonica) are exceedingly sensitive to egg movement (Dewasmes and Telliez
2000), yet also costly thermal windows in air temperatures of 15°C (McCafferty et
al. 2011). For penguins the fitness advantages of mechanosensitive feet appear to
override the high energetic costs.
The concept of a thermal window is germane to nocturnal primates. The hands
and feet of primates are richly and almost uniquely invested with Meissner
corpuscles (MCs). MCs are rapidly adapting mechanoreceptors that respond to
transient or phasic stimuli. Their distinctive morphology and location in the dermal
papillae of glabrous skin, where they connect to and tightly abut the basal surface of
the epidermis, indicate a primary role during haptic touch (Dominy 2009; Hoffmann
et al. 2004). The location and complex innervation of MCs by 1 or 2 myelinated
fibers from the subepidermal nerve plexus is expected to impose non-negligible
energetic and thermal costs to primates active under cool temperatures. Such costs
might even extend to the scalp in the form of localized thermal windows associated
with somatocortical processing (George et al. 1993). To explore such possibilities,
we captured infrared images of a nocturnal haptic specialist, the aye-aye
(Daubentonia madagascariensis).
Aye-ayes are a distinctive and enigmatic primate. They have elongated and ectaxonic
hands with a disproportionately long, thin, and clawed 3rd digit that has been
described as villiform, filamentous, gracile, and grotesquely attenuated (Fig. 2a)
(Cartmill 1974; Jouffroy 1975; Oxnard 1981; Owen 1863). Digit III is not only
independently mobile (Milliken et al.1991), but also multiaxial because of a
unique ball-and-socket metacarpophalangeal (MP) joint (Soligo 2005). As a result
of this unique morphology, the digit is vulnerable to injury and poorly suited for
bearing load during palmigrade locomotion; indeed, digit III is hyperextended at
the MP joint, flexed at the interphalangeal joints, and parkedto minimize
loading during locomotion (Fig. 2b)(Kivellet al.2010; Krakauer et al.2002;
Soligo 2005).
Such digital morphology functions to facilitate percussive foraging or tap-
scanning (Erickson 1991,1995,1998;Erickson et al. 1998), a haptic-auditory
behavior that contributes to the detection of embedded beetle larvae and to the
material assessment of foods (Ancrenaz et al.1994; Andriamasimanana 1994; Iwano
1991; Iwano and Iwakawa 1988; Lhota et al. 2008,2009; Petter and Peyrieras 1970;
Pollock et al. 1985; Sterling 1994; Sterling and McCreless 2006; Sterling et al.
1994). Accordingly, aye-ayes are described as having a well-developed
sensorimotor intelligence (Gibson 1986; Sterling and Povinelli 1999)thatissupported
in part by a large and expanded somatosensory cortex (Kaufman et al.2005). Such
haptic specializations suggest that digit III might be richly innervated with MCs and
590 G.L. Moritz, N.J. Dominy
potentially a costly thermal window. Here we test this hypothesis by acquiring IRT
images of aye-ayes engaged in a variety of passive and probative behaviors.
Fig. 2 a Metacarpophalangeal flexion of digit III during probative foraging (photograph by D. Haring,
used with permission). bMP extension of digit III during palmigrade locomotion over a force plate (see
Kivell et al. 2010; photograph by D. Haring, used with permission). cThermograph of an aye-aye
investigating a food object. The relatively cool middle digit (T
digit III
=26.9°C, SD = 1.1) is the result of
preimage MP extension during palmigrady (cf. T
human skin
=32.8°C, SD = 0.6). dAn aye-aye grasping a
food object. The relatively warm middle digit (T
digit III
=29.6°C, SD = 0.2) is the result of MP flexion
during haptic assessment. eThe aye-aye Kali engaged in tap-scanning. The right flexed middle digit is
substantially warmer (T
digit III
=26.7°C, SD =0.8) than its extended counterpart (T
digit III
=22.9°C, SD =1.4).
fNotched boxplot of T
digit III
during MP extension and flexion. Boxes represent the interquartile range
between the first and third quartiles and the line inside represents the median; nonoverlapping notches
signify a difference at the 95% confidence level. Whiskers denote the lowest and highest values. On
average, T
digit III
increased 2.0°C when the MP joint was flexed to accommodate haptic behaviors such as
tap-scanning and probing (t=9.3, p<0.0001).
Thermography of Vascular Supply of Aye-Ayes 591
Materials and Methods
Study Sites and Subjects
We studied 8 adult aye-ayes within the indoor, temperature-controlled enclosures of
the Duke Lemur Center and San Francisco Zoo (ca. 25°C; Table I). We filmed the
subjects from a distance of ca. 1 m during routine enrichment activities. Each
activity motivated the aye-ayes to approach, evaluate, and extract prepared foods.
Thus we filmed the middle digit when it was engaged in 3 sequential activities and
positions: 1) locomotor approach resulting in a state of extension at the MP joint, 2)
tap-scanning resulting in rapid flexion and extension at the MP joint, and 3) probing
and removal of food resulting in full flexion at the MP joint. We defined states of
MP flexion or extension as angular deviations >10º from a neutral position. The
difficulty of the extraction tasks varied. Food rewards contained within cardboard or
eggshells were extracted quickly, whereas foods embedded in bamboo sheaths were
more challenging to excavate.
Thermal Imaging and Analysis
We estimated the surface temperatures of aye-ayes with a handheld infrared thermal
imaging camera (ThermaCAM SC640; FLIR Systems, Boston, MA). The camera
uses a 640×480 pixel focal plane array to produce 307,200-pixel thermographs
(accuracy±1°C for objects 5120°C). For each thermograph, we recorded the state
of flexion of the MP joint and estimated the surface temperature of individual digits
) with commercial software that can calculate the temperature of selected pixels
within a user-drawn polygon (ThermoVision ExaminIR Max v. 1.10, FLIR
Systems). Here, T
is defined as the average temperature of all pixels within an
irregular polygon extending from the MP joint to the distal apical pad of a given
digit (excluding the nail or claw). This protocol was approved by the Duke Lemur
Center Research Committee (approval no. O-9-137-08-5) and the Chancellors
Animal Research Committee of the University of California, Santa Cruz
(approval no. 0811).
Table I Summary information for focal subjects
Name Body mass (g) Sex Age (yr) Provenance
Bellatrix 2620 F 5 DLC
Kali 2920 F 13 DLC
Lucrezia 2960 F 9 DLC
Medea 2470 F 6 DLC
Mephistopheles 2670 M 25 DLC
Nify 1910 M 2 SFZ
Sabrina 2750 F 7 SFZ
Warlock 2450 M 12 SFZ
DLC Duke Lemur Center; SFZ San Francisco Zoo
592 G.L. Moritz, N.J. Dominy
We estimated T
of each visible digit and used these values as independent
sample points. To compare variation in T
within each test condition, i.e., state of
MP extension or flexion, we used one-way ANOVAs and Tukeyspost hoc test of
honestly significant differences (HSD). To compare variation in T
between the 2
test conditions, we used a repeated-measures t-test. We performed all statistical tests
using JMP v. 8.0.2 for Macintosh.
We examined 81,345 pixels from 81 thermographs. Digit I (the pollex) was almost
always obscured in our thermographs due to the grasping posture of the hand and the
lateral vantage point of the camera operator. Accordingly, our results are limited to
digits II-V. Among digits II, IV, and V, we found little variation in surface
temperature regardless of whether the MP joint was flexed (T
digits II, IV, V
p=0.88) or extended (T
digits II, IV, V
=2.2, p=0.12; Table II). Much more
variable, however, was T
digit III
(Fig. 2c,d), which was typically 2.3°C cooler than the
other digits when the MP joint was extended (F
=15.3, p<0.0001, Tukey HSD,
P<0.05; Fig. 2e). Yet T
digit III
increased significantly (an average of 2.0°C; repeated
measures t=9.3, df=33, P<0.0001; Table II; Fig. 2f) when the MP joint was flexed
to accommodate active tap-scanning and probing. We observed a similar change in
digit V, but the difference was marginally significant and almost certainly the artifact
of a small sample size (n= 3 images in a state of MP flexion).
In some individual cases, we recorded relatively extreme temperature
differentials. For example, Fig. 2e of the female Kali shows that T
digit III
of the
left hand was ca. 6.1°C cooler than T
digit II
and T
digit IV
(29.3° and 28.8°C,
respectively), whereas the right middle finger, which is flexed at the MP joint and
engaged in haptic tap-scanning of a sealed food container, is ca. 3.8°C warmer
than its counterpart. Such warming occurred within 3 min of the onset of digital
Table II Effects of MP joint extension and flexion on the mean surface temperature (±1 SD) of individual
digits (T
Extension at MP joint Flexion at MP joint
Digit Nimages Mean T
Nimages Mean T
Mean difference p
II 42 27.8± 2.5
(22.731.9) 20 28.5± 1.8
(24.331.4) 0.7 0.253
III 55 24.9± 1.7
(21.027.8) 34 26.9± 2.1
(22.730.5) 2.0 <0.0001
IV 58 27.4± 2.6
(23.030.8) 18 28.5± 1.8
(23.831.4) 1.1 0.711
V 21 26.5± 2.5
(22.329.9) 3 28.4± 1.3
(25.130.8) 1.9 0.049
Within-condition test, ANOVA Tukeys HSD: Values for individual digits that are statistically different
from each other at the p<0.05 level are followed by different letters in superscript; values that are
statistically indistinguishable from each other are followed by the same letter in superscript.
Between-condition test, repeated-measures t-test based on samples sizes in the flexion condition
Thermography of Vascular Supply of Aye-Ayes 593
Here we report estimates of digital surface temperatures (T
) based on IRT. The
middle digit of aye-ayes is a highly specialized haptic sense structure. It is a vital
foraging tool that is expected to feature a high density of dermal mechanoreceptors
and therefore radiate relatively more heat than other digits. We found that T
digit III
was typically 2.3°C cooler and sometimes as much as 6.0°C cooler than other digits
when the aye-ayes were engaged in palmigrade locomotion. Yet T
digit III
warmed to
near parity with the other digits when the metacarpophalangeal joint was flexed to
accommodate percussive foraging and digital probing. These findings suggest a
uniquely dynamic vascular supply to digit III during haptic sensation.
At least 3 compatible factors could account for the relatively cool temperatures of digit
III during nonhaptic behaviors. First, the thin and elongate morphology of digit III results
in a relatively high surface-to-volume ratio. Because such a ratio is unfavorable for heat
retention, controlled vasoconstriction is expected to reduce thermal costs during inactivity
or locomotion. Analogous examples of anatomical structures under thermal control
include the tails of California ground squirrels (Spermophilus beecheyi:Runduset al.
2007)andthebillsoftocotoucans(Ramphastos toco:Tattersallet al.2009). Second,
the importance of minimizing loading to digit III during palmigrade locomotion results
in a high degree of extension at the MP joint (Fig. 2b;Kivellet al. 2010; Krakauer et al.
2002;Oxnard1981). Such hyperextension might cause stricture of the palmar digital
artery, termed stenotic kinking, that could result in cooler surface temperatures across
the digit. Third, digit III has relatively reduced vascular requirements, as it is virtually
devoid of subcutaneous fat. Moreover, the only muscle belly present (of the interossei
palmaris) is diminished compared to its presence in the other digits (Soligo 2005).
Tak en tog ethe r, s uch reduce d meta boli c d ema nds are e xpe c ted to c ontr ibut e to
relatively lower temperatures during nonhaptic activities, when digit III is practically
functionless. Thus, although the underlying physiological mechanisms that drive the
dynamic temperature changes reported here are unknown, our results highlight the
potential thermal costs of a highly specialized sensory structure.
We believe that numerous potential applications of IRT exist within the field of
primatology, a discipline with a long-standing interest in thermoregulatory behaviors
(Brain and Mitchell 1999; Schmid 2011). For example, the few recent anthropological
and primatological applications of IRT have had widely different aims, focusing on the
effects of social signals, body size, and daily temperature changes on the surface
temperatures of humans and nonhuman primates (Glander et al.2011;Nakayamaet al.
2005; Perry and Dominy 2009). Overall, our findings contribute to the expanding role
of IRT in studies focused on animal functional physiology and anatomy.
Acknowledgments 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.
594 G.L. Moritz, N.J. Dominy
Ancrenaz, M., Lackman-Ancrenaz, I., & Mundy, N. (1994). Field observations of aye-ayes (Daubentonia
madagascariensis) in Madagascar. Folia Primatologica, 62,2236.
Andriamasimanana, M. (1994). Ecoethological study of free-ranging aye-ayes (Daubentonia madagas-
cariensis) in Madagascar. Folia Primatologica, 62,3745.
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, 585598.
Cartmill, M. (1974). Daubentonia,Dactylopsila, woodpeckers and klinorhynchy. In R. D. Martin, G. A.
Doyle, & A. C. Walker (Eds.), Prosimian biology (pp. 655670). Gloucester: Duckworth.
Cena, K., & Clark, J. A. (1973). Thermographic measurements of the surface temperatures of animals.
Journal of Mammalogy, 54, 10031007.
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
Dewasmes, G., & Telliez, F. (2000). Tactile arousal threshold of sleeping king penguins in a breeding
colony. Journal of Sleep Research, 9, 255259.
Dominy, N. J. (2009). Evolution of sensory receptor specializations in the glabrous skin. In L. R. Squire
(Ed.), Encyclopedia of neuroscience, vol. 4 (pp. 3942). Oxford: Academic Press.
Erickson, C. J. (1991). Percussive foraging in the aye-aye, Daubentonia madagascariensis.Animal
Behaviour, 41, 793801.
Erickson, C. J. (1995). Feeding sites for extractive foraging by the aye-aye, Daubentonia madagascar-
iensis.American Journal of Primatology, 35, 235240.
Erickson, C. J. (1998). Cues for prey location by aye-ayes (Daubentonia madagascariensis). Folia
Primatologica, 69,3540.
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, 19,111122.
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, 545568.
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, 125136.
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. 93103). Cambridge:
Cambridge University Press.
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.
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, 11381147.
Iwano, T. (1991). The usage of the digits of a captive aye-aye (Daubentonia madagascariensis). African
Study Monographs, 12,8798.
Iwano, T., & Iwakawa, C. (1988). Feeding behaviour of the aye-aye (Daubentonia madagascariensis) on
nuts of ramy (Canarium madagascariensis). Folia Primatologica, 50, 136142.
Jouffroy, F. K. (1975). Osteology and myology of the lemuriform postcranial skeleton. In I. Tattersall & R.
W. Sussman (Eds.), Lemur biology (pp. 149192). New York: Plenum Press.
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, 10261037.
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, 15491557.
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, 105118.
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, 786795.
Thermography of Vascular Supply of Aye-Ayes 595
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,
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
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, 17271738.
McCafferty, D. J. (2007). The value of infrared thermography for research on mammals: Previous
applications and future directions. Mammal Review, 37, 207223.
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, 337345.
Milliken, G. W., Ward, J. P., & Erickson, C. J. (1991). Independent digit control in foraging by the aye-aye
(Daubentonia madagascariensis). Folia Primatologica, 56, 219224.
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, 12211226.
Muchlinski, M. N. (2010). Ecological correlates of infraorbital foramen area in primates. American
Journal of Physical Anthropology, 141, 131141.
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, 783790.
Owen, R. (1863). Monograph on the aye-aye (Chiromys madagascariensis, Cuvier). London: Taylor and
Oxnard, C. E. (1981). The uniqueness of Daubentonia.American Journal of Physical Anthropology, 54,
Perry, G. H., & Dominy, N. J. (2009). Evolution of the human pygmy phenotype. Trends in Ecology &
Evolution, 24, 218225.
Petter, J. J., & Peyrieras, A. (1970). Nouvelle contribution a l'etude d'un lemurien Malagache, le aye-aye
(Daubentonia madagascariensis E. Geoffroy). Mammalia, 34, 167193.
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, 435447.
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, 1437214376.
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. 339351). Cambridge: Cambridge
University Press.
Soligo, C. (2005). Anatomy of the hand and arm in Daubentonia madagascariensis: A functional and
phylogenetic outlook. Folia Primatologica, 76, 262300.
Sterling, E. J. (1994). Aye-ayes: Specialists on structurally defended resources. Folia Primatologica, 62,
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. 159184). New York: Springer.
Sterling, E. J., & Povinelli, D. J. (1999). Tool use, aye-ayes, and sensorimotor intelligence. Folia
Primatologica, 70,816.
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, 62,115124.
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, 526532.
Tattersall, G. J., & Cadena, V. (2010). Insights into animal temperature adaptations revealed through
thermal imaging. Imaging Science Journal, 58, 261268.
Tattersall, G. J., Andrade, D. V., & Abe, A. S. (2009). Heat exchange from the toucan bill reveals a
controllable vascular thermal radiator. Science, 325, 468470.
596 G.L. Moritz, N.J. Dominy
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, 953964.
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, 182188.
West, P. M., & Packer, C. (2002). Sexual selection, temperature, and the lion's mane. Science, 297, 1339
Thermography of Vascular Supply of Aye-Ayes 597
... Unlike the eyes, vibrissae regions are thermally insulated, being covered by non-vibrissal hairs. A refined neural and vascular control allows temperature modulation in response to touch (i.e., active touch), maintaining tactile sensitivity under different thermal conditions (Mauck et al., 2000;Moritz and Dominy, 2012). In aquatic and semiaquatic mammals, infrared thermography has revealed selective heating of the vibrissal system. ...
The aim of this work was to investigate the thermal biology of the Spix's yellow-toothed cavy (Galea spixii) from the hot and dry environment of the Brazilian Caatinga by infrared thermography and biophysical equations. We monitored the rectal temperature, as well as the non-evaporative (radiative and convective pathways) and evapo-rative heat exchanges of males and females. The mean rectal temperature of females and males was 37.58 ± 0.02 and 37.47 ± 0.02 °C, respectively. We identified thermal windows by infrared thermography. The surface temperatures and the long-wave radiation heat exchanges were higher in the periocular, preocular, pinnae and vib-rissae regions, in that order. The surface temperature of the periocular and preocular regions correlated positively with rectal temperature. Convective heat exchange was insignificant for thermoregulation by G. spixii. Evapora-tive heat loss increased when the thermal environment inhibited the radiative pathway. Females showed higher evaporative thermolysis than males at times of greater thermal challenge, suggesting a lower tolerance to heat stress. Therefore, infrared thermography identified the thermal windows, which represented the first line of defense against overheating in G. spixii. The periocular and preocular surface temperatures could be used as predic-tors of the thermal state of G. spixii.
... Thermal imaging can also provide insight into thermal windows (McCafferty 2007;Tattersall et al. 2012). For example, thermal imaging has been used to demonstrate that the bill of birds is a thermal window (Tattersall et al. 2009(Tattersall et al. , 2017 as well as the middle digit of the aye-aye's hand (Moritz and Dominy 2012). Thermal windows can potentially explain some thermoregulatory properties that animals can use, like how they handle high ambient heat. ...
Thermoregulation of animals is becoming an increasingly important field as climate change begins to affect ambient temperature and precipitation. Understanding animals’ thermoregulatory properties allows us to monitor potentially vulnerable species. For my thesis, I examined the thermoregulation of Peromyscus and Mus musculus using flow-through respirometry and thermal imaging. The original goal was to create a working model for thermoregulation in Peromyscus leucopus and maniculatus but, due to lack of specimens, I examined lab mice as a comparison. Some information was already known from earlier studies and the present study aimed to update physiological information on mice. I hypothesized that higher temperatures would lead to increases metabolic rate and water loss and that the tail would be a major contributor to the radiative heat loss. Mice were placed in respirometry chambers at temperatures of 25, 30, and 35°C. At 25°C, the animals displayed the highest metabolic rate and evaporative water loss likely due to an increased level of activity. Due to high activity at the beginning of the experiment, data from 25°C were omitted from the analyses. The highest evaporative water loss for both lab and field mice was at 35°C. Field mice also had the highest metabolic rate at 35°C. However, lab mice displayed an almost equivalent metabolic rate at 30°C and 35°C. The tail did not dissipate as much heat as the back of the mouse, indicating that the tail may only play a secondary role in thermoregulation or heat dissipation at higher temperatures.
... The most extreme specialization within the aye-aye hand, however, lies in the third digit, which is both extremely slender ( Figure 1) and mobile, possessing a ball-and-socket joint at the metacarpophalangeal junction and a mechanism for folding the third digit over the fourth during locomotion (Soligo, 2005). This digit also appears to possess a uniquely dynamic vascular supply, resulting in significant changes in surface temperature during flexion of this joint (Moritz & Dominy, 2012). Functionally, this digit is principally used as a foraging tool for the extraction of xylophagous larvae, but is additionally used for drinking liquids (such as egg yolks), extracting pulp from soft fruits, and as an all-purpose probe (especially by younger animals) to explore their environment (Lamberton, 1911;Petter & Peyrieras, 1970). ...
Full-text available
Objectives: Accessory digits have evolved independently within several mammalian lineages. Most notable among these is the pseudothumb of the giant panda, which has long been considered one of the most extraordinary examples of contingent evolution. To date, no primate has been documented to possess such an adaptation. Here, we investigate the presence of this structure within the aye-aye (Daubentonia madagascariensis), a species renowned for several other specialized morphological adaptations in the hand, including a morphologically unique third digit. Materials and methods: We combine physical dissection techniques with digital imaging processes across a sample of seven individuals (six adults and one immature individual) to describe and visualize the anatomy of the wrist and hand within the aye-aye. Results: A distinct pseudothumb, which consists of both a bony component (an expanded radial sesamoid) and a dense cartilaginous extension (the "prepollex") was observed in all specimens. We demonstrate that this pseudodigit receives muscular attachments from three muscles, which collectively have the potential to enable abduction, adduction, and opposition. Finally, we demonstrate that the pseudothumb possesses its own distinct pad within the palm, complete with independent dermatoglyphs. Discussion: Pseudothumbs have been suggested to improve palmar dexterity in taxa with overly -generalized first digits (e.g., pandas) and to widen the hand for digging (e.g., some fossorial moles), but the aye-aye's pseudothumb represents what we believe is a heretofore unrecognized third functional role: its accessory digit compensates for overspecialization of its fingers for non-gripping functions (in this case, the aye-aye's unique "tap foraging" practices).
... Recent research in captivity has focused on the aye-aye's sensory capabilities -including the use of scent (Delbarco-Trillo et al., 2013), and vision and response to different frequencies of light (Fuller, 2014;Melin et al., 2012) -and anatomical adaptations (Kaufman et al., 2005Kivell et al., 2010;Soligo, 2004;Moritz and Dominy, 2012;Pellis and Pellis, 2012;Toler, 2011;Toler and Wall, 2013). ...
... Tail and feet comprise less than 25% of G. microtarsus body surface although their contribution to total heat exchange at temperatures above 20˚C-24˚C was considerable. A similar response is found in rabbits and elephant ears [28] [29] [30] [31], guanaco fur [32], penguin feet [33], bird bills [2] [34], digits [35], combs and wattles of several fowl [36], and ungulate horns and antlers [37] [38]. The tail, in particular, is commonly acknowledged as an important organ to modulate radiative heat dissipation via vasomotor adjustments in rats [39] [40] [41]. ...
Full-text available
In this paper, we combine polynomial functions, Generalized Estimating Equations, and bootstrap-based model selection to test for signatures of linear or nonlinear relationships between body surface temperature and ambient temperature in endotherms. Linearity or nonlinearity is associated with the absence or presence of cutaneous vasodilation and vasoconstriction, respectively. We obtained experimental data on body surface temperature variation from a mammalian model organism as a function of ambient temperature us-ing infrared thermal imaging. The statistical framework of model estimation and selection successfully detected linear and nonlinear relationships between body surface temperature and ambient temperature for different body regions of the model organism. These results demonstrate that our statistical approach is instrumental to assess the complexity of thermoregulation in endotherms.
... Likewise, the surface temperature will be close to the ambient temperature, due to peripheral vasoconstriction, to reduce the heat loss (Tattersall and Cadena 2010). Thermal windows have been reported in several mammalian species, including seals (Mauck et al. 2003;Erdsack et al. 2012), mole-rats (Šumbera et al. 2007), otters (Kuhn and Meyer 2009), sea lions (Nienaber et al. 2010), African elephants (Weissenböck et al. 2010), camels (Abdoun et al. 2012), and lemurs (Moritz and Dominy 2012). However, most of these studies were only able to speculate about the actual effectiveness of thermal windows for maintaining homeothermia, because the thermal changes between the body surface and the environment were not quantified. ...
This study aimed to evaluate the diurnal variation of the sensible heat transfer in red-rumped agoutis (Dasyprocta leporina) bred in captivity in a semi-arid environment. In addition, we seek to identify thermal windows by infrared thermography during the daytime period (07:00, 09:00, 11:00, 14:00, and 16:00). The body surface temperature was higher in the pinna (36.84 ± 0.11 °C), followed by the hind limbs (36.55 ± 0.11 °C). These body regions were primarily responsible for heat loss by radiation (which was 10.13 ± 1.17 W m −2 and 11.19 ± 1.17 W m −2 , respectively), and acted like biological thermal windows. Heat transfer by convection was more intense in the body trunk and hind limbs at all times of the day. Thus, sensible heat transfer is important for maintaining homeothermy in red-rumped agouti in hot environments. In conclusion, these rodents use specialized body regions (pinna and hind limbs) for heat transfer.
... Daubentonia is therefore allocated to its own family (Daubentoniidae) and infraorder (Chiromyiformes). The aye-aye is perhaps best known for its acoustic foraging behaviours, termed percussive foraging or tap-scanning [18], and suite of anatomical specializations, particularly in the hand, skull and central nervous system [18][19][20][21][22][23][24][25][26][27]. The elongated middle finger of aye-ayes-described as villiform, filamentous, and grotesquely attenuated-is one of its most outstanding traits, for it is equipped with a unique ball-and-socket metacarpophalangeal joint [24] and capable of extreme mobility [28] and speed (tap intervals of 97.7 ± 19.9 ms [29]). ...
Full-text available
Recent reports suggest that dietary ethanol, or alcohol, is a supplemental source of calories for some primates. For example, slow lorises (Nycticebus coucang) consume fermented nectars with a mean alcohol concentration of 0.6% (range: 0.0–3.8%). A similar behaviour is hypothesized for aye-ayes (Daubentonia madagascariensis) based on a single point mutation (A294V) in the gene that encodes alcohol dehydrogenase class IV (ADH4), the first enzyme to catabolize alcohol during digestion. The mutation increases catalytic efficiency 40-fold and may confer a selective advantage to aye-ayes that consume the nectar of Ravenala madagascariensis. It is uncertain, however, whether alcohol exists in this nectar or whether alcohol is preferred or merely tolerated by nectarivorous primates. Here, we report the results of a multiple-choice food preference experiment with two aye-ayes and a slow loris. We conducted observer-blind trials with randomized, serial dilutions of ethanol (0–5%) in a standard array of nectar-simulating sucrose solutions. We found that both species can discriminate varying concentrations of alcohol; and further, that both species prefer the highest available concentrations. These results bolster the hypothesized adaptive function of the A294V mutation in ADH4, and a connection with fermented foods, both in aye-ayes and the last common ancestor of African apes and humans.
Full-text available
Many ideas have been put forward for the adaptive value of the cassowary casque; and yet, its purpose remains speculative. Homeothermic animals elevate body temperature through metabolic heat production. Heat gain must be offset by heat loss to maintain internal temperatures within a range for optimal performance. Living in a tropical climate, cassowaries, being large bodied, dark feathered birds, are under thermal pressure to offload heat. We tested the original hypothesis that the casque acts as a thermal window. With infrared thermographic analyses of living cassowaries over an expansive range of ambient temperatures, we provide evidence that the casque acts as a thermal radiator, offloading heat at high temperatures and restricting heat loss at low temperatures. Interestingly, at intermediate temperatures, the casque appears thermally heterogeneous, with the posterior of the casque heating up before the front half. These findings might have implications for the function of similar structures in avian and non-avian dinosaurs.
This chapter reviews various bioinspired approaches for the design of fluidic networks in wearable and architectural applications that have common elements to the fluidic mechanisms for biological thermal management. Fluidic cooling mechanisms for building windows can also benefit solar panel design. The chapter summarizes common manufacturing methods for wearable and architectural fluidic designs over large areas, where there are differing general requirements for scale, cost, contained flow, wearability, and mechanical flexibility. The fluidic designs for thermal management of buildings can be generally grouped into three main types: (i) thermal storage in fluidic layers, (ii) forced convection for thermal control, and (iii) fluidic networks for adaptive windows. The chapter also summarizes some of the fabrication methods for larger fluidic networks. It presents a review of various bioinspired approaches for the design of fluidic networks in wearable and architectural applications. © 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Boschstr. 12, 69469 Weinheim, Germany. All rights reserved.
Full-text available
The morphology and function of sensory receptors in the glabrous skin of vertebrates are described. The fundamental characteristics of these receptors are conserved across vertebrate orders, which suggests that they appeared early in vertebrate evolution to sense basic environmental stimuli of universal importance. The specialization and location of certain receptors in the glabrous skin tends to be associated with the evolution of modified dermal structures that are used to detect and evaluate food objects. Selection for specialized foraging behaviors and corresponding sensory receptors also favored the relative expansion of the somatosensory cortex, a trend that is evident across mammals, including humans.
The regulation of the vasculature in the skin is a complex process involving both perivascular nerves and local endothelial‐mediated control. In this study, the perivascular innervation in the mystacial pad of the rat was characterized based upon immunochemical and lectin binding characteristics and distribution. All of the innervation labeled with anti‐protein gene product 9.5 (PGP 9.5), which was used in double‐ and triple‐labeling combinations with the Griffonia simplicifolia lectin (GSA) and antibodies against a variety of neuropeptides, enzymes, and structural proteins. GSA histofluorescence revealed an intricate microvasculature within the rows of tactile vibrissae, which form a natural grid to standardize analyses. Specific features of the vascular organization were confirmed by scanning electron microscopy. Each interval between adjacent vibrissae contained a predictably organized microvascular module composed of separate arterial channels and capillary networks for each of several different structures: papillary muscles, facial muscles, the interior of vibrissal follicle‐sinus complexes, vibrissal papillae, and the upper dermis of the intervibrissal fur. Each module was innervated by at least two sets of sensory, at least two sets of sympathetic, and at least one possible set of parasympathetic. These sets not only differed in their biochemical characteristics, but also in their relative position within the arterial walls and their distribution among the microvasculature to the various structures. As such, the microvasculature to each type of structure had a particular combination of innervation, suggesting that separate neuronal mechanisms may be involved in regulating the blood flow to different types of targets even within the confines of a small territory of tissue. J. Comp. Neurol. 389:545–568, 1997. © 1997 Wiley‐Liss, Inc.
The study of how animals apportion time and energy (energetics) can provide much insight into physiology, ecology and evolution (Bartholomew, 1982; Geiser, 2004; Schmidt-Nielsen, 1997). Body temperature has a profound effect on the ability of animals to function effectively. Since all animals generate heat internally to some extent, energetics is closely linked to the problem of heat management and thermoregulation. For example, homeothermic or ‘warm-blooded’ animals (birds and mammals) must produce a great amount of heat in order to maintain a high and constant body temperature in cold as well as in warm surroundings (Schmidt-Nielsen, 1997). Moreover, natural environments can be extremely variable in their thermal attributes and consequently animals show behavioural and physiological adaptations that enable them to cope with these external gradients.
The study of limb morphology is no longer, as it has been until recently, simply a complement to the study of external characters and the skull, traditionally regarded by systematists and paleontologists as more significant. The concerns of zoologists today are much wider, extending from pure systematics to ecoethology, and the study of the movements involved in locomotion and prehension requires a profound understanding of limb morphology.
Seals have adapted to the high heat transfer coefficient in the aquatic environment by effective thermal insulation of the body core. While swimming and diving, excess metabolic heat is supposed to be dissipated mainly over the sparsely insulated body appendages, whereas the location of main heat sinks in hauled-out seals remains unclear. Here, we demonstrate thermal windows on the trunk of harbour seals, harp seals and a grey seal examined under various ambient temperatures using infrared thermography. Thermograms were analysed for location, size and development of thermal windows. Thermal windows were observed in all experimental sessions, shared some common characteristics in all seals and tended to reappear in similar body sites of individual seals. Nevertheless, the observed variations in order and location of appearance, number, size and shape of thermal windows would imply no special anatomical site for this avenue of heat loss. Based on our findings, we suggest that, in hauled-out seals, heat may be transported by blood flow to a small area of the wet body surface where the elevation of temperature facilitates evaporation of water trapped within the seals' pelages due to increased saturation vapour pressure. The comparatively large latent heat necessary for evaporation creates a temporary hot spot for heat dissipation.
We surgically implanted temperature sensitive telemeters intraperitonealy in free-ranging baboons. Thereafter, we recorded body temperature changes while the baboons were free-ranging and under visual observation. Two distinct patterns of daily body temperature fluctuations occurred; they were related to the availability of drinking water. Core body temperature fluctuated by as much as 5.3°C and regularly exceeded 41°C. Behavioral adaptations of the baboons, notably sandbathing, appeared to be associated with the regulation of body temperature.
Aye-ayes (Daubentonia madagascariensis) locate the mines of xylophagous insects by tapping the middle finger on wood surfaces. When a mine is found, the wood is gnawed away and the prey is extracted, using the same digit [1, 2]. This method of foraging might appear inefficient [3, 4], particularly since wood-boring insect larvae often tunnel long distances [5]. Indeed, in a field study, aye-aye excavations were found not only at the terminus of such mines, where grubs are most likely to be found, but also at their midsections [5], although it remained unclear whether the latter represented errors or placements resulting in prey capture. The mines become secondarily occupied by elaterid, buprestid and tenebrionid beetle larvae, adult katydids, crabs and frogs [5], and Pollock et al. [6] have suggested that aye-ayes may eat both frogs and elaterids. However, it is unknown whether aye-ayes can detect such prey if they are not located in close proximity to woodborers. Further, as they bore forward, coleopteran and lepidopteran larvae pack their mines with masticated wood similar to sawdust (‘frass’) and it is unknown whether the frass aids or interferes with the aye-aye’s detection capabilities. The present study simulates some of these subsurface conditions and provides experimental analysis of the search cues available to aye-ayes.