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

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 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.

Full text

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 .
Thermography
Int J Primatol (2012) 33:588–597
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
e-mail: Gillian.L.Moritz@Dartmouth.edu
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

Introduction
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 =31.0–32.2°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
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 “parked”to 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 5–120°C). For each thermograph, we recorded the state
of flexion of the MP joint and estimated the surface temperature of individual digits
(T
digit
) 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
digit
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 Chancellor’s
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
digit
of each visible digit and used these values as independent
sample points. To compare variation in T
digit
within each test condition, i.e., state of
MP extension or flexion, we used one-way ANOVAs and Tukey’spost hoc test of
honestly significant differences (HSD). To compare variation in T
digit
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.
Results
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
:F
2,52
=1.3,
p=0.88) or extended (T
digits II, IV, V
:F
2,129
=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
3,184
=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
activity.
Table II Effects of MP joint extension and flexion on the mean surface temperature (±1 SD) of individual
digits (T
digit
)
Extension at MP joint Flexion at MP joint
Digit Nimages Mean T
digit
†
Nimages Mean T
digit
†
Mean difference p
‡
II 42 27.8± 2.5
a
(22.7–31.9) 20 28.5± 1.8
a
(24.3–31.4) 0.7 0.253
III 55 24.9± 1.7
b
(21.0–27.8) 34 26.9± 2.1
b
(22.7–30.5) 2.0 <0.0001
IV 58 27.4± 2.6
a
(23.0–30.8) 18 28.5± 1.8
a
(23.8–31.4) 1.1 0.711
V 21 26.5± 2.5
a
(22.3–29.9) 3 28.4± 1.3
a,b
(25.1–30.8) 1.9 0.049
†
Within-condition test, ANOVA Tukey’s 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

Discussion
Here we report estimates of digital surface temperatures (T
digit
) 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

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