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Polar Biology ISSN 0722-4060 Polar BiolDOI 10.1007/s00300-014-1446-5
Behavioral audiogram of two Arctic foxes(Vulpes lagopus)
Amanda L. Stansbury, JeanetteA. Thomas, Colleen E. Stalf, LisaD. Murphy, Dusty Lombardi, JeremyCarpenter & Troy Mueller
1 23
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SHORT NOTE
Behavioral audiogram of two Arctic foxes (Vulpes lagopus)
Amanda L. Stansbury • Jeanette A. Thomas •
Colleen E. Stalf • Lisa D. Murphy • Dusty Lombardi •
Jeremy Carpenter • Troy Mueller
Received: 22 September 2013 / Revised: 30 December 2013 / Accepted: 2 January 2014
� Springer-Verlag Berlin Heidelberg 2014
Abstract With increased polar anthropogenic activity,
such as from the oil and gas industry, there are growing
concerns about how Arctic species will be affected.
Knowledge of species’ sensory abilities, such as auditory
sensitivities, can be used to mitigate the effects of such
activities. Herein, behavioral audiograms of two captive
adult Arctic foxes (Vulpes lagopus) were measured using a
yes/no paradigm and descending staircase method of signal
presentation. Both foxes displayed a typical mammalian
U-shaped audiometric curve, with a functional hearing
range of 125 Hz–16 kHz (sensitivity B 60 dB re: 20 lPa)
and average peak sensitivity of 24 dB re: 20 lPa at 4 kHz.
The foxes had a lower frequency range and sensitivity than
would be expected when compared to previous audiograms
of domestic dogs (Canis familiaris) and other carnivores.
These differences indicate Arctic foxes (V. lagopus) may
have a lower frequency range than previously expected,
which was similar to the only other fox species tested to
date, kit foxes (Vulpes macrotis). Alternatively, differences
may be due to testing constraints, such as masking of test
signals by ambient noise and/or an unintentionally trained
conservative response bias, which most likely resulted in
underestimated hearing curves. While results of this study
should be interpreted with caution due to its limitations,
findings indicate that foxes have a narrower frequency
range than formerly presumed. Anthropogenic activities
near fox habitats can mitigate their impacts by reducing
noise at frequencies within the functional hearing range
and peak sensitivities of this species.
Keywords Arctic fox � Vulpes lagopus � Hearing �Behavioral audiogram
Introduction
Mammals have a highly developed and specialized sense of
hearing, with increased amplitude sensitivity and broader
frequency ranges, compared to other vertebrates (Stebbins
1980). There is considerable variation in the auditory
capabilities among mammals, with species-specific curves
ranging across several octaves (Heffner and Heffner 1982).
While audiometric tests have only been conducted on a
fraction of mammalian species, known hearing curves
could be used to predict the expected frequency ranges and
sensitivities for related, but untested, species.
There has been very little investigation into the auditory
capabilities of one group of mammals: foxes. In particular,
the sensory abilities of Arctic foxes (Vulpes lagopus) are of
interest because of increased anthropogenic activity in
Arctic regions. The oil and gas industry is coming under
increasing pressure to mitigate noise associated with their
operations which may harass or harm wildlife (Wagner and
Armstrong 2010). For oil and gas companies to
Electronic supplementary material The online version of thisarticle (doi:10.1007/s00300-014-1446-5) contains supplementarymaterial, which is available to authorized users.
A. L. Stansbury � J. A. Thomas
Department of Biological Sciences, Western Illinois University,
Moline, IL 61265, USA
A. L. Stansbury (&)
Sea Mammal Research Unit, Scottish Oceans Institute,
University of St. Andrews, East Sands KY16 9LB, Scotland, UK
e-mail: stansbury.amanda@gmail.com
C. E. Stalf � L. D. Murphy
Niabi Zoo, Coal Valley, IL 61240, USA
D. Lombardi � J. Carpenter � T. Mueller
Columbus Zoo and Aquarium, Powell, OH 43065, USA
123
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DOI 10.1007/s00300-014-1446-5
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appropriately design equipment and modify procedures to
minimize noise pollution, it is important to know the
hearing sensitivity of Arctic foxes (V. lagopus), especially
at frequencies of sounds produced by anthropogenic
activities.
No previous investigations have measured the hearing
curve of the Arctic fox (V. lagopus). However, their sen-
sitivities may be predicted by comparison to closely related
species. The hearing ability of only one canid species, the
domestic dog (Canis familiaris), has been tested. Behav-
ioral audiograms of four dog breeds were obtained using a
yes/no paradigm by Heffner (1983). The dog audiograms
ranged from 50 Hz to 46 kHz (B60 dB re: 20 lPa) and
peak sensitivity of 0–10 dB re: 20 lPa at 8 kHz. An
abstract on the acoustic sensitivities of one fox species, the
kit fox (Vulpes macrotis), was published by Bowles and
Francine (1993). Hearing thresholds of four wild-caught
foxes were measured using a startle response to playbacks
of tones and were found to have a functional hearing range
of 1–20 kHz. Amplitude sensitivity was not reported, with
the exception of the peak sensitivity which was -15 dB re:
20 lPa between 2 and 4 kHz (Bowles and Francine 1993).
Carnivores tend to be more sensitive to ultrasonic fre-
quencies compared to other mammals. When considering
terrestrial carnivores, the high-frequency limits range from
44 kHz in the ferret, Mustafa putorius, (sensitivity is 60 dB
re: 20 lPa; Kelly et al. 1986) to 85 kHz for the domestic
cat, Felis catus, (sensitivity is 70 dB re: 20 lPa; Heffner
and Heffner 1985). As a carnivore, the foxes’ high-fre-
quency limit would be expected to fall within this range.
However, the kit foxes’ high-frequency limit was 20 kHz
(Bowles and Francine 1993), suggesting fox species may
have a lower high-frequency limit than other carnivore
species.
The present study documented the functional audiogram
of the Arctic fox (V. lagopus).
Materials and methods
Subjects and facilities
Two 1-year-old male Arctic foxes (V. lagopus), ‘‘Brutus’’
and ‘‘Cassius,’’ were the test subjects of this study. The
foxes were farmed, captive-born siblings. Both were naive,
and initial training was conducted at an indoor facility at
the Niabi Zoo (Coal Valley, Illinois) starting in February
2009. Their diet consisted of dry Mazuri� Exotic Canine
Diet, and the majority of the daily ration was used during
training sessions. In February 2010, they were moved to
Columbus Zoo and Aquarium in Powell, Ohio, where
training was completed and all test sessions occurred. In
Columbus, both foxes were fed about � of their daily
ration before 0900 h each day, and no additional food was
given until test sessions each afternoon. Testing was
completed in August 2010.
The foxes were tested individually in an indoor, off-
exhibit cement room (1.29 9 2.21 9 1.52 m) attached
behind the public display area. A chain-link fence sepa-
rated the animals from a small maintenance area, which
housed the test equipment and separated the researcher and
trainer from the foxes during sessions (see Online Resource
1 for a diagram of the testing enclosure). While one fox
was tested, the other remained on public exhibit.
Test apparatus and stimuli
The testing area consisted of a center stationing target and
a response paddle to either side. Each fox had a unique
target consisting of a PVC handle with a small (approxi-
mately 25 mm diameter) plastic shape attached at the tip.
This target was used to call the animal to station before
initiating trials. When at station, the animal sat directly in
front of the target and touched the target with its nose,
which oriented the head toward the speaker. Between trials,
the target was removed and the animal was free to roam
within the enclosure until recalled for the next trial. To the
right of the fox’s center station was a signal-present (or
‘‘sound’’) response paddle, and to the left was a signal-
absent (or ‘‘no sound’’) response paddle. Both paddles were
suspended from the fence by a PVC pole, placed 0.75 m
away from the center station.
Test equipment
A sinusoidal test signal was generated using a Wavetek
model 90 function generator. Hearing sensitivity between
40 Hz and 64 kHz was tested in approximate octave
intervals, with additional frequencies tested at the lower
and upper threshold limits. Test frequencies included the
following: 40, 50, 62.5, 125, 250, 500, 1,000, 2,000, 4,000,
8,000, 16,000, 32,000, 48,000, and 64,000 Hz signals.
Only one frequency was presented during a session, and
each frequency was tested over multiple sessions until a
threshold was obtained, which took between two and four
sessions per frequency.
To project a test signal, the researcher activated the
signal with a remote control connected to a signal-condi-
tioning box developed by Whitlow Au (Tremel et al. 1998).
This conditioning box had an attenuator with a 90-dB
range, set the duration of the signal to 1.62 s, and con-
trolled the rise and fall time to 190 ms. Signals were pre-
sented at a randomly predetermined interval between 2 and
14 s after the fox stationed and the researcher activated the
remote control. To confirm signal projection, a Tektronix
2245A oscilloscope monitored the outgoing signal. An
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Onkyo speaker and amplifier system (model CS415, linear
frequency response of 40 Hz to 100 kHz) projected the
signal and was mounted 0.75 m in front of the fox’s
station.
Measurement of signal and ambient noise level
Sound pressure level (SPL) measurements were taken at
the position of the animal’s station, 0.75 m directly in front
of the speaker. The projected signal level was measured
using either a Quest 2700 digital SPL meter (sensitivity
between 4 Hz and 50 kHz at 35–140 dB ± 3 dB) with a
linear weighting or a TDJ-824 SPL meter (sensitivity
between 31.5 Hz and 8.5 kHz at 30–130 dB ± 1.5 dB)
with a C-weighting. Measurements taken with C-weighting
were corrected and reported as with a linear weighting. All
projected signal levels were verified for each frequency
before the study, every 2 weeks during tests, and after
testing. Which SPL meter was used depended on the test
frequency, and both SPL meters were calibrated before
testing using a B and K calibrator. Signal levels were
additionally verified throughout testing using the oscillo-
scope monitoring the outgoing signal.
Because testing occurred in a zoo environment, ambient
noise could not be eliminated. The ambient noise level was
sampled throughout sessions using the TDJ-824 SPL meter.
If ambient noise levels exceeded 50 dB re: 20 lPa, testing
was paused until ambient noise dropped. While typically
in-air SPL measurements are made 3 feet (0.914 m) away
from the source, due to space constraints in the testing
environment, this was not possible. Sample recordings of
background noise were made using a Lenovo laptop with a
built-in microphone (sampling rate 44 kHz, 24 bits, 1/3
octave bands, arithmetic average of peaks using peak root
mean square). Signal levels of each test frequency were
verified using a known amplitude sinusoidal calibration
signal in the software program, SpectraPLUS 5.0.
Test procedures
All behaviors were trained using positive reinforcement by
pairing an acoustic bridge (clicker) with food reinforce-
ment (kibble). Throughout testing, a modified yes/no par-
adigm was used. In each trial, a sinusoidal tone was either
present (yes) or absent (no), and the subject was required to
respond differentially (Green and Swets 1966). If the
stimulus was present, the fox was required to stand behind
the signal-present response paddle (right). If it was absent,
the fox was trained to stand behind the signal-absent
response paddle (left). Using traditional yes/no methods,
the subject was required to remain at the station for a given
period of time until a cue released the subject to respond.
This method was adapted for the highly active Arctic fox
(V. lagopus) such that the fox was allowed to leave station
immediately upon perceiving the tone, rather than waiting
for a cue to choose its response. This ensured the time
between the presentation of the tone and being released to
respond did not affect the subjects’ performance. While
this procedure is similar to a go/no-go design (i.e., the
subject leaves the station upon presentation of a stimulus or
remains at station if no stimulus is presented), a preferen-
tial bias favoring either the go or no-go conditions could
affect results. During training, both foxes displayed an
initial bias in favor of the ‘‘go’’ condition, so during testing,
they were required to leave the station for both conditions.
When no sound was presented, a hand cue (pointing at the
signal-absent response paddle) indicated to the fox to leave
station. This removed the previous bias in favor of the
‘‘go’’ condition.
During tests, an equal number of signal-present and
signal-absent trials per block were randomly assigned using
a Gellerman series (Gellerman 1933) with eight trials per
block. The first block was a ‘‘warm-up’’ in which tone
amplitudes were played at an easily audible level ([90 dB
re 20 uPa). If the fox’s performance during the warm-up
block was[80 % (i.e., the fox did not miss more than two
of eight trials), testing continued. A descending staircase
method of signal presentation was used (Fay 1988) in
which amplitude was decreased in 3-dB steps after a cor-
rect response and was then increased in 5-dB steps after an
incorrect response.
Each trial started with the presentation of the stationing
target centered between the two response paddles. This cue
signaled the fox to station. Once the animal stationed (i.e.,
sat directly in front of the target, with the head oriented
toward the speaker), the trainer said ‘‘station,’’ and the trial
began. Either a signal-present or signal-absent cue was
projected at a random interval between 2 and 14 s. For the
signal-present trials, a tone was played and the fox was
reinforced with three to four pieces of kibble for moving to
and standing behind the signal-present paddle. For the
signal-absent trials, the trainer gave a hand cue (pointing to
the signal-absent paddle) and the fox was reinforced with
three to four pieces of kibble for moving to and standing
behind the signal-absent paddle.
For incorrect responses, a time-out of 2–3 s occurred
before re-stationing the fox. This occurred either with a
miss (when a tone was played but the fox did not respond
to the signal present) or a false alarm (when no tone was
played but the fox responded signal present). However,
below threshold, the fox was expected not to perceive the
tone and thus would remain at station. This would be an
incorrect response, and thus, the fox received an error time-
out although the fox was behaving as trained. This could
potentially frustrate and confuse the fox. To prevent frus-
tration and encourage correct performance of the trained
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behaviors, if a tone was presented near threshold (within
5 dB of the estimated hearing threshold) and the fox did
not leave station within 3 s, the fox was given a hand cue to
touch the signal-absent paddle and reinforced with one
piece of kibble. The varied magnitude of reinforcement
(one piece of kibble when the fox was assumed to have not
perceived the stimulus versus three to four pieces of kibble
for an appropriate response) encouraged correct responses
near threshold while preventing frustration. The response
was recorded as being incorrect, and the amplitude
increased by 5 dB accordingly for the next trial.
Two precautions were used to prevent the trainer from
unintentionally cueing the subject to the correct
response: (a) The trainer could not hear the test tone
because she wore a noise-reducing headset (Talkabout
T6500), which attenuated sound by up to 32 dB and
(b) the equipment operator (outside the testing area)
indicated to the trainer, via the headset, when to bridge
and reinforce the fox for an appropriate response.
Although the trainer was able to hear some high-ampli-
tude test signals, tones near the foxes’ hearing threshold
were not audible to the trainer.
Calculation of the hearing threshold
Reversals (the dB level at which the fox responded incor-
rectly and the dB level at which the fox subsequently
responded correctly) were averaged over all sessions of a
particular frequency and were used to estimate the hearing
sensitivity threshold for that frequency (see Online
Resource 2). A minimum of 15 reversals were averaged for
each test frequency to obtain the hearing threshold. The
number of blocks per session varied, depending on how
quickly the fox reached the first reversal, but was never
more than 80 trials per session. If the fox responded
incorrectly during [50 % of the trials in a block (i.e., the
fox missed four of eight trials), the session was ended to
prevent frustration. The last block was a ‘‘cool-down’’ in
which all signal amplitudes were played at [90 dB. Data
from a session were judged to be acceptable if the fox’s
performance during the cool-down block was [80 % cor-
rect (i.e., the fox did not miss more than two of eight trials).
The functional frequency range was reported as the fre-
quencies at which the fox responded with an amplitude
sensitivity of \60 dB re: 20l Pa. To evaluate potential
masking, the sum of the critical ratios and the spectrum
level of the masking noise were used to approximate the
lowest possible masked threshold. The critical ratios were
estimated by taking 10 times the log of the center fre-
quency divided by 10 (Fay 1988). Then, 1/3 octave band
noise levels were converted to spectrum level by sub-
tracting 10 times the log of 23 % of the center frequency.
Thresholds within 5 dB of the estimated level were
assumed to be masked. Estimated masking thresholds were
reported for each test frequency up to 16 kHz.
Results
Hearing thresholds
Testing occurred over 32 sessions per fox, with a total of
3,882 trials. The number of reversals per frequency, the
average signal level over all reversals, and the percentage
of false alarms for each test frequency are summarized in
Table 1. At 40 Hz, both foxes performed at chance (i.e.,
50 % accuracy, or 4 out of 8 trials) for 96 dB re: 20 lPa
signals, so no threshold was obtained. The lowest fre-
quency the foxes responded to was 50 Hz, with a sensi-
tivity of 86 dB re: 20 lPa. The foxes were most sensitive to
4 kHz tones. Sensitivity declined at higher frequencies, and
at 64 kHz, neither animal responded so no threshold was
measured. To find the upper-frequency limit, 48 kHz was
tested (i.e., midway between 32 and 64 kHz). At 48 kHz,
the sensitivity was 86 dB re: 20 lPa. The functional
hearing range (B60 dB re: 20 lPa) was 125 Hz–16 kHz.
Both foxes performed consistently across test frequencies,
and all standard deviations around threshold were below
approximately 4.2 dB for Brutus and 9.4 dB for Cassius.
Table 1 Hearing thresholds in dB re: 20 lPa and summary statistics
on reversals for two Arctic foxes (Vulpes lagopus) reported by test
frequency
Test
frequency
(Hz)
Number of reversals
per fox
Threshold
in dB
Percentage
false alarms
40 Chance
performance
50 15/17 87/85 8.5/4.3
62.5 16/15 77/73 4.3/4.4
125 18/18 59/58 5.7/7.2
250 15/15 44/49 4.1/1.8
500 17/15 43/41 5.8/6.6
1,000 15/15 33/33 4.5/3.8
2,000 20/16 27/28 5.5/2.3
4,000 16/15 22/25 3.4/0.5
8,000 19/16 27/29 4.4/5.3
16,000 15/16 51/48 1.4/7.0
32,000 15/16 73/73 5.8/6.8
48,000 15/15 86/86 10.8/4.9
64,000 No response
Results are reported for Brutus and then Cassius (i.e., 15/17 indicates
15 for Brutus, 17 for Cassius). The number of reversals averaged to
obtain a threshold, the estimated threshold level, and the occurrence
of false alarm percent (number of false alarms divided by total
number of trials multiplied by 100) are listed
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The audiograms of both foxes are shown in Fig. 1, super-
imposed over calculated masking threshold levels at each
test frequency. In Fig. 2, the foxes’ audiograms are com-
pared to the audiogram of domestic dogs (C. familiaris)
tested by Heffner (1983).
Estimated masking thresholds
Ambient noise during sessions ranged from 46 to 55 dB re:
20 lPa. Overall noise was broadband, with some electrical
noise concentrated below 100 Hz. Ambient noise was
highest at low frequencies, with a peak at 500 Hz. The
lowest possible masked threshold was calculated as the
sum of the assumed critical ratios and the spectrum level of
the ambient noise and is plotted against both foxes’
thresholds in Fig. 1. The threshold of the fox was within
5 dB of the estimated masking threshold at 250, 500,
1,000, and 2,000 Hz. Thresholds at these frequencies were
assumed to be masked. It should be noted that the equip-
ment used to make these measurements was not ideal; a
laptop and in-built microphone were used. These values
provided an estimate of the background noise for fre-
quencies tested up to 16 kHz, but should not be taken as
absolute.
Discussion
Functional hearing thresholds
The functional hearing range of the Arctic fox (V. lagopus;
B60 dB re: 20 lPa) was between 125 Hz and 16 kHz, with
peak sensitivity of 24 dB at 4 kHz. The foxes’ hearing was
not as sensitive as in domestic dogs (C. familiaris; Heffner
1983). Heffner (1983) did not report ambient noise levels
because the dog tests occurred in an anechoic chamber and
environmental noise was very low. The hearing sensitivity
differences between the fox and dogs could be due to
higher ambient noise during our study. Based on the kit
foxes’ (V. macrotis) peak sensitivity (-15 dB re: 20 lPa
between 2 and 4 kHz; Bowles and Francine 1993), the
Arctic foxes (V. lagopus) were also less sensitive than kit
foxes (V. macrotis).
The decreased sensitivity compared to other species
could indicate that the current investigation underestimated
the full frequency range of Arctic foxes (V. lagopus). The
study was limited because it was conducted in a zoo
environment and masking potentially underrated the spe-
cies’ auditory capabilities. Data on critical ratios are not
available for any canid species to interpret the degree of
masking that might have occurred in this study. However,
at test frequencies of 250, 500, 1,000, and 2,000 Hz,
thresholds overlapped the estimated masking threshold,
which was calculated using an assumed critical ratio typi-
cal of many mammals, and so the thresholds were assumed
to be masked. Test equipment was limited and only
examined ambient noise levels for test frequencies up to
16 kHz. Ambient noise levels at ultrasonic frequencies
were not known. However, it is not expected that ambient
noise levels at the ultrasonic test frequencies (32 and
48 kHz) would have approached the foxes’ tested thresh-
olds (approximately 70 dB re: 20 lPa at 32 kHz). The low/
upper-frequency limit of the foxes’ hearing in this study is
not believed to be masked by ambient noise.
Fig. 1 Behavioral audiograms of two captive Arctic foxes (Vulpes
lagopus). The functional hearing range was defined at a threshold
level B60 dB re: 20 lPa, or from 125 Hz to 16 kHz. Average peak
sensitivity, the lowest threshold amplitude detected, was 24 dB at
4 kHz. Hearing thresholds are superimposed over calculated masking
thresholds (the sum of the assumed critical ratios and the spectrum
level of the ambient noise)
Fig. 2 Behavioral audiogram of two Arctic foxes (Vulpes lagopus)
compared with the lowest and highest hearing thresholds of four
breeds of domestic dogs (Canis familiaris, thresholds averaged across
all tested dogs). Data taken from Heffner (1983)
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Given the hearing abilities of the domestic dog (C. fa-
miliaris) and other carnivores, Arctic foxes (V. lagopus)
have a lower than expected upper-frequency limit. How-
ever, the upper-frequency limit is similar to the only other
fox species tested to date, kit foxes (V. macrotis). Fox
species may have a smaller frequency range than previ-
ously anticipated. However, the training paradigm used
herein may have also affected the measured thresholds;
both foxes maintained a low false alarm rate throughout the
tests. This is consistent with the bias Schusterman (1974)
observed in hearing studies on pinnipeds where initial
training and experience of the subject were found to create
a conservative bias. Using traditional psychophysical
methods, false alarm rates are limited to ensure good
stimulus control during tests and sessions exceeding a
specified false alarm rate are disregarded. Thresholds
obtained with a more liberal bias would likely be lower,
and the frequency range wider than what is suggested by
the current audiogram.
Implications
The audition of Arctic foxes (V. lagopus) is of particular
interest to the oil and gas industry working in Arctic
regions. Based on the auditory range and amplitude sen-
sitivities found in this study, companies should design
equipment and modify procedures to minimize the impact
of anthropogenic noise on the fox. Typical anthropogenic
activity falls within the foxes’ audible range; for example,
in-air noise from an Arctic oil pile driving operation was
found to be highest between 100 Hz and 6 kHz (Blackwell
et al. 2004). Ideally, anthropogenic noise above or below
the foxes’ threshold, i.e., below 125 Hz or above 16 kHz,
would have the least impact on this species. However, as
this may not be feasible, efforts to reduce amplitude levels
at these frequencies would be beneficial, and especially
noise within the maximum hearing sensitivity range of the
Arctic fox (V. lagopus), 2–4 kHz, should be minimized.
Conclusions
The functional hearing range of the Arctic fox (V. lagopus;
B60 dB re: 20lPa) was 125 Hz–16 kHz with a peak sen-
sitivity of 24 dB at 4 kHz. Compared to the domestic dog
(C. familiaris) and other carnivores, this best hearing fre-
quency range and sensitivity were lower than expected.
Masking and training strategies may have underestimated
the frequency limits of the foxes. Alternatively, fox species
may have a lower upper-frequency limit than previously
expected as the range was similar to the only other fox
species tested to date. Future research could test the
validity of these results using a more controlled behavioral
audiogram or an auditory evoked potential study. Addi-
tionally, the foxes tested in this study were farm bred and
results may not be applicable to wild populations. Further
evaluation of other fox species, including wild populations,
would be valuable.
Acknowledgments This research was conducted as a master’s
thesis at Western Illinois University. The Department of Biological
Sciences at Western Illinois University (WIU) contributed all of the
test equipment. The study was partially funded by a student grant
from the WIU Graduate School. Food and animal costs were donated
by the zoos. The critiques by Dr. Brian Peer and Dr. Jeff Engel and by
external reviewers, especially Jack Terhune, were invaluable to pro-
ducing this publication. The authors thank Laura Monaco Torelli and
Tara Gifford for advising training procedures, and Marc Silpa, Nicole
Spinoza, Kirk Massey, and the keepers of the Columbus Zoo for
volunteering time and making this research possible.
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