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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

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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

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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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