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Effects of Environmental Complexityand Temporary Captivity on ForagingBehavior of Wild-Caught Meadow VolesAmaranta E. Kozucha & M. Elsbeth McPheea
a Department of Biology and Microbiology, University ofWisconsin–OshkoshPublished online: 21 Feb 2014.
To cite this article: Amaranta E. Kozuch & M. Elsbeth McPhee (2014) Effects of EnvironmentalComplexity and Temporary Captivity on Foraging Behavior of Wild-Caught Meadow Voles, Journal ofApplied Animal Welfare Science, 17:2, 157-171, DOI: 10.1080/10888705.2014.881256
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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 17:157–171, 2014
Copyright © Taylor & Francis Group, LLC
ISSN: 1088-8705 print/1532-7604 online
DOI: 10.1080/10888705.2014.881256
Effects of Environmental Complexity andTemporary Captivity on Foraging Behavior of
Wild-Caught Meadow Voles
Amaranta E. Kozuch and M. Elsbeth McPhee
Department of Biology and Microbiology, University of Wisconsin–Oshkosh
Increased housing of wild nonhuman animals in captivity for conservation, research, and rehabili-
tation has revealed the importance of systematically analyzing effects of the captive environment
on behavior. This study focused on the effects of complexity and time held in captivity on foraging
behaviors of wild-caught, adult meadow voles (Microtus pennsylvanicus). Forty-six individuals
captured from a meadow outside Oshkosh, WI, were assigned to 1 of 4 captive treatment groups:
simple/<50 days (SS), simple/>50 days, complex/<50 days, and complex/>50 days. Number of
dish visits, proportion foraging, and frequency of nonforaging behaviors recorded during a 15-
min foraging trial were measured for all subjects. Kruskal-Wallis and Mann-Whitney U Tests
were conducted to analyze 4 different comparisons within this behavioral data. Overall, neither
time in captivity or environmental complexity affected nonforaging behaviors. In contrast, foraging
behaviors did change with treatment: Voles were less active at food dishes and visited control dishes
more in treatment group SS than in the other treatment groups. In addition, sex-related differences
in foraging behaviors were maintained when voles were exposed to environmental complexity. This
article includes options for wildlife managers to adapt captive environments to meet the welfare
and behavioral needs of translocated wild nonhuman mammals.
Keywords: environmental complexity, captivity, foraging, wild-caught, sex-related differences
The need to provide nonhuman animals in captivity with an environment that promotes en-
hanced well being and maintains species-typical behaviors has become increasingly important
as captive housing is more commonly used in conservation, research, and rehabilitation. The
use of social (Schrijver, Bahr, Weiss, & Wurbel, 2002), physical (Simonsen, 1990), sensory
(Shepherdson, Bemment, Carman, & Reynolds, 1989), or feeding enrichment (Rooney &
Sleeman, 1998) can significantly improve the overall welfare of animals housed in captivity
temporarily or indefinitely. An environment void of species-appropriate stimuli has been shown
Correspondence should be sent to M. Elsbeth McPhee, Department of Biology and Microbiology, University of
Wisconsin–Oshkosh, 800 Algoma Boulevard, Oshkosh, WI 54901. Email: [email protected]
157
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158 KOZUCH AND MCPHEE
to restrict an animal’s ability to perform species-typical behaviors (Lambert, Fernandez, &
Frick, 2005; Shivik, Palmer, Gese, & Osthaus, 2009; Wurbel, Chapman, & Rutland, 1998),
giving rise to abnormal behavior such as stereotypic pacing (Mallapur & Chellam, 2002) or
digging (Wiedenmayer, 1997). The provision of challenging and behaviorally relevant activities
in captivity, however, may elicit the expression of naturalistic behaviors and the maintenance
of appropriate skills (Carlstead, Seidensticker, & Baldwin, 1991; Newberry, 1995; Stoinski &
Beck, 2004), thereby improving the welfare of captive animals (Baumans, 2011; Lewis, Presti,
Lewis, & Turner, 2006; Shepherdson, 1999).
Numerous studies conducted on a variety of species across taxa provide support for de-
signing captive enclosures that incorporate complex and dynamic characteristics known as
environmental enrichment (Beck & Castro, 1994; Beck, Castro, Stoinski, & Ballou, 2002;
Burrell & Altman, 2006; Novak, O’Neill, Beckley, & Suomi, 1994). Enrichment provides
valuable stimuli that help deter aberrant behaviors and elicit a range of behaviors similar to
those observed in the wild (Carlstead & Shepherdson, 1994; Shivik et al., 2009). Jensvold,
Sanz, Fouts, and Fouts (2001) observed a near doubling of time spent traveling and an increase
in locomotor behaviors in captive chimpanzees (Pan troglodytes) when increased captive space
and complexity were provided. The study concluded that the combination of environmental
factors encouraged the expression of species-typical motor behaviors.
In bank voles (Clethrionomys glareolus), however, those deprived of complexity were more
likely to develop stereotypies than were those deprived of adequate space (Odberg, 1987).
Similarly, the proportion of stereotypical behaviors in captive leopards (Panthera pardus) was
shown to decrease with the increase of natural activity after the addition of structural objects
(Mallapur & Chellam, 2002).
Most animals in the wild spend a high proportion of their daily activity budgets in foraging
behaviors (Herbers, 1981). Therefore, providing complexity to captive animals can increase
perceived opportunities to forage. The use of objects, increased cage size, complexity in the
form of natural substrates, food variety, and social grouping was shown to increase the feeding
and exploratory behaviors of bobcats (Lynx rufus; Molla, Quevedo, & Castro, 2011). Adding
food-related enrichment, such as browsing, frozen treats, and hiding items in manipulable
objects, increases time spent on foraging activities and can elicit immediate behavioral changes
as long as food is present (Altman, 1999). McPhee (2002) was able to significantly decrease
off-exhibit stereotypical behavior in nine captive felines by providing intact calf carcasses.
In the wild, behaviors such as foraging are the result of constant tradeoffs between energy
gain, energy loss, and risk. There are no such tradeoffs in captivity because of the predictable
availability of food and decreased risk. Enrichment, however, can provide opportunities for
animals to make complex choices and thus maintain efficient foraging behavior. For example,
Cheal (1987) found that enriched Mongolian gerbils (Meriones unguiculatus) forage more
rapidly than do gerbils who experienced little or no enrichment, thus suggesting that enriched
animals still incorporate the idea of risk in their foraging decisions. To date, however, few
researchers have systematically examined the effects of environmental complexity during tem-
porary captive housing on foraging behavior in animals caught in the wild.
Thus, we investigated the effects of barren and complex environments over two time periods
during temporary captive housing on the foraging repertoires of meadow voles (Microtus penn-
sylvanicus) caught in the wild. We hypothesized that (a) time in captivity would erode foraging
behaviors, but (b) environmental complexity would maintain natural foraging behaviors in
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 159
animals housed in captivity. To test these hypotheses, we measured changes in foraging behavior
as a function of complexity of the housing environment and time in captivity. We predicted that
the less time an animal had been in captivity, the more active their foraging behavior would
be, and that animals housed in a simple environment would express fewer foraging behaviors
and be less persistent foragers compared with those housed in a complex environment.
MATERIALS AND METHODS
Subjects
Adult, wild meadow voles were captured within a wet meadow located on Winnebago County
Park property in Oshkosh, WI (latitude, 44.024ıN; longitude, �88.542ıW). They were brought
into the University of Wisconsin–Oshkosh animal facility during two separate trapping sessions:
May 11, 2011, to June 15, 2011, and June 29, 2011, to July 9, 2011. The weights at the time they
were captured in the wild were used to distinguish between subadult and adult individuals: 22 g
to 33 g and �34 g, respectively (Krebs, Keller, & Tamarin, 1969; Myers & Krebs, 1971); only
adults were brought into the lab. Subsequent habituation to the foraging arena and behavioral
testing were conducted during the 1st and 2nd weeks of August 2011.
Animals brought into captivity were quarantined for 2 weeks in a room separate from the
general housing room. Individuals were injected with a broad spectrum antiparasitic, ivermectin
(1:10 mL in water dilution, 1 mL/0.2 kg dosage), and were given a full external body rub with
a cloth moistened with Adams Flea and Tick mist immediately upon arrival at the laboratory.
Animal Welfare Ethics
The wild meadow voles included in this study were part of a larger trapping effort to gather a
founder population to start a breeding program. Meadow voles were captured from the same
location over two trapping intervals during the summer of 2011. Twenty-four of the captured
individuals during May 11, 2011, to June 15, 2011, were held in captivity for no longer than
100 days. Twenty-two individuals from the trapping interval from June 29, 2011, to July 9, 2011,
were held no longer than 50 days in the assigned environment. A total of 46 individuals were
captured to be used in this study during the two time periods: 26 females and 20 males (Table 1).
Of the 26 females, 15 were pregnant and were allowed to give birth in captivity. Females
were not pregnant while they were tested for their foraging response. Animal welfare and
health were monitored according to approved Institutional Animal Care and Use Committee
protocols. The number of individuals collected from the wild was permitted under the permit
#SRL-NER-228 from the Wisconsin Department of Natural Resources.
Experimental Groups and Captive Housing
Adult individuals were assigned randomly to either a complex or simple environmental group
(Table 1), but consideration was taken to balance the sexes within each treatment. Within
these groups, animals were further divided by time of capture and length of stay in captive
environment (>50 days [long], <50 days [short]). Thus, animals were in one of four treatment
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160 KOZUCH AND MCPHEE
TABLE 1
Sample Size of Individuals Assigned to Environment
(Simple and Complex) and Amount of Time Held in Captivity
(Short: <50 days; Long: >50 days)
Captive Lines Complex Simple Total
Long 8♀ 4♂ 5♀ 7♂ 13♀ 11♂ (24)
Short 6♀ 5♂ 7♀ 4♂ 13♀ 9♂ (22)
Total 14♀ 9♂ (23) 12♀ 11♂ (23) 46
Note. Total of four treatment groups (n D 46).
groups: complex long (CL), complex short (CS), simple short (SS), and simple long (SL). To
minimize differences due to age and experience in the wild prior to captivity, subadult meadow
voles were not included in this study.
The housing room was lit with fluorescent bulbs, which remained on a 14:10-hr light cycle
to simulate summer conditions. Rat chow pellets (Tekland #8604) and water were provided ad
libitum in both environments. Sunflower seeds were given three times a week to supplement
their diet (�10 seeds per individual per time).
Simple and complex environments were defined by differences in substrate, amount of
space, and presence of unpredictable environmental elements provided in the cage. Simple
environmental cages were standard mouse cages measuring 27.9 cm � 17.8 cm � 15.2 cm
(8-quart; per Guide for the Care and Use of Laboratory Animals, National Research Council,
1996) and lined with sani-chip bedding; a cotton-fiber nesting square was also placed in the
cage.
Complex environmental cages were 58.4 cm � 41.4 cm � 31.4 cm (56-quart) Sterilite
containers with removable lids. The lid was modified to allow for airflow by removing the
center and replacing it with 0.6 cm of mesh (�50.8 cm � 33 cm). The containers were also
modified to hold one water bottle and an adjacent feeding dish. Two substrates were used to line
the complex cage: sani-chip bedding for sanitation purposes and orchard grass hay to simulate
natural substrate. Novel objects were provided to individuals on a weekly rotation (see online
Supplementary Table 1) to promote expression of naturalistic behaviors. The environmental
cage was assumed to be initially novel; therefore, no objects were given during the 1st week.
Several of the objects were used a second time (after one full rotation of all objects) for
individuals assigned to the CL environment because the number of weeks in captivity was
greater than the number of objects provided. Objects were randomly assigned to present an
element of unpredictability that helped ensure an object’s novelty (Paquette & Prescott, 1988).
All cages were fully cleaned once a week, and a second weekly cleaning was performed
if it was needed. Housing and experimental procedures were approved by the University of
Wisconsin–Oshkosh’s Institutional Animal Care and Use Committee.
Behavioral Testing
Foraging behavior was tested in a 0.8 m � 1.1 m black plastic arena. All individuals were
habituated to the testing arena for 1 hr 4 days prior to testing to minimize the exploration of
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 161
FIGURE 1 Diagram of testing arena with six dishes, three of which were randomly chosen to hold food.
Measurements along the outside arena wall indicate the length of the arena walls. Measurements for dashed
and solid lines indicate distance between dishes.
the arena due to novelty and to emphasize exploration for food. Each arena was filled with
sani-chip bedding, and six empty dishes (PVC pipe end cap, 5.1-cm diameter) were placed
in a circular pattern (Figure 1) within the center of the arena. After habituation, the sani-chip
from the arena was placed into a plastic bag so that it could be used during the behavioral test.
Reusing the sani-chip provided the individuals with their familiar odor, thereby minimizing the
novelty of the arena.
Individuals were food-deprived in their experimental home cages for 4 hr prior to testing
to motivate food exploration during the test; water was still provided ad libitum. Subjects
were tested individually. Prior to placing an individual into the arena, three dishes within the
circular pattern of six dishes were randomly selected to contain a fresh 0.5 cm � 1 cm slice
of Macintosh apple. Pilot studies showed that captive voles readily consume apple slices. Each
individual was transferred from his or her cage to the arena in a small square container to
minimize the stress of being handled. Subjects were always placed into the arena in the same
corner (Figure 1).
Each test was recorded with a Sony Handycam (Model DCR-SR68) mounted on a tripod
(Figure 1). Behavioral testing ran for 15 min, and the timer began once the animal was released
into the arena. Once testing was completed, animals were placed back into their original cages
and immediately given rat chow pellets and sunflower seeds.
Analysis
Video recording of behavior. Behavioral testing for all subjects was video-recorded and
transferred to a MacBook Pro OS-X computer for future viewing. Each instance of a-priori
selected behaviors was viewed and manually recorded into the program JWatcher Version 1.0
(Blumstein & Daniel, 2007). For each 15-min test, eight parameters were measured (see online
Supplementary Table 2). All-occurrence (duration and number of behaviors for 15 min) and
instantaneous (behavior observed at 5-s intervals for 15 min) sampling were used to record
foraging and nonforaging behaviors for each animal during his or her trial (Altman, 1974).
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162 KOZUCH AND MCPHEE
Each subject was recorded once, and analysis of each behavioral parameter was independent
of each other, thereby eliminating pseudoreplication.
Behaviors selected to measure differences in foraging repertoire indicated decision making
by voles to search, locate, and consume available food items. These data were measured in
units of frequency and proportion, as well as the number of behaviors observed (see online
Supplementary Table 3). Frequency of grooming, inactivity, and ambulating indicated how
many times a nonforaging behavior was observed during a test aimed at optimally retrieving
a reward. Dish-visiting behavior (number of visits to food dishes vs. control dishes) showed
decision making of individuals posed with two “patch” quality options. Greater interest in food
dishes was assumed to be optimal, while greater interest in control dishes was assumed to be
suboptimal. The duration of foraging behaviors indicated the proportion of time an individual
would spend searching (locomoting), locating (not consuming), and consuming food in a risk-
free but familiar environment.
Statistical analysis of behaviors. The duration, frequency, and number of behaviors were
analyzed in program R (Version 2.11.0, R Development Core Team, 2011). First, the number of
visits to control and food dishes by all subjects were compared using the Mann-Whitney U Test
to confirm that dishes were chosen because of food presence rather than the novelty of the dish.
We compared behaviors in four ways: (1) across treatment (CL, SL, CS, and SS); (2) across
(a) treatment and (b) environment by sex; (3) between complex and simple environments, short
time and long time in each environment, and time regardless of environment; and (4) between
sex within environment (complex, simple). We used the Kruskal-Wallis test for (1) and (2a)
comparisons, and the Mann-Whitney U Test was used for (2b), (3), and (4) comparisons.
Nonparametric statistical testing was used because the behavioral variables chosen were not
normally distributed (Runyon & Haber, 1980). Dish visit by all subjects was compared against
a significant p value of .05. To account for multiple comparisons, tests examining nonforaging
behaviors (grooming, ambulating, and inactivity) were compared against an adjusted ˛ D .017;
number of visits to dishes were considered significantly different at ˛ D .05, and proportion
of behaviors expressed during the 15-min trial were considered significant at ˛ D .017.
RESULTS
Meadow voles in this study, regardless of treatment, significantly visited food dishes more
often than they visited control dishes (W D 800.5, p < .05, ˛ D .05).
Environment and Time Interaction (1)
In general, there were no significant differences in nonforaging behaviors (grooming, ambulat-
ing, and inactivity) across the four treatment groups (CS, CL, SS, and SL; Table 2). Foraging
behaviors, however, did differ significantly as a function of treatment. Specifically, the duration
of inactivity at a food dish differed (�2D 12.55, df D 3, p D .01, ˛ D .02) between the
treatment groups. No other foraging behaviors differed between treatment groups (Tables 2
and 3).
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 163
TABLE 2
The p Values for Differences in Frequency of Behaviors Expressed Overall and Between Sexes
(Female and Male) in Environment (C, S) and Treatment (SS, SL, CS, and CL) Groups
Frequencya Number of Visits tob
Comparison Group Grooming Ambulating Inactivity Food Dishes Control Dishes
Environment Alone
Overall .725 .974 .826 .62 .42
Females .208 .918 .270 .19 .44
Males .265 .772 .283 .39 .88
Time � Environment
Overall .017* .892 .331 .17 .07
Females .021 .662 .553 .14 .14
Males .344 .889 .340 .29 .42
Note. For each group, males and females were analyzed separately. Refer to Table 1 for sample sizes.aSignificant at ˛ D .017.bSignificant at ˛ D .05.
*p D .0171.
Time Within Environment (3)
Simple. Within the simple environment, there were significant differences in the number,
frequency, and duration of foraging and nonforaging behaviors. Individuals visited control
dishes more frequently when housed in a simple environment for a short time than when
housed for a long time (W D 29.5, p < .03, ˛ D .05; Table 4, Figure 2). These two groups (SS,
SL), however, did not differ in the number of visits to food dishes (Table 4). The frequency of
nonforaging behaviors did not significantly differ as a function of time in a simple environment
(Table 4).
TABLE 3
The p Values for Differences in Proportions of Behaviors Observed for 15 min
Between Environments (C, S) and Treatment (SS, SL, CS, CL) Groups
Comparison Group Consuming Not Consuming Locomoting
Environment Alone
Overall .955 .353 .589
Females .680 .210 .150
Males .660 .620 .380
Time � Environment
Overall .752 .012* .105
Females .462 .144 .342
Males .535 .028 .075
Note. For each group, males and females were analyzed separately. Italicized valueis significant at corresponding ˛ value. Refer to Table 1 for sample sizes.
*Significance at ˛ D .017.
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164 KOZUCH AND MCPHEE
TABLE 4
The p Values of Differences Between Sex Within Environment, Time Within Environment,
and Environment Within Time
Variables
Sex/
Simple
Sex/
Complex
Time/
Simple
Time/
Complex
Environment/
Short
Environment/
Long
Nonforaginga
Grooming .582 .256 .018 .041 .24 .93
Ambulating .059 .016 .618 .742 .36 .77
Inactivity .042 .948 .074 .582 .31 .79
Dish visitingb
Food dishes .877 .034 .059 .384 .16 .09
Control dishes .384 .071 .025 .370 .21 .04
Foragingc
Consuming .951 .346 .642 .325 .42 .66
Not consuming .688 .500 .005 .479 .49 .22
Locomoting .975 .022 .022 .878 .45 .10
Note. Refer to Table 1 for sample sizes. Italicized values are significant at corresponding ˛ value.aSignificant at ˛ D .017.bSignificant at ˛ D .05.cSignificant at ˛ D .017.
FIGURE 2 Number of visits to nonfood dishes during long and short periods of time housed in a simple
environment (SS and SL; p D .025, ˛ D .05). Error bars indicate standard error. Circle indicates outlier. Refer
to Table 1 for sample size.
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 165
The Mann-Whitney U Test showed the duration of foraging behavior differed significantly
as a function of time (W D 20.5, p < .01, ˛ D .02; n D 23). Individuals from the SS treatment
group were observed spending more time at a food dish not consuming than did individuals
from the SL group (SS, n D 11; SL, n D 12; Figure 3B, Table 4).
Complex. Animals housed in a complex environment showed no difference in frequency
of nonforaging or foraging behaviors as a function of time (Table 4). In addition, duration of
foraging behavior also did not differ across time groups in this environment (Table 4).
Environment Within Time (3)
The behavior of subjects housed in complex and simple environments was analyzed for
differences within the two time groups (<50 days and >50 days) using the Mann-Whitney
U Test. Only visits to control dishes were observed to be significantly different between
environments within a long period of captivity (W D 107.5, p D .04, ˛ D .05; Table 4).
Individuals within the complex environment visited more control dishes than did those housed
in a simple environment for the same time, but they equally visited food dishes. The animals did
not differ in their foraging (Table 4) and nonforaging behaviors as a function of environment
in either time group (Table 4).
Environment Alone (3)
The inclusion of complexity within the captive environment did not affect the duration, fre-
quency, or number of foraging and nonforaging behaviors (Tables 2 and 3).
Sex
Across treatment groups and environments (2a, 2b). Female behavior during a for-
aging trial did not differ as a function of environment or treatment group (Tables 2 and 3);
likewise, males exhibited no behavioral differences between groups (Tables 2 and 3).
Within environments (4). Overall, there were no differences in frequency of nonforaging
behaviors between males and females as a function of environment (simple and complex),
except for ambulating (W D 97, p D .016, ˛ D .017; Table 4). Females housed in a complex
environment were observed ambulating more during the foraging trial compared with their
complement males. In the complex environment, however, males and females exhibited a
significant difference in the number of visits to food dishes (W D 97, p < .05, Figure 4A,
Table 4): Females exposed to complexity while in captivity visited food dishes on average 5
times more than males in the same environment. In contrast, females and males housed in a
simple environment did not differ in the number of visits to food dishes (Figure 4B). Similarly,
sexes in neither the complex nor the simple environment significantly differed in the number
of visits to nonfood dishes or the duration of foraging behaviors (Table 4).
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166 KOZUCH AND MCPHEE
FIGURE 3 (A) Proportion of nonconsuming time for treatment groups (CL, n D 10; CS, n D 9; SL, n D 8;
and SS, n D 10). (B) Proportion of nonconsuming time during time in environments. Individuals who did not
visit any dish were excluded. Significant differences, p < .01, are indicated by asterisks. Error bars indicate
standard error. Circles indicate outliers.
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 167
FIGURE 4 Number of visits to food dishes by females and males in the (A) complex environment (p D
.034, ˛ D .05) and (B) simple environment (p D .88, ˛ D .05). Error bars indicate standard error. Circles
indicate outliers. Refer to Table 1 for sample size.
DISCUSSION
Nonhuman animals of all ages exposed to complex environments during captivity show en-
hanced neuronal activity (Lambert et al., 2005), physiology parameters (Van Loo et al., 2002),
and physical health (Van de Weerd et al., 2002), which can increase the expression of naturalistic
behaviors. There is, however, a lack of consensus on the type(s) of environmental modifications
most beneficial for maintaining welfare and species-specific behaviors of caged animals (Olsson
& Dahlborn, 2002).
Kitchen and Martin (1996) increased cage size and usable space for captive marmosets
(Callithrix jacchus jacchus), which caused an increase in locomoting, foraging, and socializing.
In addition, complexity in the form of manipulable objects and feeding enrichment maintained
natural foraging behavior in captive Western lowland gorillas (Gorilla gorilla gorilla; Rooney &
Sleeman, 1998). In another study, the presentation of manipulable novel objects to chimpanzees
(Pan troglodytes schweinfurthii) decreased inactivity, but habituation reduced the effectiveness
of objects if they were not rotated (Paquette & Prescott, 1988). The most effective modifi-
cations may be those based on the biology and wild behavior of the species being housed.
Nevertheless, Lewis et al. (2006) concluded that research is still needed to identify which
environmental factors lead to maximal welfare and naturalistic behaviors in captive animals.
In fact, the key is likely in a combination of factors that may lead to appropriate behavioral
expression.
In our study, environmental modifications in captive housing combined natural substrate,
increased cage size, rotated novel objects, and manipulable enrichment items. We documented
that there was no influence of environmental complexity alone on the foraging behaviors of
meadow voles. We did find, however, that foraging behaviors differed due to an interaction
between length of time in captivity and level of environmental complexity. Specifically, voles
were less active at food dishes and visited control dishes more when they were housed in a
simple environment for less than 50 days compared with when they were housed for longer
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168 KOZUCH AND MCPHEE
than 50 days. Increased visits to control dishes were also observed in voles housed in a complex
environment for longer than 50 days as compared with voles housed in a simple environment
for the same time.
Nonetheless, these results could demonstrate that a simple environment does not provide
opportunities to appropriately forage and thus the environment rapidly alters a vole’s foraging
repertoire, but behaviors differed over time within the same environment—in other words,
foraging behavior was less effective in the simple environment after a long time in captivity
than it was in the simple environment after a shorter time. Therefore, longer time within an
environment may provide benefits for maintaining foraging behavior, such as habituation to
the novel environment.
Introduction into a novel environment can be quite stressful for any animal. Dickens,
Delehanty, and Romero (2010) suggested that the process of translocation (movement of an
individual from one wild location to another, often with a short, intermediate stay in captivity)
can lead to acute and chronic stress in individuals and lead to changes in behavioral coping
strategies. These strategies can be expressed as anxiety, increased fleeing or freezing, or changes
in food intake, for example.
The length of time in captivity needed to reduce this stress is unknown and could be species-
specific (Dickens et al., 2010; Teixeira, De Azevedo, Mendl, Cipreste, & Young, 2007), yet
some individuals may receive relief from stress through environmental enrichment (Carlstead
& Shepherdson, 2000; Young, 2003). Our study mimics a translocation scenario because our
subjects were wild-caught animals brought into captivity for a limited period of time. This
aspect of our research, therefore, highlights stress as a plausible influence on foraging behavior.
Nonetheless, the reason for the lack of behavioral differences between meadow voles housed
for less than 50 days in a simple environment and both complex treatment groups remains
unclear.
Our work reveals interesting effects of environmental complexity on species-specific be-
haviors. We found that sex-related differences in foraging behaviors are more likely to be
maintained in animals housed in a complex captive environment than in a simple one. Specif-
ically, females in the complex environment visited food dishes more during a foraging test
than did males (regardless of time in that environment), coinciding with increased locomotion,
whereas no differences were observed between sexes housed in a simple environment. This is
in contrast to Cheal (1987), who found no difference in foraging behaviors of female and male
gerbils housed in enriched cages.
The presence of differences in foraging between sexes is not surprising from a theoretical
perspective. Ecologists have long understood that female mammals require more energy and
nutrients than do males (of the same taxa) to gestate, lactate, and rear young (Andersson, 1994).
The complex environment used in this study provided individuals with greater manipulation
and control over natural substrates to build burrows and nests similar to those in the wild.
Nest material has been shown to be a vital component within a rodent’s environment where
changes to nest construction affect body weight and food intake (Olsson & Dahlborn, 2002).
Redman, Selman, and Speakman (1999) found that male, short-tailed field voles (Microtus
agrestis) had lower food intake rates than did females when both were allowed to build complex
nests of wood wool. The distinct difference in nest structure between complex and simple
environments suggests the increased variability of nest size and coverage could maintain sex-
specific differences in foraging behavior.
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FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 169
CONCLUSION
Overall, this study uniquely identifies time in captivity as a variable that strongly influences
foraging behaviors of captive-housed meadow voles. Our results show that the eroding effects of
time are diminished when complexities such as cage size, natural substrate, and unpredictability
are added to the environment. If environmental complexity cannot be provided, however, this
study shows that a shorter time in captivity may be detrimental to foraging behavior because
wild animals have not had time to overcome the stress of a captive environment. No matter how
long the animals were in captivity, however, environmental enrichment maintained appropriate
sex differences in foraging behavior, which are the result of the need for males and females to
meet differential energy requirements (Low, 2000).
The influence of an interaction between time and environment found in this study can lend
valuable insight into enhancing programs for mammalian species conservation. Understanding
the effects of temporarily holding wild animals in captivity can increase the efficacy of
rehabilitation programs and translocations for species management. Examining the effects of
time in a captive environment on behavior will elucidate the optimal amount of time to house an
animal that will maintain a natural range of behaviors. Maintaining healthy captive animals and
the expression of naturalistic behavior can increase individual welfare, thereby better preparing
animals who are held temporarily if they are going to be released back into the wild.
ACKNOWLEDGMENTS
We would like to graciously thank the University of Wisconsin-Oshkosh for providing the
facilities and financial assistance to complete this project. We gratefully acknowledge the eager
volunteers, Diana Cartier, Korin Franklin, Jenn Gingras, Sara Hagerdorn, Suzanne Hietpas,
Kenneth Kieck, Jennifer Mohl, Brad Spanbauer, and Brittney Wiggins, who gave numerous
hours to trap in the field and assist with facility upkeep. We are appreciative of the expertise
of Greg Adler, Dana Vaughn-Merriman, Kelly Schill, and Colleen McDermott, who proposed
useful advice for developing the project and maintaining the captive population. Also thanks
to the Wisconsin County Parks for permitting us to use the meadow for trapping.
SUPPLEMENTAL MATERIAL
Supplemental data for this article can be accessed on the publisher’s website.
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