This article was downloaded by: [Dr Kenneth Shapiro]On: 09 June 2015, At: 11:46Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Click for updates

Journal of Applied Animal WelfareSciencePublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/haaw20

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

To link to this article: http://dx.doi.org/10.1080/10888705.2014.881256

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the“Content”) contained in the publications on our platform. However, Taylor & Francis,our agents, and our licensors make no representations or warranties whatsoever as tothe accuracy, completeness, or suitability for any purpose of the Content. Any opinionsand views expressed in this publication are the opinions and views of the authors,and are not the views of or endorsed by Taylor & Francis. The accuracy of the Contentshould not be relied upon and should be independently verified with primary sourcesof information. Taylor and Francis shall not be liable for any losses, actions, claims,proceedings, demands, costs, expenses, damages, and other liabilities whatsoever orhowsoever caused arising directly or indirectly in connection with, in relation to or arisingout of the use of the Content.

This article may be used for research, teaching, and private study purposes. Anysubstantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,systematic supply, or distribution in any form to anyone is expressly forbidden. Terms &

Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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: mcpheem@uwosh.edu

157

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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).

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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).

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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).

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

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.

REFERENCES

Altman, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 48, 227–260.

Altman, J. D. (1999). Effects of inedible, manipulable objects on captive bears. Journal of Applied Animal Welfare

Science, 2, 123–132.

Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton University Press.

Baumans, V. (2011). Environment enrichment for laboratory rodents and rabbits: Requirements of rodents, rabbits, and

research. ILAR Journal, 46, 162–170.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

170 KOZUCH AND MCPHEE

Beck, B. B., & Castro, M. I. (1994). Environments for endangered primates. In E. F. Gibbons, E. J. Wyers, E. Waters,

& E. W. Menzel (Eds.), Naturalistic environments in captivity for animal behavior research (pp. 259–270). Albany:

State University of New York Press.

Beck, B. B., Castro, M. I., Stoinski, T. S., & Ballou, J. D. (2002). The effects of prerelease environments and postrelease

management on survivorship in reintroduced 71 golden lion tamarins. In D. G. Kleiman & A. B. Rylands (Eds.),

Lion tamarins: Biology and conservation (pp. 283–300). Washington, DC: Smithsonian Institute.

Blumstein, D. T., & Daniel, J. C. (2007). Quantifying behavior the JWatcher way. Sunderland, MA: Sinauer.

Burrell, A. M., & Altman, J. D. (2006). The effects of the captive environment on activity of captive cotton-top

tamarins (Saguinus oedipus). Journal of Applied Animal Welfare Science, 9, 269–276.

Carlstead, K., Seidensticker, J., & Baldwin, R. (1991). Environmental enrichment for zoo bears. Zoo Biology, 10,

3–16.

Carlstead, K., & Shepherdson, D. (1994). Effects of environmental enrichment on reproduction. Zoo Biology, 13,

447–458.

Carlstead, K., & Shepherdson, D. S. (2000). Alleviating stress in zoos with environmental enrichment. In G. P.

Moberg & J. A. Mench (Eds.), The biology of animal stress: Basic principles and implications for animal welfare

(pp. 337–354). New York, NY: CABI.

Cheal, M. (1987). Environmental enrichment facilitates foraging behavior. Physiology and Behavior, 39, 281–283.

Dickens, M. J., Delehanty, D. J., & Romero, L. M. (2010). Stress: An inevitable component of animal translocation.

Biological Conservation, 143, 1329–1341.

Gattermann, R., Weinandy, R., & Fritzsche, P. (2004). Running-wheel activity and body composition in golden hamsters

(Mesocricetus auratus). Physiology and Behavior, 82, 541–544.

Hansen, L. T., & Berthelsen, H. (2000). The effect of environmental enrichment on the behaviour of caged rabbits

(Oryctolagus cuniculus). Applied Animal Behaviour Science, 68, 163–178.

Herbers, J. M. (1981). Time resources and laziness in animals. Oecologia, 49, 252–262.

Jensvold, M. L. A., Sanz, C. M., Fouts, R. S., & Fouts, D. H. (2001). Effect of enclosure size and complexity on the

behaviors of captive chimpanzees (Pan troglodytes). Journal of Applied Animal Welfare Science, 4, 53–69.

Kitchen, A. M., & Martin, A. A. (1996). The effects of cage size and complexity on the behaviour of captive common

marmosets, Callithrix jacchus jacchus. Laboratory Animals, 30, 317–326.

Krebs, C. J., Keller, B. L., & Tamarin, R. H. (1969). Microtus population biology: Demographic changes in fluctuating

populations of M. Ochrogaster and M. Pennsylvanicus in Southern Indiana. Ecology, 50, 587–607.

Lambert, T. J., Fernandez, S. M., & Frick, K. M. (2005). Different types of environmental enrichment have discrepant

effects on spatial memory and synaptophysin levels in female mice. Neurobiology of Learning and Memory, 83,

206–216.

Lewis, M. H., Presti, M. H., Lewis, J. B., & Turner, C. A. (2006). The neurobiology of stereotypy 1: Environmental

complexity. In G. Mason & J. Rushen (Eds.), Stereotypic animal behaviour: Fundamentals and applications to

welfare (2nd ed., pp. 190–226). Wallingford, UK: CAB International.

Low, B. S. (2000). Why sex matters: A Darwinian look at human behavior. Princeton, NJ: Princeton University Press.

Mallapur, A., & Chellam, R. (2002). Environmental influences on stereotypy and the activity budget of Indian leopards

(Panthera pardus) in four zoos in Southern India. Zoo Biology, 21, 585–595.

McPhee, M. E. (2002). Intact carcasses as enrichment for large felids: Effects on on- and off-exhibit behaviors. Zoo

Biology, 21, 37–47.

Molla, M. I., Quevedo, M. A., & Castro, F. (2011). Bobcat (Lynx rufus) breeding in captivity: The importance of

environmental enrichment. Journal of Applied Animal Welfare Science, 14, 85–95.

Myers, J. H., & Krebs, C. J. (1971). Genetic, behavioral, and reproductive attributes of dispersing field voles Microtus

pennsylvanicus and Microtus ochrogaster. Ecological Monographs, 41, 53–78.

National Research Council. (1996). Animal environment, housing, and management. In N. Grossblatt (Ed.), Guide for

the care and use of laboratory animals (pp. 21–55). Washington, DC: The National Academies Press.

Newberry, R. C. (1995). Environmental enrichment: Increasing the biological relevance of captive environment. Applied

Animal Behaviour Science, 44, 229–243.

Novak, M. A., O’Neill, P., Beckley, S. A., & Suomi, S. J. (1994). Naturalistic environments for captive primates. In

E. F. Gibbons (Ed.), Naturalistic environments in captivity for animal behaviour research (pp. 235–257). Albany:

State University of New York Press.

Odberg, F. O. (1987). The influence of cage size and environmental enrichment on the development of stereotypies in

bank voles (Clethrionomys glareolus). Behavioral Processes, 14, 155–173.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015

FORAGING BEHAVIOR OF WILD-CAUGHT MEADOW VOLES 171

Olsson, I. A. S., & Dahlborn, K. (2002). Improving housing conditions for laboratory mice: A review of ‘environmental

enrichment.’ Laboratory Animals, 36, 243–270.

Paquette, D., & Prescott, J. (1988). Use of novel objects to enhance environments of captive chimpanzees. Zoo Biology,

7, 15–23.

R Development Core Team. (2011). R: A language and environment for statistical computing. Vienna, Austria:

R Foundation for Statistical Computing. Retrieved from http://www.r-project.org

Redman, P., Selman, C., & Speakman, J. R. (1999). Male short-tailed field voles (Microtus agrestis) build better

insulated nests than females. Journal of Comparative Physiology B, 169, 581–587.

Rooney, M. B., & Sleeman, J. (1998). Effects of selected behavioral enrichment devices on behavior of Western

lowland gorillas (Gorilla gorilla gorilla). Journal of Applied Animal Welfare Science, 1, 339–351.

Runyon, R. P., & Haber, A. (1980). Fundamentals of behavioral statistics (4th ed.). Reading, MA: Addison-Wesley.

Schrijver, N. C. A., Bahr, N. I., Weiss, I. C., & Wurbel, H. (2002). Dissociable effects of isolation rearing and

environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology Biochemistry

and Behavior, 72, 209–224.

Shepherdson, D. (1999). New perspectives on the design and management of captive animal environments. In F. L.

Dolins (Ed.), Attitudes and animals: Views in animal welfare (pp. 143–151). Cambridge, UK: Cambridge University

Press.

Shepherdson, D., Bemment, N., Carman, M., & Reynolds, S. (1989). Auditory enrichment for lar gibbons Hylobates

lar at London Zoo. International Zoo Yearbook, 28, 256–260.

Shivik, J. A., Palmer, G. L., Gese, E. M., & Osthaus, B. (2009). Captive coyotes to their counterparts in the wild:

Does environmental enrichment help? Journal of Applied Animal Welfare Science, 12, 223–235.

Simonsen, H. B. (1990). Behaviour and distribution of fattening pigs in the multi-activity pen. Applied Animal

Behaviour Science, 27, 311–324.

Stoinski, T. S., & Beck, B. B. (2004). Changes in locomotor and foraging skills in captive-born, reintroduced golden

lion tamarins (Leontopithecus rosalia rosalia). American Journal of Primatology, 62, 1–13.

Teixeira, C. P., De Azevedo, C. S., Mendl, M., Cipreste, C. F., & Young, R. J. (2007). Revisiting translocation and

reintroduction programmes: The importance of considering stress. Animal Behaviour, 73, 1–13.

Van de Weerd, H. A., Aarsen, E. L., Mulder, A., Kruitwagen, C. L. J. J., Hendriksen, C. F. M., & Baumans, V. (2002).

Effects of environmental enrichment for mice: Variation in experimental results. Journal of Applied Animal Welfare

Science, 5, 87–109.

Van Loo, P. L. P., Kruitwagen, C. L. J. J., Koolhaas, J. M., Van de Weerd, H. A., Van Zutphen, L. F. M., & Baumans,

V. (2002). Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice. Applied

Animal Behaviour Science, 76, 65–81.

Wiedenmayer, C. (1997). Causation of the ontogenetic development of stereotypic digging in gerbils. Animal Behaviour,

53, 461–470.

Wurbel, H., Chapman, R., & Rutland, C. (1998). Effect of feed and environmental enrichment on development of

stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science, 60, 69–81.

Young, R. J. (2003). Environmental enrichment for captive animals. Oxford, UK: Blackwell Scientific.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

11:

46 0

9 Ju

ne 2

015