This article was downloaded by: [Dr Kenneth Shapiro]On: 09 June 2015, At: 10:36Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH,UK

Journal of Applied AnimalWelfare SciencePublication details, including instructions forauthors and subscription information:http://www.tandfonline.com/loi/haaw20

If You Knew What WasGood For You! The Value ofEnvironmental EnrichmentsWith Known Welfare BenefitsIs Not Demonstrated by SowsUsing Operant TechniquesMonica Renee Pittman Elmore a d , Joseph PaulGarner a e , Anna Kerr Johnson b , Richard D. Kirkdenc , Brian Thomas Richert a & Edmond Anthony Pajor af

a Department of Animal Sciences , Purdue Universityb Department of Animal Science , Iowa StateUniversityc Department of Veterinary Medicine , University ofCambridge , United Kingdomd University of Illinoise Stanford Universityf University of CalgaryPublished online: 28 Jun 2012.

To cite this article: Monica Renee Pittman Elmore , Joseph Paul Garner , AnnaKerr Johnson , Richard D. Kirkden , Brian Thomas Richert & Edmond AnthonyPajor (2012) If You Knew What Was Good For You! The Value of EnvironmentalEnrichments With Known Welfare Benefits Is Not Demonstrated by Sows UsingOperant Techniques, Journal of Applied Animal Welfare Science, 15:3, 254-271, DOI:10.1080/10888705.2012.683982

To link to this article: http://dx.doi.org/10.1080/10888705.2012.683982

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all theinformation (the “Content”) contained in the publications on our platform.However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness,or suitability for any purpose of the Content. Any opinions and viewsexpressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of theContent should not be relied upon and should be independently verified withprimary sources of information. Taylor and Francis shall not be liable for anylosses, actions, claims, proceedings, demands, costs, expenses, damages,and other liabilities whatsoever or howsoever caused arising directly orindirectly in connection with, in relation to or arising out of the use of theContent.

This article may be used for research, teaching, and private study purposes.Any substantial or systematic reproduction, redistribution, reselling, loan,sub-licensing, systematic supply, or distribution in any form to anyone isexpressly forbidden. Terms & Conditions of access and use can be found athttp://www.tandfonline.com/page/terms-and-conditions

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 15:254–271, 2012

Copyright © Taylor & Francis Group, LLC

ISSN: 1088-8705 print/1532-7604 online

DOI: 10.1080/10888705.2012.683982

If You Knew What Was Good For You!The Value of Environmental

Enrichments With Known WelfareBenefits Is Not Demonstrated by Sows

Using Operant Techniques

Monica Renee Pittman Elmore,1 Joseph Paul Garner,1

Anna Kerr Johnson,2 Richard D. Kirkden,3

Brian Thomas Richert,1 and Edmond Anthony Pajor1

1Department of Animal Sciences, Purdue University2Department of Animal Science, Iowa State University

3Department of Veterinary Medicine, University of Cambridge,

United Kingdom

This study assessed the motivation of gestating sows housed in standard, barren

gestation stalls (used for breeding/implantation and/or gestation) for access to

environmental enrichment. Enrichment consisted of a cotton rope or rubber mat in

comparison to positive (additional food when fed at commercial levels) and neg-

ative (empty trough) controls. Although environmental enrichment may improve

animal welfare, sows’ valuation of enrichments is largely unknown. This study

used an operant panel and obtained behavioral measures to quantify motivation.

As indicated by a higher price paid and lower latencies to press the panel and

enter the treatment stall (all comparisons, p < .05), sows demonstrated higher

motivation for food compared with all treatments. Sows housed in gestation stalls

Monica Renee Pittman Elmore is now at the University of Illinois Urbana-Champaign. Joseph

Paul Garner is now at Stanford University. Edmond Anthony Pajor is now at the University of

Calgary.

Correspondence should be sent to Monica Elmore, Department of Animal Sciences, University

of Illinois Urbana-Champaign, 1207 West Gregory Drive, Urbana, IL 61801. Email: MonicaRPE

lmore@gmail.com

254

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 255

did not demonstrate high motivation via operant responding for a cotton rope or a

rubber mat; nor did they demonstrate any differences in behavioral measures (all

comparisons, p > .10). Although sows’ motivation for a mat did not differ from

that for an empty trough, previous work has demonstrated the welfare benefits

associated with comfort flooring.

Mounting concern for the welfare of nonhuman animals has led to the banning

of sow gestation stalls in a number of states in America and the European Union

(Council Directive 2001/88/EC). Although stalls have been banned for the entire

length of gestation, their use is still permitted during breeding and embryo

implantation (Council Directive 2001/88/EC) to prevent negative impacts on

sow reproductive performance (Arey & Edwards, 1998; Kongsted, 2004). Stalls

have been criticized for causing both physical and social restriction to the animal

(Chapinal et al., 2010; European Food Safety Authority, 2007; Pajor, 2005) com-

pared with group housing (Barnett, Hemsworth, Cronin, Jongman, & Hutson,

2001; Bracke, Metz, Spruijt, & Dijkhuizen, 1999). In addition, most stall and

group systems lack environmental complexity and stimulation (Broom, Mendl,

& Zanella, 1995; Durrell, Sneddon, & Beattie, 1997). Barren environments have

been associated with impairments in learning (Sneddon, Beattie, Dunne, &

Neil, 2000), increases in negative social interactions: biting (Beattie, Walker,

& Sneddon, 1996), signs of apathy (Arey, 1993), and chronic stress (de Jong

et al., 2000), all of which can lead to detriments in animal welfare. Therefore,

investigation into welfare improvements to barren sow housing, including stalls,

is needed.

Environmental enrichment can be defined as biologically relevant (Würbel &

Garner, 2007) additions or modifications to the environment that allow coping

with stressors by promoting species-specific coping behaviors such as foraging

and rooting (Stolba & Wood-Gush, 1989; Van de Weerd & Day, 2009) and

may be linked to the experience of positive affective states in animals (Boissy,

Manteuffel, et al., 2007).

It is important to note that not all resources provided to animals are en-

richments, only those that meet the criteria outlined above. Enrichments may

improve the welfare of sows housed in barren environments by providing op-

portunities for natural behaviors such as foraging (Feddes & Fraser, 1994;

Tuyttens, 2005; Whittaker, Edwards, Spoolder, Lawrence, & Corning, 1999),

which may reduce chronic hunger in restricted-fed sows by increasing gut fill

(e.g., straw; Fraser, 1975) and can lead to reductions in abnormal behavior (e.g.,

stereotypic; Fraser, 1975; Spoolder, Burbidge, Edwards, Simmins, & Lawrence,

1995). In addition, physical and thermal comfort may be improved by the

provision of straw bedding or rubber mats (Boyle, Regan, Leonard, Lynch,

& Brophy, 2000; Elmore, Garner, Johnson, Richert, & Pajor, 2010; Tuyttens,

2005). The motivation of sows for environmental enrichments is largely un-

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

256 ELMORE ET AL.

known but is essential knowledge for developing housing that promotes animal

welfare.

Motivation studies can identify resources of value to animals (Dawkins, 1983,

1990) that lead to science-based recommendations, and, ultimately, to improve-

ments in animal welfare. The willingness of an animal to “pay” for access to

a resource is an index of how the animal “feels” about that resource (Dawkins,

1990). This knowledge will become increasingly important as scientists strive

to measure affective states in animals (Boissy, Arnould, et al., 2007; Boissy,

Manteuffel, et al., 2007; Mendl, Burman, Parker, & Paul, 2009). Investigation

into the motivation of animals frequently utilizes measures that are derived from

human economic theory, with elasticity of demand being the most commonly

employed measure in animal studies (Holm, Jensen, & Jeppesen, 2002; Matthews

& Ladewig, 1994; Sherwin & Nicol, 1997). Due to the criticisms against the use

of elasticity (Kirkden, Edwards, & Broom, 2003; Mason, McFarland, & Garner,

1998), reservation price (or the highest price paid) was adopted in this study; it

is considered a more robust and valid measure of animal motivation (Kirkden

et al., 2003; Mason, Cooper, & Clarebrough, 2001; Mason et al., 1998).

The aim of this study was to compare the motivation of gestating sows housed

in standard, barren gestation stalls for access to one of four resources: (a) cotton

rope (enrichment); (b) rubber mat (enrichment); (c) additional food (positive

control) when fed at commercial levels, �30–60% of ad libitum intake (Barnett

et al., 2001; Kirkden & Pajor, 2006a); or (d) an empty trough (negative control).

A cotton rope allows for the expression of oral behaviors observed during for-

aging (Feddes & Fraser, 1994), without complications to existing infrastructure,

which can be problematic when providing other substrates (e.g., straw in a liquid

manure system). Rubber mats can increase flooring and thermal comfort (Boyle

et al., 2000; Tuyttens, Wouters, Struelens, Sonck, & Duchateau, 2008) and can

improve welfare by, for example, reducing lesions (Elmore et al., 2010). We

hypothesized that sow motivation would be affected by the resource provided.

Specifically, we reasoned that sows would show high motivation for food, a

known valued resource, especially when feed-restricted (Matthews & Ladewig,

1994; Patterson-Kane, Pittman, & Pajor, 2008). We further hypothesized, based

on similar negative controls (Cooper, 2004; Mason et al., 2001), that sows

would show low motivation for an empty trough, an assumed unvalued resource.

We predicted that motivation for enrichments of value to the sow would be

significantly different from motivation for an empty trough. Since controls can

act as both low and high comparators to aid in the assessment of resource

value (Cooper, 2004), it is important to use them in animal motivation studies.

In addition, we hypothesized that the behavior of the sows would vary due to

treatment; where sows provided with a cotton rope would show an increase in

general activity due to an increase in foraging-type behaviors (Feddes & Fraser,

1994), sows provided with a rubber mat would show an increase in resting

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 257

behaviors due to an increase in flooring comfort (Boyle et al., 2000; Gravas,

1979; Tuyttens et al., 2008).

MATERIALS AND METHODS

All experimental procedures were approved by the Purdue University Animal

Care and Use Committee. This experiment was conducted daily from 08:00 hr–

12:00 hr during November of 2008 through August of 2009 at the Purdue

University swine farm.

Animals and Husbandry

A total of 40 enrichment naïve Landrace � Yorkshire multiparous (2.15 ˙ 0.36

parities; mean ˙ standard deviation [SD]) sows were used in this study. The

sows were confirmed pregnant via ultrasound (performed by a trained swine

farm employee) at 35 days postbreeding, were moved from gestation housing

(either stalls or groups) to a separate test barn, and were given 24 hr to habituate

to their surroundings prior to the start of the experiment. All sows had previous

experience with both group housing and gestation stalls. The sows had access

to water ad libitum from a nipple drinker and were fed approximately 2.3 kg of

sow gestation diet (12.6% CP and 0.55% lysine) each morning. To enhance the

external validity of our findings, sows were not fed ad libitum but were feed-

restricted to commercial levels. Artificial lighting was provided continuously

for videorecording purposes (infrared was not possible in the barn), air quality

was controlled by a negative pressure exhaust system, and the average room

temperature was recorded at the start of each day and varied due to season

(20.6 ˙ 1.7ıC; mean ˙ SD). Farm employees observed the sows at 08:00 hr

and 15:00 hr daily for overall health.

Treatments

Sows were fed and tested in the same standard, barren gestation stall (hereafter

“test stall”). The test stalls (2.13 m L � 0.61 m W) were constructed of steel and

were positioned over fully slatted concrete flooring. In front of each test stall

was an alleyway (measuring approximately 4 m in length) that led to a separate

stall where the resource was provided (hereafter “treatment stall”; Figure 1). The

alleyway, constructed of opaque plastic boards, created a visual barrier for the

sows. On completion of the operant task, the sow gained immediate access to

the resource by walking forward and entering the treatment stall. Due to space

constraints, the provision of a full-length rubber mat in front of the stall was

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

258 ELMORE ET AL.

FIGURE 1 Schematic of room layout with four testing stations. At each testing station,

there were two test sows (T1 and T2), each with her own test stall and treatment stall (where

the assigned resource was provided). However, both sows at each station used the same

operant panel for testing. Sows were tested in homogenous treatment pairs. Treatments were

rotated and balanced across replications to account for location in the room (color figure

available online).

not feasible; a separate treatment stall was required. Resource provision was

standardized to allow for proper comparison against “positive” and “negative”

controls; therefore, all treatments were accessed in a separate treatment stall via

an alleyway. Due to this standardization, sow motivation to exercise, novelty of

the treatment stall, and other potential confounds were controlled for by testing

sow motivation for the negative control (empty trough).

Sows were assigned to one of four treatments at the start of the experiment

(n D 10 sows per treatment): (a) an empty trough in a standard concrete stall

(negative control), (b) cotton rope (environmental enrichment), (c) rubber mat

(environmental enrichment), or (d) additional food (positive control). Food was

considered a positive control in this study because sows were fed at commercial

levels (�30–60% of ad libitum intake; Barnett et al., 2001; Kirkden & Pajor,

2006a), which likely results in feelings of hunger and high motivation for

additional food. The sows remained on the same treatment for the duration

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 259

of the experiment and were not tested on all treatments due to time constraints

imposed by gestation. For the rope treatment, one cotton rope (2.54 cm W,

30.48 cm L, with ends unbraided) was attached with a hose clamp to the bars of

the stall and was allowed to hang freely. The cotton ropes were replaced during

testing if more than half of the length (approximately 15 cm from the bottom)

or half of the diameter (approximately two of the three unbraided sections) was

absent or excessively damaged. In addition, a new rope was provided at the

start of each testing series (see section Experimental Apparatus and Procedure)

and for each new test subject. For the mat treatment, a perforated rubber mat

(1.83 m L � 0.61 m W, hole diameter �2.54 cm) spanning the length and width

of the stall (minus the area covered by the feed trough) was provided to the

sows. For the positive control, a single 0.91 kg portion of the sows’ standard

gestation diet was used as the reward. The enrichments were rotated between

replicates to balance for location in the room.

The room layout used in this experiment consisted of four test stations in the

corners of the room, with two sows per station (Figure 1). Both sows at each

station were test subjects, but the testing times for the sows were staggered 1 hr

apart from each other. The sows were not tested in isolation; they were allowed

olfactory and auditory contact with their respective neighbors. However, a visual

barrier (approximately 1 m L � 1 m H) was installed between the two stalls

to reduce any disruption caused by the companion during testing; this barrier

was not present between the treatment stalls. In addition, because barriers were

not placed in the front of the test stalls, sows had limited contact with one

another when moving from the test stall to the treatment stall. Sows were tested

in homogenous treatment pairs to avoid the influence of a neighbor’s treatment

on sow motivation (e.g., the smell of food when working for an empty trough).

Treatments were rotated and balanced across replications to account for location

in the room.

Experimental Apparatus and Procedure

Sows were allowed 1 hr each morning to consume their daily meal in the test

stall, and any unconsumed feed was removed prior to testing. Sow motivation

for access to the resource was tested 7 days per week following feeding. At the

start of testing each morning, the sow’s feed trough was removed and replaced

with the operant panel. The operant gate consisted of a stainless steel panel

(13 cm L � 10 cm W) attached to a modified gestation-stall, food-trough frame,

which was positioned at the height of the sow. The panel was locked in place

and could not be pressed until the gate had been fitted to the stall. A light cue

(above the snout panel) signaled when the panel was unlocked. A panel press

was registered by a computer when the sow had depressed the panel with her

snout.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

260 ELMORE ET AL.

Prior to testing, sows were trained to press the operant panel (up to 10 presses)

with food as the reward (daily meal; 2 days). Following this initial training, their

assigned resource (empty trough, cotton rope, rubber mat, or food) became

the reward for 5 days of additional training (previously described: Elmore

et al., 2011). After completion of training, sows were permitted access to the

enrichments only after “paying” for access via presses on the operant panel.

Therefore, a traditional closed economy was employed in this study (Cooper,

2004; Mason et al., 1998).

Sows were placed on an ascending series of fixed ratio (FR) schedules, where

the number of panel presses required by the sow increased by 50% each day

after FR 10 (FR 1, 10, 15, 23, 35, 53, 80, 120, 180, 270, 405, 608, 912, 1368,

and 2052). Sow testing order was varied to reduce the impact of the neighbor’s

actions on the sows’ motivation and operant responding. Sows were given 1 hr

each day to complete the required FR schedule. If the sow succeeded, the panel

swung open, and she was permitted immediate access to the resource via an

alleyway (described earlier). The sows were given 5 min to enter the treatment

stall on their own. After this time, the experimenter escorted the sow to the

treatment stall by (a) a hand on her back or (b) if necessary, a herding board.

The sows were then locked inside the treatment stall with a rear gate until the

next day; then testing was repeated (providing a maximum of 23 hr access to

the resource). Resource access times varied depending on the testing order of

the sows and the time it took each sow to reach the required FR schedule.

If the sow failed to reach the required FR schedule within 1 hr, she remained

in the test stall, was not permitted access to the resource, and testing ceased.

The following day, the sow was given a second chance to reach the required

FR schedule. If she succeeded, she was permitted access to the resource, and

testing continued according to the prescribed series of FR schedules. If she

failed a second time, testing ceased permanently for that series. Two separate

series were performed to allow the sows more time to familiarize themselves

with the operant procedure and the resource. The highest price paid represented

the sows’ motivation for the resource. It was calculated from the second series

and was defined as the highest FR schedule that the sow successfully achieved

prior to cessation of pressing (Kirkden & Pajor, 2006b). For additional details

on the training and testing procedures used in this study, refer to Elmore et al.

(2011).

Behavioral Observations

The behavior of the sows during operant response and resource access was

recorded continuously throughout the experiment using time-lapse video. The

sows were marked with livestock paint (All-Weather® Paintstik®) for identifica-

tion on the video. The paint was reapplied as needed. One black/white camera

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 261

(Panasonic WV-BP330, Secaucus, NJ) was mounted on the ceiling above each

pair of test stalls and treatment stalls. The output was recorded using a time-

lapse VCR (Panasonic AGTL950P, Secaucus, NJ) and a multiplexer (Panasonic

WJ-FS216, Secaucus, NJ) in 48 hr mode. All behavior data on the day of highest

price paid for the resource were quantified by one experienced observer.

Latency to press the operant panel, defined as the time (s) between operant

panel attachment and the test sow’s first press, was collected as an additional

measure of motivational strength. Resource use was quantified as (a) general

activity (to measure rope use) and (b) resting behavior (to measure mat use).

General activity (defined as drinking, eating, and manipulating the rope or stall

components: biting, nosing, and rooting) was quantified using 1-0 sampling

every 1 min for a maximum of 23 hr (from the start of resource access until the

following morning at feeding). Finally, resting behavior (defined as kneeling,

sitting, or lying) was quantified using this same procedure. However, all sow

behaviors were not scored (e.g., standing inactive); they were not of interest to

the research question.

Statistical Analysis

Data were analyzed as a generalized linear model (GLM) or as a repeated

measures mixed model (REML), where appropriate, in JMP 6 for Windows

(2005). Data were transformed as necessary to meet the assumptions of GLM

or REML: homogeneity of variance, normality of error, and linearity (Grafen

& Hails, 2002). Significant results (p < .05) were examined with post hoc tests

to further describe the relationship between the tested interactions. Statistical

trends were considered as p < .10. Equivalence tests were performed to confirm

sufficient statistical power for negative results of importance to our hypotheses.

Unless indicated, numerical data are presented as raw means ˙ SE within the

text. For graphing purposes, data are presented on transformed scales where

necessary.

Motivation data. The highest price paid, representing motivation for the

resource, was quantified as the highest FR schedule that the sow successfully

completed. The model used was treatment, blocked by group (accounts for

variability due to replication); location (stall location within the testing station);

and testing order (first or second sow to test). We used equivalence tests of

the Tukey’s 95% confidence interval to test nonsignificant motivation results for

sufficient power. We wished to detect a twofold difference between treatment

means, in particular, compared with the negative control (empty trough). In

addition, the highest number of presses (regardless of schedule completion) was

analyzed; however, this had no effect on statistical outcomes (data not shown)

and was therefore not included within the manuscript. Latency to press the

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

262 ELMORE ET AL.

panel and latency to enter the treatment stall were also analyzed. Latency to

press the operant panel acted as an indicator of motivation to work on the

operant, and latency to enter the treatment stall acted as an indicator of certainty

and anticipation for the resource. The prediction was that lower latencies would

represent an increased motivation for access to the resource. Due to video error,

latency to press the panel for 5 sows was missing (one food, two mat, and two

empty trough). The model used for latency to press the panel was the same

as described earlier. Latency to enter the stall was the same as earlier with the

addition of latency for food (during training) as a covariate. Differences in the

highest price paid due to series (1 vs. 2) were analyzed as an REML, where

the sow was treated as a random effect and nested within treatment with the

interactions of treatment and series. All analyses required log transformation.

Resource use: General activity and resting behavior. Both the amount

and pattern of general activity and resting behavior exhibited by sows with

access to an empty trough (negative control) was used as a comparator for all

other treatments. We were most interested in the sows’ behavior (a) while first

accessing the resources and (b) the next morning prior to their being returned to

the test stall for feeding, which are known periods (based on previous data) of

high enrichment use (Elmore et al., 2011). As sow access times to the resource

varied (see section Experimental Apparatus and Procedure), this second measure

could not be collected at the same time point (19:30–21:30 hr) for all sows.

Therefore, raw data were collated in two ways: (a) from the start of resource

access (to test for differences in initial use) and (b) backward from the time since

resource access ended (to test for differences prior to feeding/resource removal).

When analyzed, both analyses showed nearly identical results (data not shown).

Therefore, to avoid repetition within the manuscript, only the general activity and

resting behavior for sows from the start of resource access are presented in the

article. Data were lumped into 1 hr bins for the entire access period (maximum

23 hr); the longest access period that was common for all sows (20 hr) was used

for analysis, and the remaining data after this time point were removed. Data

were analyzed as an REML, where the sow was treated as a random effect and

nested within treatment with all the interactions of time and treatment. Data for

general activity required square root transformation; data for resting behavior

required angular transformation to meet the assumptions of REML.

RESULTS

Motivation

The highest price paid was significantly affected by treatment (GLM: F3;32 D

6.27, p D .002; Figure 2), with sows showing higher motivation for food

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 263

FIGURE 2 Comparison of the motivation (defined as highest price paid) of gestating sows

for access to one of four resources (Food D positive control, Cotton Rope or Rubber Mat D

environmental enrichments, Empty Trough D negative control; n D 10/treatment) in a stall.

LSM ˙ SE are plotted. Significant Tukey comparisons are indicated by columns not sharing a

common letter (p < .05). To illustrate sufficient power for negative results, the upper limit of

the Tukey’s 95% confidence interval for the control treatment (empty trough) was determined

and is represented by a dashed line on the graph. Data are transformed and presented on a

log scale.

compared to a cotton rope (p D .02), a rubber mat (p D .003), and an empty

trough (p D .006). Equivalence tests revealed that we were able to detect a 1.69-

fold difference between treatment means and therefore had sufficient power in

this experiment. Latency to press the operant panel was also affected by treatment

(GLM: F3;27 D 6.51, p D .002; Figure 3), where sows working for food showed

a reduced latency to press the panel compared with a cotton rope (p < .001).

There was also a trend for sows working for food to show a reduced latency

to press the panel compared with a rubber mat (p D .06) and an empty trough

(p D .08). However, no other treatment differences were found (all comparisons,

p > .10). Latency to enter the treatment stall was affected by treatment (GLM:

F3;31 D 29.43, p < .001), where sows accessing food entered the stall much

sooner (17.0 s ˙ 6.76) than for all other resources (Rope: 182.0 s ˙ 43.04; Mat:

243.90 s ˙ 32.99; Trough: 223.10 s ˙ 38.72; all comparisons, p < .05). No other

treatment differences were found (all comparisons, p > .10). Series affected the

highest price paid (REML: F1;36 D 14.31, p < .001), where sows showed higher

operant responding in Series 2 (292.33 presses ˙ 64.52) compared with Series 1

(238.78 presses ˙ 84.66). However, the interaction of series and treatment was

not significant (REML: F3;36 D 1.01, p D .40).

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

264 ELMORE ET AL.

FIGURE 3 Comparison of the latency to press the operant panel(s) by gestating sows for

access to one of four resources (Food D positive control, Cotton Rope or Rubber Mat D

environmental enrichments, Empty Trough D negative control; n D 10/treatment) in a stall.

LSM ˙ SE are plotted. Significant Tukey comparisons are indicated by columns not sharing

a common letter (p < .05). Data are transformed and presented on a log scale.

Resource Use: General Activity

No treatment differences were found in general activity (Food, 3.82% of obser-

vations ˙ 0.12; Rope, 10.03% ˙ 0.11; Mat, 6.56% ˙ 0.14; Trough, 7.22% ˙

0.14, back transformed data; REML: F3;31 D 2.11, p D .12) or the interaction

of general activity and time (REML: F60;619 D 1.11, p D .28). However, there

was a time effect (REML: F20;619 D 27.22, p < .001; Figure 4), where general

activity was highest during the first 2 hr after resource access and the last 1 hr

before resource access ended, regardless of assigned treatment (all comparisons,

p < .05).

Resource Use: Resting Behavior

Similar to general activity, no treatment differences were found in resting be-

havior (Food, 95.77% of observations ˙ 0.29; Rope, 87.31% ˙ 0.26; Mat,

92.26% ˙ 0.32; Trough, 90.63% ˙ 0.32, back transformed data; REML: F3;31 D

1.55, p D .22) or the interaction of resting behavior and time (REML: F60;620 D

0.94, p D .60). However, there was a time effect (REML: F20;620 D 24.21,

p < .001; Figure 5), where, regardless of treatment, resting behavior was lowest

during the first 5 hr after resource access and the last 2 hr before resource access

ended (all comparisons, p < .05).

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 265

FIGURE 4 Change in general activity behavior over time since start of treatment access

(h), all treatments combined (n D 40). LSM ˙ SE are plotted. Data points that were

significantly different from the mean are indicated by *p < .05. Data are transformed and

presented on a square root scale.

FIGURE 5 Change in resting behavior over time since start of treatment access (h), all

treatments combined (n D 40). LSM ˙ SE are plotted. Data points that were significantly

different from the mean are indicated by *p < .05. Data are transformed and presented on

an angular scale.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

266 ELMORE ET AL.

DISCUSSION

This study represents one of the first attempts to assess the value of enrichments

to gestating sows housed in standard, barren stalls, where the motivation of

sows for a positive control (additional food when fed at commercial levels),

negative control (empty trough), or enrichments (cotton rope or rubber mat)

were compared. As predicted, sows showed the highest motivation (as indicated

by the highest price paid and a reduced latency to press the operant panel or

enter the treatment stall) for access to food. The motivation of sows for access

to a cotton rope or a rubber mat did not differ significantly from that for an

empty trough, indicating that these enrichments were not highly valued by the

sows in this study.

A previous study—using the same operant equipment, training, and testing

procedures—assessed the motivation of sows for access to a food reward at

various hunger levels, creating a food-based reference scale (Patterson-Kane,

Kirkden, & Pajor, 2011). According to this scale, sows in the present study

showed high levels of motivation for both enrichments and an empty trough,

responding at similar rates to sows who had consumed 0–25% (approximately

0–2 kg) of their ad libitum intake level. However, this finding is likely due

to the rewarding nature of locomotion and investigation to stall-housed sows

and an association between the trough and access to food by feed-restricted

sows, introduced by the operant procedure and controls (see later for further

discussion).

The majority of work concerning environmental enrichment for swine has

focused on grow/finish pigs (Van de Weerd & Day, 2009) but can provide

insight into enrichments that can be beneficial to sows as well. In a study by

Van de Weerd, Docking, Day, Avery, & Edwards (2003), researchers found that

pigs interacted most with enrichments that stimulated foraging and exploratory

behavior, including odorous, deformable, chewable, and destructible enrich-

ments. This finding mirrored those of Feddes & Fraser (1994), who found that

cotton ropes elicited higher responses from piglets when the end was exposed

(allowing greater destructibility) compared with a loop or a rubber strip. This

study represents one of the first attempts to provide a cotton rope to sows

as a form of environmental enrichment. Due to additional labor requirements,

disease considerations, and current difficulties for the liquid manure-handling

systems (Day et al., 2002; Tuyttens, 2005), straw is not commonly provided

in U.S. swine systems. A cotton rope may offer an alternative to straw and

allow for the expression of oral behavior (chewing) in intensive systems, which

may be especially important for sows who are feed-restricted. However, based

on the behavior and motivation measures gathered in this study, a cotton rope

does not appear to be a valuable enrichment to gestating sows housed in stalls.

For commercial sows fed a restricted diet, �30–60% of their ad libitum intake

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 267

(Barnett et al., 2001; Kirkden & Pajor, 2006a), the expression of the appetitive

component of foraging behavior—without the consummatory component (lead-

ing to gut fill and satiety; Rushen, 1984)—may be insufficient to satisfy the

needs of the sow (de Jonge, Tilly, Baars, & Spruijt, 2008; Hughes & Duncan,

1988), thus reducing motivation for a cotton rope. It is interesting to note that

the motivation for a cotton rope varied across sows, with some sows showing

very high motivation for rope access. This indicates that a cotton rope may be

a highly valued enrichment to some, but not all, sows. However, the feasibility

and economic impact of tailoring enrichment provision for individual sows is not

practical in commercial conditions; therefore, an environmental enrichment that

is valued by a wider proportion of sows should be identified for implementation

on farms.

Previous work has shown that sows prefer to rest on rubber mats (Elmore

et al., 2010; Gravås, 1979; Tuyttens et al., 2008) and that mats can lead to

many benefits for sow welfare, including an increase in the ease of getting up

and down (Elmore et al., 2010), reduced slipping (Boyle et al., 2000), fewer

lesions (Elmore et al., 2010), and a reduction in lesion healing time (Zurbrigg,

2006). However, based on the motivation and behavior measures in this study,

sows did not value access to a rubber mat in a stall. Although the empty trough

treatment was added to control for potential confounds of the operant procedure,

the opportunity for locomotion in the alleyway (measuring �4 m in length)

for all treatments may have been rewarding enough to overshadow any slight

preferences the sows had for a rubber mat. In addition, sows were permitted

5 min to enter the stall on their own, allowing them to investigate the alleyway

and, potentially, the other test sow prior to being locked in the treatment stall.

Again, the rewarding nature of investigation may have overpowered any slight

preferences for the mat.

In addition, another possible explanation may be the ecological constraints

on learning introduced by the operant used in this study (Young, Macleod, &

Lawrence, 1994). Sows were required to press the operant panel with their snouts

to gain access to the resource, which lends itself nicely to resources that fulfill

a similar motivation (substrates to root and forage) but may be counterintuitive

for other resources (comfort flooring). Although the operant panel was artificial

(Cooper, 2004), we also incorporated a naturalistic task of walking to access all

resources. However, this may have been insufficient to overcome the constraints

on responding imposed by the operant when working for the rubber mat.

Finally, the lack of motivation observed for a rubber mat may reflect a

fundamental shortcoming of using operant conditioning techniques. When using

these techniques, we are asking the sow to make a decision in the short term

based on long-term benefits. This may not be problematic for resources that

have obvious immediate consequences (e.g., food and gut fill) but may be more

difficult for resources whose benefits are not as immediately forthcoming (e.g.,

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

268 ELMORE ET AL.

comfort flooring leading to long-term improvements in leg health). In future

studies, testing sows with known leg problems (lameness or hoof lesions) may

increase the sows’ willingness to work on an operant panel to gain access to

this flooring substrate.

CONCLUSION

Gestating sows housed in standard, barren gestation stalls did not demonstrate

high motivation via operant responding for either a cotton rope or a rubber mat,

or any differences in behavior. Although motivation did not differ from that for

an empty trough, previous work has demonstrated health and welfare benefits

associated with the provision of a rubber mat. As animal welfare scientists

strive to measure affective states in animals to improve their welfare, further

investigation into both the value of enrichments to sows and techniques to

understand the sows’ perspective will become increasingly important in the

literature.

ACKNOWLEDGMENTS

This project was supported by the National Research Initiative of the U.S.

Department of Agriculture, Cooperative State Research Education, and Exten-

sion Service, Grant 2005-35204-15215. We thank Dick Byrd and the Purdue

University swine farm staff for their efforts in the construction of experimental

apparatuses. We also thank the following people for their assistance: Dr. Emily

Patterson-Kane (advice on experimental methods), Barry Elmore (installation

and repair of video equipment), Dr. Eric Furgason (repair of operant equipment),

Melissa Elischer (aid in the collection of motivation data, and behavior video

analysis), and Dr. Don Lay (comments on the manuscript).

REFERENCES

Arey, D. S. (1993). The effect of bedding on the behaviour and welfare of pigs. Animal Welfare, 2,

235–246.

Arey, D. S., & Edwards, S. A. (1998). Factors influencing aggression between sows after mixing

and the consequences for welfare and production. Livestock Production Science, 56, 61–70.

Barnett, J. L., Hemsworth, P. H., Cronin, G. M., Jongman, E. C., & Hutson, G. D. (2001). A review

of the welfare issues for sows and piglets in relation to housing. Australian Journal of Agricultural

Research, 52, 1–28.

Beattie V. E., Walker, N., & Sneddon, I. A. (1996). An investigation of the effect of environmental

enrichment and space allowance on the behaviour and production of growing pigs. Applied Animal

Behaviour Science, 48, 151–158.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 269

Boissy, A., Arnould, C., Chailou, E., Désiré, L., Duvaux-Ponter, C., Greiveldinger, L., : : : Veissier,

I. (2007). Emotions and cognition: A new approach to animal welfare. Animal Welfare, 16(S),

37–43.

Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling, L. J., : : : Aubert,

A. (2007). Assessment of positive emotions in animals to improve their welfare. Physiology &

Behavior, 92, 375–397.

Boyle, L. A., Regan, D., Leonard, F. C., Lynch, P. B., & Brophy, P. (2000). The effect of mats on

the welfare of sows and piglets in the farrowing house. Animal Welfare, 9, 39–48.

Bracke, M. B. M., Metz, J. H. M., Spruijt, B. M., & Dijkhuizen, A. A. (1999). Overall welfare

assessment of pregnant sow housing systems based on interviews with experts. Netherlands

Journal of Agricultural Science, 47, 93–104.

Broom, D. M., Mendl, M. T., & Zanella, A. J. (1995). A comparison of the welfare of sows in

different housing conditions. Animal Science, 61, 369–385.

Chapinal, N., Ruiz de la Torre, J. L., Cerisuelo, A., Gasa, J., Baucells, M. D., : : : Manteca, X.

(2010). Evaluation of welfare and productivity in pregnant sows kept in stalls or in 2 different

group housing systems. Journal of Veterinary Behavior, 5, 82–93.

Cooper, J. J. (2004). Consumer demand under commercial husbandry conditions: Practical advice

on measuring behavioural priorities in captive animals. Animal Welfare, 13, S47–S56.

Council Directive 2001/88/EC amending Council Directive 91/630/EEC.

Dawkins, M. S. (1983). Battery hens name their price: Consumer demand theory and the measure-

ment of ethological ‘needs.’ Animal Behaviour, 31, 1195–1205.

Dawkins, M. S. (1990). From an animal’s point of view: Motivation, fitness, and animal welfare.

Behavioral and Brain Sciences, 13, 1–61.

Day, J. E. L., Burfoot, A., Docking, C. M., Whittaker, X., Spoolder, H. A. M., & Edwards, S. A.

(2002). The effects of prior experience of straw and the level of straw provision on the behaviour

of growing pigs. Applied Animal Behaviour Science, 76, 189–202.

de Jong, I. C., Prelle, I. T., van de Burgwal, J. A., Lambooij, E., Korte, S. M., Blokhuis, H. J., &

Koolhaas, J. M. (2000). Effects of environmental enrichment on behavioral responses to novelty,

learning, and memory, and the circadian rhythm of cortisol in growing pigs. Physiology &

Behavior, 68, 571–578.

de Jonge, F. H., Tilly, S.-L., Baars, A. M., & Spruijt, B. M. (2008). On the rewarding nature of

appetitive feeding behaviour in pigs (Sus scrofa): Do domesticated pigs contrafreeload? Applied

Animal Behaviour Science, 114, 359–372.

Durrell, J., Sneddon, I. A., & Beattie, V. E. (1997). Effects of enrichment and floor type on behaviour

of cubicle loose-housed dry sows. Animal Welfare, 6, 297–308.

European Food Safety Authority. (2007). Scientific report on animal health and welfare aspects of

different housing and husbandry systems for adult breeding boars, pregnant, farrowing sows, and

unweaned piglets. Annex to ESFA Journal, 572, 1–100.

Elmore, M. R. P., Garner, J. P., Johnson, A. K., Kirkden, R. D., Richert, B. T., & Pajor, E. A. (2011).

Getting around social status: Motivation and enrichment use of dominant and subordinate sows

in a group setting. Applied Animal Behaviour Science, 133, 154–163.

Elmore, M. R. P., Garner, J. P., Johnson, A. K., Richert, B. T., & Pajor, E. A. (2010). A flooring

comparison: The impact of rubber mats on the health, behavior, and welfare of group-housed

sows at breeding. Applied Animal Behaviour Science, 123, 7–15.

Feddes, J. J. R., & Fraser, D. (1994). Non-nutritive chewing by pigs: Implications for tail-biting and

behavioral enrichment. Transactions of the ASAE, 37, 947–950.

Fraser, D. (1975). The effect of straw on the behaviour of sows in tether stalls. Animal Production,

21, 59–68.

Grafen, A., & Hails, R. (2002). Modern statistics for the life sciences. Oxford, UK: Oxford University

Press.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

270 ELMORE ET AL.

Gravås, L. (1979). Behavioral and physical effects of flooring on piglets and sows. Applied Animal

Ethology, 5, 333–345.

Holm, L., Jensen, M. B., & Jeppesen, L. L. (2002). Calves’ motivation for access to two different

types of social contact measured by operant conditioning. Applied Animal Behaviour Science, 79,

175–194.

Hughes, B. O., & Duncan, I. J. H. (1988). The notion of ethological ‘need,’ models of motivation

and animal welfare. Animal Behaviour, 36, 1696–1707.

JMP 6 for Windows. (2005). Cary, NC: SAS Institute.

Kirkden, R. D., Edwards, J. S. S., & Broom, D. M. (2003). A theoretical comparison of the consumer

surplus and the elasticities of demand as measures of motivational strength. Animal Behaviour,

65, 157–178.

Kirkden, R. D., & Pajor, E. A. (2006a). Motivation for group housing in gestating sows. Animal

Welfare, 15, 119–130.

Kirkden, R. D., & Pajor, E. A. (2006b). Using preference, motivation and aversion tests to ask

scientific questions about animals’ feelings. Applied Animal Behaviour Science, 100, 29–47.

Kongsted, A. G. (2004). Stress and fear as possible mediators of reproduction problems in group

housed sows: A review. Acta Agriculturae Scandinavica, 54, 58–66.

Mason, G. J., Cooper, J., & Clarebrough, C. (2001). Frustrations of fur-farmed mink. Nature, 410,

35–36.

Mason, G. J., McFarland, D., & Garner, J. (1998). A demanding task: Using economic techniques

to assess animal priorities. Animal Behaviour, 55, 1071–1075.

Matthews, L. R., & Ladewig, J. (1994). Environmental requirements of pigs measured by behavioural

demand functions. Animal Behaviour, 47, 713–719.

Mendl, M., Burman, O. H. P., Parker, R. M. A., & Paul, E. S. (2009). Cognitive bias as an indicator

of animal emotion and welfare: Emerging evidence and underlying mechanisms. Applied Animal

Behaviour Science, 118, 161–181.

Pajor, E. A. (2005). Sow housing: Science, behavior, and values. Animal Welfare Forum: Sow

Housing and Welfare. Journal of the American Veterinary Medical Association (JAVMA), 226,

1340–1344.

Patterson-Kane, E. G., Kirkden, R. D., & Pajor, E. A. (2011). Measuring motivation in swine: The

food-metric scale. Journal of Applied Animal Welfare Science, 14, 175–186.

Patterson-Kane, E. G., Pittman, M., & Pajor, E. A. (2008). Operant animal welfare: Productive

approaches and persistent difficulties. Animal Welfare, 17, 139–148.

Rushen, J. (1984). Stereotyped behaviour, adjunctive drinking and the feeding periods of tethered

sows. Animal Behaviour, 32, 1059–1067.

Sherwin, C. M., & Nicol, C. J. (1997). Behavioural demand functions of caged laboratory mice for

additional space. Animal Behaviour, 53, 67–74.

Sneddon, I. A., Beattie, V. E., Dunne, L., & Neil, W. (2000). The effect of environmental enrichment

on learning in pigs. Animal Welfare, 9, 373–383.

Spoolder, H. A. M., Burbidge, J. A., Edwards, S. A., Simmins, P. H., & Lawrence, A. B. (1995).

Provision of straw as a foraging substrate reduces the development of excessive chain and bar

manipulation in food restricted sows. Applied Animal Behaviour Science, 43, 249–262.

Stolba, A., & Wood-Gush, D. G. M. (1989). The behaviour of pigs in a semi-natural environment.

Animal Production, 48, 419–425.

Tuyttens, F. A. M. (2005). The importance of straw for pig and cattle welfare: A review. Applied

Animal Behaviour Science, 92, 261–282.

Tuyttens, F. A. M., Wouters, F., Struelens, E., Sonck, B., & Duchateau, L. (2008). Synthetic lying

mats may improve lying comfort for gestating sows. Applied Animal Behaviour Science, 114,

76–85.

Van de Weerd, H. A., & Day, J. E. L. (2009). A review of environmental enrichment for pigs housed

in intensive housing systems. Applied Animal Behaviour Science, 116, 1–20.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015

VALUE OF ENRICHMENTS TO SOWS 271

Van de Weerd, H. A., Docking, C. M., Day, J. E. L., Avery, P. J., & Edwards, S. A. (2003).

A systematic approach towards developing environmental enrichment for pigs. Applied Animal

Behaviour Science, 84, 101–118.

Whittaker, X., Edwards, S. A., Spoolder, H. A. M., Lawrence, A. B., & Corning, S. (1999). Effects

of straw bedding and high fibre diets on the behaviour of floor fed group-housed sows. Applied

Animal Behaviour Science, 63, 25–39.

Würbel, H., & Garner, J. P. (2007). Refinement of rodent research through environmental enrichment

and systematic randomization. NC3Rs (National Centre for the Replacement, Refinement and

Reduction of Animals in Research), 9, 1–9.

Young, R. J., Macleod, H. A., & Lawrence, A. B. (1994). Effect of manipulandum design on operant

responding in pigs. Animal Behaviour, 47, 1488–1490.

Zurbrigg, K. (2006). Sow shoulder lesions: Risk factors and treatment effects on an Ontario farm.

Journal of Animal Science, 84, 2509–2514.

Dow

nloa

ded

by [

Dr

Ken

neth

Sha

piro

] at

10:

36 0

9 Ju

ne 2

015