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Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound Marc B.M. Bracke * Animal Sciences Group of Wageningen, Wageningen University and Research Centre, P.O. Box 65, 8200 AB Lelystad, The Netherlands Accepted 5 October 2006 Available online 17 November 2006 Abstract To validate (further) a semantic model called RICHPIG, which was designed to assess enrichment materials for pigs, a study was conducted to examine the importance of three assessment criteria, namely destructibility, hygiene and sound. These material properties were studied using a specially constructed object consisting of a piece of sisal rope, metal wire and three fixed chain links hanging in the pens. The object was considered to be not destructible (ND), hygienic (HY) and not making sound (NS). After a habituation period of 18 h treatments were applied in that the object was (or was not) made destructible with a partial cut in the rope (DE) and/or was soiled with excreta (not hygienic, NH) and/or was allowed to make a tinkling sound by releasing the chain links (SO). The three treatments were applied in a 2 Â 2 Â 2 factorial design on a commercial farm in seven replicates using seven different units containing eight pens per unit. At five moments in time, ranging from 18 h before until 1 h after treatment, a range of behaviours was recorded including the frequency-related parameter AMI (animal–material interactions) and four intensity- related parameters. Repeated measures ANOVA’s showed significant effects of time and hygiene as well as interactions between time and hygiene, between time and destructibility and between destructibility and sound. Soiling (NH) significantly decreased, and destructibility (DE) significantly increased attractiveness, while sound (SO) was not significant. Only moderate correlations between AMI and the four intensity- related parameters were found (median r = 0.41, all P < 0.05), indicating that frequency-related parameters alone may not suffice to determine behavioural importance for animal welfare. This study showed that it is in principle possible to study material properties independent of material type and that it is in principle possible to measure behavioural intensities on a commercial farm. Furthermore, the finding that hygiene and destructibility were more important for pigs than tinkling sounds provided preliminary support for the RICHPIG model. # 2006 Elsevier B.V. All rights reserved. Keywords: Environmental enrichment; Pigs; Modelling; Housing; Toys; Validation; Assessment criteria; Intensity www.elsevier.com/locate/applanim Applied Animal Behaviour Science 107 (2007) 218–232 * Tel.: +31 320 238205; fax: +31 320 238094. E-mail address: [email protected]. 0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2006.10.001

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Page 1: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

Multifactorial testing of enrichment criteria: Pigs

‘demand’ hygiene and destructibility more than sound

Marc B.M. Bracke *

Animal Sciences Group of Wageningen, Wageningen University and Research Centre,

P.O. Box 65, 8200 AB Lelystad, The Netherlands

Accepted 5 October 2006

Available online 17 November 2006

Abstract

To validate (further) a semantic model called RICHPIG, which was designed to assess enrichment

materials for pigs, a study was conducted to examine the importance of three assessment criteria, namely

destructibility, hygiene and sound. These material properties were studied using a specially constructed

object consisting of a piece of sisal rope, metal wire and three fixed chain links hanging in the pens. The

object was considered to be not destructible (ND), hygienic (HY) and not making sound (NS). After a

habituation period of 18 h treatments were applied in that the object was (or was not) made destructible with

a partial cut in the rope (DE) and/or was soiled with excreta (not hygienic, NH) and/or was allowed to make a

tinkling sound by releasing the chain links (SO). The three treatments were applied in a 2 � 2 � 2 factorial

design on a commercial farm in seven replicates using seven different units containing eight pens per unit.

At five moments in time, ranging from 18 h before until 1 h after treatment, a range of behaviours was

recorded including the frequency-related parameter AMI (animal–material interactions) and four intensity-

related parameters. Repeated measures ANOVA’s showed significant effects of time and hygiene as well as

interactions between time and hygiene, between time and destructibility and between destructibility and

sound. Soiling (NH) significantly decreased, and destructibility (DE) significantly increased attractiveness,

while sound (SO) was not significant. Only moderate correlations between AMI and the four intensity-

related parameters were found (median r = 0.41, all P < 0.05), indicating that frequency-related parameters

alone may not suffice to determine behavioural importance for animal welfare.

This study showed that it is in principle possible to study material properties independent of material type

and that it is in principle possible to measure behavioural intensities on a commercial farm. Furthermore, the

finding that hygiene and destructibility were more important for pigs than tinkling sounds provided

preliminary support for the RICHPIG model.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Environmental enrichment; Pigs; Modelling; Housing; Toys; Validation; Assessment criteria; Intensity

www.elsevier.com/locate/applanim

Applied Animal Behaviour Science 107 (2007) 218–232

* Tel.: +31 320 238205; fax: +31 320 238094.

E-mail address: [email protected].

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2006.10.001

Page 2: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

1. Introduction

Environmental enrichment is important for the welfare of farm animals, which are often kept

in barren environments (e.g. Young, 2003).

In 2001 the European Commission adopted a directive (2001/93/EC) which states that:

‘‘Pigs must have permanent access to a sufficient quantity of material to enable proper

investigation and manipulation activities, such as straw, hay, wood, sawdust, mushroom

compost, peat or a mixture of such, which does not compromise the health of the animals.’’

The directive leaves considerable room for interpretation as it is not clear what is proper

investigation and manipulation. Furthermore, the value of enrichment material is most likely

determined not only by the type of material as listed in the directive, but also by other material

properties such as the amount and frequency of material provision, hygiene, destructibility and

responsiveness, e.g. being moved or making sounds in response to interaction with the object.

A semantic model, called RICHPIG, was constructed based on a systematic and formalised

analysis of scientific information collected in a database (Bracke et al., 2007a,b). RICHPIG

allows calculating scores for the (relative) value of different enrichment materials for pigs using a

list of assessment criteria. The assessment criteria, which are welfare-relevant material

properties, and their weighting factors were derived from the scientific knowledge base following

procedures described earlier for welfare assessment in pregnant sows (Bracke et al., 2002) and

tail biting (Bracke et al., 2004). RICHPIG’s weighting factors were shown to be moderately

comparable to the scores given by eight European experts (Bracke et al., 2007b). In addition, the

model uses simple weighted average calculation rules for reasons of parsimony, assuming linear

additivity unless there is scientific evidence to the contrary. The approach, however, has been

(implicitly) criticised by authors preferring non-linear modelling (e.g. Van Calker, 2005). To help

resolve this issue, research should be ‘asking’ the pigs for a ‘decision’. However, the problem was

how to design a suitable experiment to determine the relative importance of different assessment

criteria and their interactions.

Such experiments have been designed. Zonderland et al. (2003), for example, compared four

hanging materials (rope, wood, chain, metal pipe) that were selected because they differed with

respect to flexibility and destructibility. They suggested that a combination of ’flexibility’ and

’destructibility’ might be relevant, because a high level of manipulation of the flexible and

destructible rope was measured with an automated recording technique, called an ‘AMI-sensor’

(AMI = animal–material interaction), which measured object displacements of the hanging

objects. This conclusion was tentative, however, because the material properties were inherently

confounded with the type of material.

As to the assessment criterion ‘destructibility’, Feddes and Fraser (1994) found that pigs

interacted more with a cotton rope than with a less destructible rubber strip, and that the amount

of chewing on a loop of rope increased dramatically when a small cut was made allowing the

material to be damaged more easily. Within RICHPIG this work in particular provides

experimental evidence for the claim that destructibility (formulated more generally as ‘Change’

in RICHPIG) probably is an important material property. This experiment, however, did not give

information about the relationship of destructibility with other assessment criteria.

Van de Weerd et al. (2003) took another, rather elegant approach. They used Multiple

Stepwise Regression analysis to determine which material properties contributed the most to

AMI times recorded on days 1 and 5 of the experiment that involved presenting 74 different

enrichment materials to 444 small groups of pigs. The authors confirmed that destructibility was

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 219

Page 3: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

important on day 5. Van de Weerd et al. (2003), following many others (e.g. Grandin et al., 1983;

Von Zerboni and Grauvogl, 1984; Sambraus and Kuchenhoff, 1992; Blackshaw et al., 1997;

Stubbe, 2000) also noted that the pigs often lost interest in loose objects, which became soiled

with excreta. Such general consensus among scientists contributed to the high weighting factor

for the assessment criterion ‘Hygiene’ in RICHPIG. However, to my knowledge this has never

been shown experimentally.

In order to investigate the important criteria, destructibility and hygiene, a third,

presumably much less important criterion was added to provide a negative contrast. ‘Sound

producing’ was chosen as it was supported by only few statements in the model’s database.

The criterion ‘Sound’ was incorporated in RICHPIG mainly with reference to the underlying

conceptual framework (Anon., 2001a), where functional behaviour (e.g. through being able to

at least produce a sound) was expected to increase attention, provided the sounds were not

disturbing (e.g. loud noise). For this reason a low intensity sound was selected as the third

experimental treatment.

The common conceptual framework used for welfare assessment in general and semantic

modelling in particular recognises the importance of the triad ‘incidence’, ‘duration’ and

‘intensity’ (Anon., 2001a, after Willeberg, 1991). This implies that in addition to the

frequencies and durations that are commonly reported in behavioural research, the ‘intensity’

dimension should perhaps also be taken into account, as may be recognised in e.g. consumer

demand theory (e.g. Dawkins, 1990). Intensities/‘demands’ are rarely reported in applied, on-

farm studies, perhaps because they are believed to require complex experimental set-ups (e.g.

automated push-doors in a closed economy). Perhaps, also there is no need to report

intensities, namely when intensities positively correlate with the prevailing frequencies and

durations. To elucidate the potential role of behavioural intensities for on-farm welfare

assessment this study examined four potentially intensity-related parameters, called Tailwag

(tail wagging, perhaps indicating an elevated level of arousal), Imax (maximum intensity),

Iavg (average intensity) and Ifreq (intensity frequency, i.e. occurrence of a predetermined

intensity threshold), and compared these parameters with the conventional frequency-related

parameter, called AMI (animal–material interaction, i.e. total object play, see Bracke et al.,

2006).

The relative importance of three assessment criteria (destructibility, hygiene and sound) were

studied as treatments applied to groups of growing pigs in a 2 � 2 � 2 factorially designed

experiment measuring a range of behavioural parameters. The objectives of the study were to

examine how the treatments affect pig behaviour, how intensity-related measures relate to AMI,

what this means for the relative importance of the three assessment criteria, and by implication to

help further validate RICHPIG.

2. Materials and methods

2.1. Animals and farm

The observations were done in one building of a commercial farm where uniform groups of 11 young,

crossbred growing pigs (age between 75 and 100 days) were reared in pens located in units (i.e. rooms)

containing eight pens per unit. Pens were 3.05 m deep and 2.65 m wide. They had a partly solid, concave

(curved) floor (1.2 m deep), extending from 0.4 m from the front wall to 1.45 m from the back wall, with

slatted floors in the front and the back of the pen. All pens had a dry feeder containing a drinking nipple and a

chain hanging on the pen wall dividing neighbouring pens.

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232220

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2.2. Enrichment objects

The object consisted of a piece of straight sisal rope (length: 30 cm, diameter: 10 mm), which was fixated

at both ends of the rope with wire rope clips, and which was fortified with iron wire, extending 15 cm above

the rope, where the iron wire was attached to a nylon rope. At the tope of the iron wire, and outside the reach

of the pigs, three links of a metal chain, which were mutually fixed with sticky tape, were attached in such a

way that these links could not make a sound when first introduced in the pen, but would make a tinkling, soft

bell-like sound during AMI when the sticky tape was released for the sound treatment. All objects were

hanging 15–20 cm (depending on the size of the pigs) above the front slatted area, on the opposite side of the

pen to the feeder.

2.3. Treatments

Before the objects were inserted information about the pen and the unit was collected (number of pigs per

pen, age of the pigs, clinical inspection and disease records) and equipment used for hanging the objects was

installed. These activities provided some initial habituation of the pigs to human presence. The objects were

introduced in the pen in the afternoon of the day before treatments were applied, thus providing a short

(18 h) habituation period to the object. The objects inserted in pens were (considered to be) non-destructible

(ND, as the ends of the rope were fortified with wire rope clips), hygienic (HY, as the objects were hanging

above the floor) and without sound (NS, as the chain links were fixed).

After approximately 18 h of habituation, i.e. the next morning, the objects were briefly (0.5 h) taken out

of the pens and treated in a 2 � 2 � 2 factorial design, using all eight pens in a unit for all treatment

combinations, and using seven different units, thus generating seven replicates in the study.

The destructibility treatment involved cutting two strands of the three-stranded sisal rope. The hygiene

treatment involved soiling the rope with faeces collected earlier from the same pen. The sound treatment

involved releasing the three chain links above the rope. The eight possible treatment combinations (e.g. one

combination was DENHNS, i.e. destructible, not hygienic (i.e. soiled), no sound) were applied to randomly

selected pens in each replicate.

2.4. Measurements

Observations were conducted shortly after novel introduction into the pen (indicated as time point ‘�18’,

as this was approximately 18 h before treatment), shortly before the objects were removed for applying

treatments (indicated as time point ‘�1’, as this was 1 h before their re-introduction), immediately after

treatment (indicated as time point ‘0’), after 0.5 h (indicated as time point ‘0.5’) and after 1 h (indicated as

time point ‘1’). Continued observations after 1 h were not possible due to breakdown of the destructible

objects.

The following behaviours were recorded as the number of animals per pen involved in the behaviour at

each time point. Main behaviours, which were scanned, were lying (Ly), sitting (Sit), standing (Stand) and

walking (Walk).

Sub-behaviours were recorded at each time point for 30 s per pen following the scanning of the main

behaviours. The sub-behaviours were directed at the food (Feed, i.e. head in feeder), floor (FloorDirB), wall

(WallDirB), chain (ChainDirB), conspecifics (PigDirB, involving all pig-directed behaviour except tail

biting and ear biting), tails (Tailbite), ears (Earbite) and rope (AMI, i.e. the number of animals interacting

with the object and/or standing near it). ‘AMI’ was further divided into sub-behaviours of AMI. These

included tail wagging (Tailwag, the number of animals making at least one quick left-right-left movement of

the tail stump while being near the object), standing near the object (StandProxy), trying to bite/pushing

other pigs away (TryBite/push), mounting the wall or another pig (Mount, i.e. with the front legs off the floor

near the object, mostly performed in an attempt to reach it), nosing the object (Nose), levering the object

(Lever), biting the object (Bite, with the front teeth), chewing the object (Chew, with the molars) and pulling

the object (Pull).

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 221

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The intensity-related parameters (‘Imax’, ‘Iavg’ and ‘Ifreq’) were recorded using two prototype AMI

sensors recording the forces exerted by the pigs on the object (after Zonderland et al., 2003). Imax and Iavg

were recorded with a calibrated load cell over the 30 s observation period with the observer present in front

of the pen, while Ifreq was recorded over a longer (0.5 h) period when the observer was not present in the

unit. Ifreq was read out immediately before Imax and Iavg observation times. Since the objects were not

present in the pen in the period before time point 0, the parameter Ifreq could not be recorded at that time

point. Ifreq was, therefore, recorded only for the time points �18, �1, 0.5 and 1.

Video recordings of all behavioural and clinical observations were made with a digital camera

(Panasonic NV-GS 75) mounted on the shoulder of the observer, fitted with a wide-angle lens. All

observations were done by one observer (the author).

2.5. Statistics

Repeated measures ANOVA’s in SPSS 13 (Anon., 2001b) were used to determine the effects of

treatments over time. This test required behaviours to have a sufficiently frequent occurrence (major time-

budget behaviours). This was the case for the parameters Ly, Sit, Stand, Feed, AMI, Tailwag, Imax, Iavg and

Ifreq. It was also the case for a compound behavioural class called OExpl, ‘other exploratory behaviour’ (i.e.

pen- and pig-directed behaviour that was not directed to the object or the feeder), which resulted from

adding the number of animals involved in FoorDirB, WallDirB, ChainDirB, PigDirB, Tailbite and Earbite.

The behavioural elements FloorDirB (overall mean: 0.84 animals per 30 s. observation period) was the most

prevalent component of OExpl, followed by PigDirB (mean: 0.37). WallDirB, Tailbite and Earbite were

considerably less prevalent.

Parameters that were not normally distributed (Imax and Ifreq) were log transformed. In those cases

where significant (but unexplained) differences between treatments were found at pre-treatment times,

secondary analyses were run for the three post-treatment times, using the pre-treatment values for times�18

and �1 as covariates, thus correcting for pre-treatment differences.

The interactions with time were reported as Pillai’s trace of the multivariate tests (Olson, 1974).

The effects of treatments were reported from the tests of between-subjects effects.

The average values of selected behavioural elements were graphically visualised over measurement

times to show potentially interesting trends.

To examine relationships between intensity and frequency-related parameters (Imax, Iavg, Ifreq,

Tailwag and AMI) Pearson correlation coefficients were calculated over non-transformed values.

3. Results

3.1. Effects of time and treatment on major time-budget behaviours

Table 1 gives the significance levels and the estimated marginal means for AMI and Iavg,

which are also graphically presented in Fig. 1. Table 1 shows significant effects of time, hygiene,

the interaction of time and destructibility (for both parameters) and the interaction of time and

hygiene (only for Iavg). Clean (HY) objects showed higher AMI and a higher Iavg than soiled

(NH) objects, but this difference appeared to be present already before time 0. Post-treatment

analyses that corrected for these pre-treatment differences, however, confirmed the main effect of

hygiene, namely decreased AMI in NH as compared to HY (see Table 2).

For overall AMI the highest levels were found at introduction of the object (time�18), at time

1 the lowest level was found, while times �1, 0 and 0.5 were at an intermediate level that was

much closer to time 1 than to time�18. By contrast, for overall Iavg the lowest level was found at

time 0, while significantly higher levels were found at the other times. The significant interaction

between time and hygiene for Iavg resulted from much lower values for NH as of time 0

compared to HY, indicating that the soiling (NH) treatment took immediate effect.

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232222

Page 6: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

The interaction between time and destructibility for both AMI and Iavg indicated generally

higher values for ND compared to DE on times �18 and 0 and the reverse (higher values for DE

compared to ND) as of time 0.5, indicating that the destructible (DE) objects became attractive as

of time point 0.5, i.e. after a 0.5 h time lag. The significant interactions with time indicating a

time lag for destructibility and an immediate effect of soiling were maintained in the post-

treatment analysis (see Table 2, AMIa and Iavga).

For the sound treatment no significant effects were found. However, a trend was found in the

post-treatment AMI analysis for an interaction between time and sound, in that no-sound at time

point 0.5 tended to be preferred both over no-sound at time points 0 and 1, and over sound at all

three time points.

The results from the analysis of Imax largely resembled the results of Iavg, as can be seen from

Table 2 and Fig. 2.

Table 2 shows that a number of significant effects were found for Ifreq. In addition to the

interactions between time and hygiene and between time and destructibility, there was also a

significant effect of replicate and a significant interaction between destructibility and sound. This

latter interaction was also found for other exploratory behaviour (OExpl). Both parameters (Ifreq

and OExpl) had significantly higher values for destructible sound producing objects as compared

to non-destructible sound producing objects. In addition, OExpl (but not Ifreq) had significantly

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 223

Table 1

Repeated measures ANOVA results for the behaviour-related parameters AMI (animal–material interactions) and Iavg

(average behavioural intensity) over time (from 18 h before to 1 h after treatment)

Behaviour Treatment �18 �1 0 0.5 1 Significance Total Significance

AMI DE 3.25 b 1.54 ef 1.57 ef 2.36 c 1.82 de 0.000 2.11 a NS

ND 3.73 a 2.04 cd 1.89 de 1.43 fg 1.07 g 2.03 a

HY 3.54 2.07 2.07 2.16 1.75 NS 2.32 a 0.002

NH 3.44 1.50 1.39 1.63 1.14 1.82 b

SO 3.54 1.75 1.79 1.68 1.39 NS 2.03 a NS

NS 3.44 1.82 1.68 2.11 1.50 2.10 a

Time 3.49 a 1.79 b 1.73 bc 1.89 b 1.45 c 0.002 – –

Iavg DE 0.89 bc 0.60 de 0.49 e 1.08 a 0.95 ab 0.020 0.80 a NS

ND 0.89 bc 0.86 ab 0.56 de 0.64 de 0.64 cde 0.72 a

HY 0.92 abc 0.77 bcd 0.76 cde 1.06 a 0.99 abc 0.035 0.90 a 0.001

NH 0.86 bcd 0.69 de 0.23 f 0.66 e 0.60 e 0.62 b

SO 0.93 0.66 0.51 0.81 0.70 NS 0.72 a NS

NS 0.85 0.81 0.55 0.90 0.89 0.80 a

Time 0.89 a 0.73 a 0.53 b 0.86 a 0.80 a 0.008 - -

Within blocks (separated by solid and dotted lines) estimated marginal means differ significantly when their character-

post-scripts differ. DE, destructible; ND, not destructible; HY, hygienic; NH, not hygienic; SO, with sound; NS, no sound;

NS, not significant.

Page 7: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

higher values for destructible sound producing objects compared to the destructible no-sound

producing objects (with other combinations having intermediate values that did not differ

significantly). The significance level of the interaction of destructibility and sound was

maintained for Ifreq in the post-treatment analysis, but not for OExpl (indicating that the effect

may have been an accidental finding for OExpl).

Finally, as Table 2 shows several additional significant effects were found, that cannot easily be

explained or understood. This was the case for a significant effect of replicate for the parameter

Feed, an interaction of replicate and time for the parameters Feed and Ifreq, and an interaction of

time, destructibility, hygiene and sound for the parameter Sit. These findings, however, may not

have been incidental, as they were also observed as trends in several other parameters (see Table 2).

Visual inspection of the graphs indicates that the curves for Tailwag and to some extent Ifreq

(Fig. 2) seem to resemble AMI (Fig. 1; see also Table 3 for correlations). In Tailwag, however, the

contrast HY-NH is more pronounced (esp. at time 0), while the contrast DE-ND is less

pronounced (and at time 0.5 it is absent).

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232224

Fig. 1. Estimated means for the behaviour-related parameter AMI and the intensity-related parameter Iavg over time

(indicated as hours before and after treatment). DE: destructible; ND: non-destructible; HY: hygienic; NH: not hygienic/

soiled; SO: sound; NS: no sound.

Page 8: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

3.2. Effects of time and treatment on less frequent behaviours

Fig. 3 shows several curves for parameters that were not sufficiently frequent to allow a

repeated measures ANOVA while containing potentially interesting information.

Visual inspection of the figure indicates an apparent similarity between the curves for

ChainDirB and Tailbite, with the notable exception that in ChainDirB there is a peak for DE at

time 0.5, while in Tailbite there is a peak for ND and a trough for DE at this time point.

For the AMI sub-behaviours (where the most prevalent behaviours were Bite, TryBite/Push,

StandProxy, and Nose) there was a progressive decline of StandProxy over time, there were peaks

for Nose at time 0, esp. for NH (i.e. soiled ropes may have been nosed more), and levering (Lever)

was increased at times 0 and 0.5, and esp. the objects that produced sounds showed elevated

levering compared to objects that did not produce sounds. Furthermore, biting (Bite) showed a

pronounced divergence between HY (up) and NY (down) at time 0. Chew increased after time 0,

esp. for the DE and HY treatments. Pull also increased after time 0, and pulling was higher for

HY than for NH objects as of time 0, while there was a (delayed) cross-over for the DE and ND

objects only after time point 0.5 h.

3.3. Relationships between intensities and frequencies of AMI

Table 3 presents the Pearson correlation coefficients for all 10 possible pairwise combinations

of the parameters AMI, Imax, Iavg, Ifreq and Tailwag. Nearly all coefficients were significant

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 225

Table 2

Significance levels (P < 0.05) and trends (P < = 0.1) for the factor combinations of behaviour-related parameters with

sufficiently frequent occurrence (Ly, Sit, Stand, Feed, OExpl, AMI, Tailwag, Imax, Iavg and Ifreq)

Factor combination Ly Sit Stand Feed OExpl AMI AMIa Tailwag Imax Iavg Iavga Ifreq

Time 0.010 0.001 0.055 0.002 0.000 0.008 0.023

Time � replicate 0.029 0.062 0.061 0.024

Time � TrDE 0.000 0.000 0.044 0.020 0.037 0.028

Time � TrSO 0.076

Time � TrHY 0.084 0.000 0.035 0.001

Time � TrDE � TrSO 0.090 0.096

Time � TrDE � TrHY

Time � TrSO � TrHY

Time � TrDE � TrSO � TrHY 0.103 0.046 0.097 0.030

Replicate 0.049

TrDE 0.102 0.054 0.019 0.099

TrSO

TrHY 0.002 0.008 0.033 0.000 0.001 0.000 0.096

TrDE � TrSO 0.045 0.051

TrDE � TrHY

TrSO � TrHY

TrDE � TrSO � TrHY 0.083

Only values 0.1 and below are shown. TrDE: destructibility treatment, i.e. destructible (DE) or not destructible (ND);

TrSO: sound treatment i.e. sound (SO) or no sound (NS); TrHY: hygiene treatment, i.e. hygienic (HY) or soiled (NH);

OExpl: other, i.e. pen- and pig-directed exploration excluding object and feeder; AMI: animal–material (=object)

interaction; Imax: maximum intensity of object directed behaviour; Iavg: average intensity; Ifreq: frequency of a fixed

intensity.a Analysis for post-treatment effects only, using times�18 and�1 as covariates to correct for incidental significant pre-

treatment differences.

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M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232226

Fig. 2. Average frequencies of the behaviour-related parameters Tailwag, Ly, Sit, Stand, Feed, Imax and Ifreq over time

(indicated as hours before and after treatment). DE: destructible; ND: non-destructible; HY: hygienic; NH: not hygienic/

soiled; SO: sound; NS: no sound.

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(except Imax-Ifreq, for which there was a trend). The highest correlation (0.85) was found for

Imax-Iavg, which were both recorded using the same sensor. The frequency-related parameter

AMI correlated only moderately to the intensity-related parameters (range 0.40–0.59). AMI

correlated best with Tailwag, which was recorded as a component of AMI, being the count of the

number of tail wagging animals that were interacting with the object (i.e. that were in AMI). Ifreq

showed very low correlations to both Imax (0.13) and Iavg (0.19), and correlated moderately with

AMI (0.42).

4. Discussion

4.1. Methodological considerations

This study has shown that intensity-related parameters can be measured, even on a

commercial farm. Four intensity-related parameters (Imax, Iavg, Ifreq and Tailwag) and the

conventional frequency-related AMI (animal–material interactions) were compared as measures

of enrichment value in relation to what constitutes ‘proper investigation and manipulation’ in

pigs. Moderate correlations between AMI and the intensity-related parameters indicate that AMI

is not a perfect predictor of behavioural intensities. In addition, the rather detailed classification

of AMI sub-behaviours could not ‘capture’ the intensity-related information in this study. In line

with the common conceptual framework for welfare assessment (Anon., 2001a; Willeberg, 1991)

these findings indicate that the conventional reporting of behavioural frequencies and durations

in applied ethology could benefit from being supplemented with measures of intensities, esp. for

the purpose of assessing animal welfare.

A far-reaching conjecture built on this view could be that (lay-) people ‘see’ behavioural

intensities, which applied ethologists adhering to ethograms may be ignoring. For animal welfare

it is important to bridge the gap between science and society as much as possible. Qualitative

assessment seems to be approaching this from the ‘society’ side (Wemelsfelder et al., 2001).

Perhaps, measures of behavioural intensities can help bridge the gap from the science side. The

observer (MB, who may be biased) did not notice any effect of sound at the time of recording,

while already at that time obvious effects were an immediate aversion for the soiled (NH) ropes

(there were several incidences of a pig dashing away after an initial sniff) and a delayed but

pronounced interest in the destructible ropes as of time point 0.5, indicating that the pigs did not

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 227

Table 3

Pearson correlations coefficients for all pairwise combinations of the parameters AMI, Imax, Iavg, Ifreq and Tailwag, and

their two-tailed significance levels

Variable pair Correlation Significance

AMI–Imax 0.40 0.000

AMI–Iavg 0.46 0.000

AMI–Ifreq 0.42 0.000

AMI–Tailwag 0.59 0.000

Imax–Iavg 0.85 0.000

Imax–Ifreq 0.13 0.077

Imax–Tailwag 0.38 0.000

Iavg–Ifreq 0.19 0.010

Iavg–Tailwag 0.46 0.000

Ifreq–Tailwag 0.31 0.000

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immediately notice that the object had been made destructible. In fact, at time point 0.5 the sensor

measuring Imax and Iavg appeared to underestimate the behavioural intensity of the interaction

with the destructible ropes. This resulted from the fact that the sensors were designed to record

object displacements rather than (intense) chewing while holding the object in a fixed location.

This type of behavioural intensity, which would complement the measures reported here, has

been measured previously by Feddes et al. (1993), who automatically recorded non-nutritive

chewing in pigs using tubes filled with air.

Following earlier work in relation to tail biting (e.g. Feddes and Fraser, 1994; Jankevicius and

Widowski, 2003) this study indicated that also in relation to enrichment materials it is in principle

possible to examine the importance of material properties relatively independent of material

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232228

Fig. 3. Average frequencies of notable but infrequent behaviours over time (indicated as hours before and after

treatment): ChainDirB, Tailbite, Nose, Lever, Bite and Chew. DE: destructible; ND: non-destructible; HY: hygienic;

NH: not hygienic/soiled; SO: sound; NS: no sound.

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type. The present design may be criticised for having been confounded with the material type

‘excreta’ in the case of the no-hygiene treatment. This, however, is inherent in the semantics of

the label ‘not hygienic’. More sophisticated object designs, however, are possible, allowing

investigation of other material properties such as smell and palatability, which are other

assessment criteria in the RICHPIG model and which may help unravel the importance of

contributing factors involved in the no-hygiene treatment. More limitations of this study will be

indicated below, e.g. the possible interaction between the sound and destructibility treatment and

the provision of the chain in the pen.

4.2. Importance of the three assessment criteria: destructibility, hygiene and sound

The central objective of this paper was to determine how the material properties ‘destructibility’,

‘hygiene’ and ‘sound’ of a 30 cm long straight sisal rope affected the behaviour and behavioural

intensities of growing pigs over time.

Main findings included significant effects of time, hygiene, time interacting with hygiene, and

time interacting with destructibility.

More pigs were interested in the hygienic rope than in the soiled (NH) rope, and they were

interested with a higher intensity. Furthermore, immediately post-treatment the interest in NH

was reduced. Destructible objects, however, became interesting relative to non-destructible

objects after a period of about 0.5 h.

There was no significant effect of sound, but there was a trend for an interaction between time

and sound when AMI (object play) was analysed for only post-treatment values (and correcting

for unexplained pre-treatment differences). The interaction tended to indicate that at time point

0.5 h objects that did not produce a sound attracted more pigs than objects that did produce a

sound. There were also other indications that the pigs did notice the sounds. A first (non-

scientific) impression derives from apparently elevated levering of objects making a sound at

times 0 and 0.5 h (compared to objects not making a sound). More importantly, a significant

interaction of destructibility and sound was found for Ifreq (indicative of exploration of the

object). Sound paired with destructibility increased Ifreq compared to sound paired with non-

destructibility. Together with the observation that the overall mean values of sound for AMI and

Iavg were lower (though not significantly lower) than the means of no sound (NS), this indicates

both attractive and distracting, perhaps even aversive, effects in response to the sounds. A

possible, though somewhat far-fetched explanation pointing also to a qualification of the results

with respect to sound being produced in this study by releasing three metal-chain links, could be

that the pigs already had a chain in the pen. The low-intensity sounds of the experimental

treatment could have been associated with the somewhat similar sounds of these indestructible

and familiar chains (which tended to produce a much louder sound, perhaps disturbing ‘noise’).

When interpreting these results with respect to the importance for the pig, it should,

furthermore, be realised that this study describes a process in time. At time �18, i.e. at

introduction of the object into the pen, there is a strong novelty effect, which is known to be

important for pigs (e.g. Wood-Gush and Vestergaard, 1991). AMI reached an overall average of

almost 3.5 pigs observed near the object shortly after introduction. This level of attention was not

reached later when attractive treatments were applied, e.g. when the rope had been made

destructible. A similar graphical pattern was found for the more frequency-related intensity

parameters (Tailwag and Ifreq). By contrast, the more intensity-related parameters (Imax and

Iavg) showed elevated levels after the more attractive treatments (DE and HY) as compared to the

moment of novel object introduction. Thus, fewer animals were showing more intense object

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 229

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manipulation, even above (though not significantly above) the level of what it had been when

novel. In line with the principles behind consumer demand theory it is likely that more intense

behaviour indicates a higher motivation, in this case a higher motivation to interact with the

object. When assessing the importance of enrichment treatments, information from the

frequency-related parameter AMI could, therefore, potentially benefit from being supplemented

with intensity-related parameters.

Another note concerning the interpretation in terms of ‘importance’ is that the results of this

study probably strongly depend on timing, e.g. the habituation period and the recording time after

treatment, and perhaps also on the material used for studying the material properties. In this study

sisal rope was used. Further work must show whether the findings can be replicated using other

materials. As to the time effect, in this experiment the habituation period was 18 h. In a pilot trial,

however, soiling of the material with excreta after a much shorter habituation period did not seem to

reduce AMI, indicating that novelty may override hygiene. Based on experiences from farmers and

casual observations from scientists (e.g. Stubbe, 2000), it can be expected that prolonged

habituation periods will result in more pronounced aversive effects of soiling. Similarly, prolonged

recording times after treatment may affect the results. In this study recording could unfortunately

continue until only 1 h after treatment because of impending breakdown of the destructible objects

(another main effect of time!). At that point in time there was an indication only for Ifreq to be

converging, while the other main parameters (AMI, Imax and Iavg) did not (yet).

With these qualifications of the study in mind, the conclusion of this section nevertheless is

that this study confirmed that the material properties destructibility and hygiene were (indeed)

important, whereas sound was much less important for the pigs.

4.3. Validation of RICHPIG

This study ‘validated’, i.e. generated support for, RICHPIG in four ways.

Firstly, it confirmed the thesis of the conceptual framework underlying RICHPIG that

measures of intensity need to be taken into account when assessing animal welfare.

Secondly, it was shown that in principle it seems to be possible to test assessment criteria, i.e.

material properties, independent of material type, thus supporting the view that the assessment

criteria in the model are not merely subjective. They can be examined experimentally.

Thirdly, it confirmed RICHPIG’s overall prediction that destructibility and hygiene are

important and that sound is much less important. Using the RICHPIG model weighting factors of

4.6, 6.3 and 1.3 had been calculated for Hygiene, Change (which includes destructibility) and

Sound, respectively (overall range for 30 assessment criteria: 1.2 for moveability to 12.45 for

Tail- and earbiting). A group of 8 European experts had given median scores of 7.0, 8.0 and 4.0,

respectively, and it was shown in an earlier study that experts considered sound to be significantly

less important than destructibility and hygiene, which did not differ significantly from each other

(Bracke et al., 2007b).

At a more detailed level, however, small differences were detected. Contrary to RICHPIG’s

prediction, this study found ambiguous results with respect to sound. The database did contain a

statement indicating that noise may be aversive, and it can be argued that sound should not be an

assessment criterion for enrichment materials for pigs at all. However, this study does not suffice

to draw this conclusion at present, as the results for sound may have been affected by the

presence of a chain in the pen (see above). A second difference is that whereas both the model

and the experts had given a higher score for destructibility than for hygiene, in this study the

effect of hygiene appeared to be more pronounced (see e.g. Table 2 and AMI, Fig. 1). These

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232230

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differences, however, are small and not ‘significant’, and may have depended on the

experimental set-up.

Finally, this study tended to ‘validate’ RICHPIG’s assumption of linear modelling as indicated

by the relatively low number of significant and meaningful interactions between assessment

criteria (see Table 2). More specifically, this study did not generate sufficiently clear scientific

information (i.e. could not sufficiently make sense of those interactions that were found)

warranting non-linear modelling under the parsimony rule.

Thus, this study provides preliminary support for RICHPIG, adding to the support we have

generated earlier by comparing the model with expert opinion (Bracke et al., 2007a,b).

4.4. Implications for research

To my knowledge, this is the first multifactorially designed study in which material properties,

rather than materials types, have been investigated in the context of environmental enrichment

for pigs. Other material properties such as smell and palatability can be tested in a similar way,

and other time-frames and test-materials should be examined to improve the understanding of

what motivates pigs to explore objects in their environment. This information does not only serve

a scientific interest, but is also relevant for designing and otherwise deciding on what constitutes

‘proper’ enrichment materials.

To date demand studies have required rather complex experimental conditions. To my

knowledge, this is the first empirical study emphasising the need to take measures of behavioural

intensities into account for assessing animal welfare, and one of the first to take such measures of

‘demand’ to the commercial farm. These measures have, however, been applied in a rather

experimental set-up. The two prototype AMI sensors also differed in terms of feasibility (costs),

reliability and validity. They generated interesting, but preliminary results and should be

modified and validated further, and, if possible, be supplemented with other measures of

behavioural intensities.

Acknowledgements

The hospitality of the farmers was greatly acknowledged, as was the tolerance of my family

for letting me do this work in ‘their’ time. Many thanks to Sandra Edwards for her comments on

the first draft of the paper.

References

Anon., 2001a. Scientists’ assessment of the impact of housing and management on animal welfare. J. Appl. Anim. Welfare

Sci. 4, 3–52.

Anon., 2001b. SPSS1 Base 11.0 User’s Guide. SPSS, Chicago, Illinois.

Blackshaw, J.K., Thomas, F.J., Lee, J.-A., 1997. The effect of a fixed or free toy on the growth rate and aggressive

behaviour of weaned pigs and the influence of hierarchy on initial investigation of the toys. Appl. Anim. Behav. Sci.

53, 203–212.

Bracke, M.B.M., Spruijt, B.M., Metz, J.H.M., Schouten, W.G.P., 2002. Decision support system for overall welfare

assessment in pregnant sows A: model structure and weighting procedure. J. Anim. Sci. 8, 1819–1834.

Bracke, M.B.M., Hulsegge, B., Keeling, L., Blokhuis, H.J., 2004. Decision support system with semantic model to assess

the risk of tail biting in pigs: 1. Modelling. Appl. Anim. Behav. Sci. 87, 31–44.

Bracke, M.B.M., Zonderland, J.J., Lenskens, P., Schouten, W.G.P., Vermeer, H., Spoolder, H.A.M., Hendriks, H.J.M.,

Hopster, H., 2006. Formalised review of environmental enrichment for pigs in relation to political decision making.

Appl. Anim. Behav. Sci. 98, 165–182.

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232 231

Page 15: Multifactorial testing of enrichment criteria: Pigs ‘demand’ hygiene and destructibility more than sound

Bracke, M.B.M., Zonderland, J.J., Bleumer, E.J.B., 2007a. Expert judgement on enrichment materials for pigs validates

preliminary RICHPIG Model. Appl. Anim. Behav. Sci. 104, 1–13.

Bracke, M.B.M., Zonderland, J.J., Bleumer, E.J.B., 2007b. Expert consultation on weighting factors of criteria for

assessing environmental enrichment materials for pigs. Appl. Anim. Behav. Sci. 104, 14–23.

Dawkins, M.S., 1990. From an animal’s point of view: motivation, fitness, and animal welfare. Behav. Brain Sci. 13, 1–61.

Feddes, J.J.R., Fraser, D., 1994. Non-nutritive chewing by pigs: implications for tail-biting and behavioral enrichment.

Trans. Am. Soc. Agric. Eng. 37, 947–950.

Feddes, J.J., Fraser, D., Buckley, D.J., Poirier, P., 1993. Electronic sensing of non-destructive chewing by growing pigs.

Trans. Am. Soc. Agric. Eng. 36, 955–958.

Grandin, T., Curtis, S.E., Greenough, W.T., 1983. Effects of rearing environment on the behaviour of young pigs. J. Anim.

Sci. 57 (Suppl. 1), 137.

Jankevicius, M.L., Widowski, T.M., 2003. Does balancing for color affect pigs’ preference for different flavored tail-

models? Appl. Anim. Behav. Sci. 84, 159–165.

Olson, C.L., 1974. Comparative robustness of six tests in multivariate analysis of variance. J. Am. Stat. Ass. 69, 894–908.

Sambraus, H.H., Kuchenhoff, R., 1992. The effects of environmental objects on the resting behaviour and behavioural

abnormalities of piglets. Tierarztliche Umschau. 47, 233–242.

Stubbe, A., 2000. Entwicklung und Beurteilung einer Beschaftigungstechnik fur mastschweine in intensiven Haltungs-

systemen. In: Institut fur Agrartechnik. Universitat Hohenheim, Hohenheim.

Van Calker, K.J., 2005. Sustainability of Dutch diary farming systems: A modelling approach. Phd-thesis, Wageningen

University, The Netherlands.

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. Appl. Anim. Behav. Sci. 84, 101–118.

Von Zerboni, N., Grauvogl, A., 1984. Verhalten landwirtschaftlicher Nutztiere. Verlag Eugen Ulmer, Stuttgart.

Wemelsfelder, F., Hunter, T.E.A., Mendl, M.T., Lawrence, A.B., 2001. Assessing the ‘whole animal’: a free choice

profiling approach. Anim. Behav. 62, 209–220.

Willeberg, P., 1991. Animal welfare studies: epidemiological considerations. Proc. Soc. Vet. Epid. Prev. Med. London 76–

82.

Wood-Gush, D.G.M., Vestergaard, K., 1991. The seeking of novelty and its relation to play. Anim. Behav. 42, 599–606.

Young, R.J., 2003. Environmental enrichment for captive animals. Blackwell, Oxford.

Zonderland, J.J., Vermeer, H.M., Vereijken, P.F.G., Spoolder, H.A.M., 2003. Measuring a pig’s preference for suspended

toys by using an automated recording technique. CIGR Ej. V, 1–11.

M.B.M. Bracke / Applied Animal Behaviour Science 107 (2007) 218–232232