objects as enrichment: effects of object exposure time and delay interval on object recognition...

Objects as enrichment: Effects of object exposure

time and delay interval on object recognition memory

of the domestic pig

Amanda K. Gifford *, Sylvie Cloutier, Ruth C. Newberry

Center for the Study of Animal Well-being, Department of Animal Sciences and Department of Veterinary and

Comparative Anatomy, Pharmacology and Physiology, Washington State University, Pullman, WA 99164-6351, USA

Accepted 12 October 2006

Available online 11 December 2006

Abstract

A modified spontaneous object recognition test was used to examine object recognition memory in the

domestic pig. This test uses preference for a novel object over a previously encountered sample object as

indicating recognition of the sample object, and no preference as indicating no recognition. Two factors

hypothesized to affect object recognition are duration of exposure to the sample stimulus and delay interval

before re-exposure. Both of these factors could be manipulated in a rotational object enrichment program for

pigs. Reducing exposure time and increasing the delay interval before re-exposure should decrease object

recognition and prolong novelty-induced object exploration. We exposed 5-week-old pigs to different

sample objects in their home pens for 10 min and 2 days, respectively. We tested for object recognition

memory at various delay intervals after initial exposure by placing littermate pairs in a test pen for 10 min

and recording snout contact with a sample object and a completely novel object. At a 1-h delay, half the pairs

were tested with the 2-day sample object; the other half received the 10-min sample object. At a 3-h delay,

pairs were tested with the opposite sample object. Pairs were also tested with the 2-day sample at a 5-day

delay and the 10-min sample at a 6-day delay. We predicted that pigs would show a preference for the novel

versus the 2-day sample object at all three delays, but would only prefer the novel object over the 10-min

sample object at the 1-h and 3-h delays. Pigs did not show novelty preference in the presence of the 10-min

sample object at any delay. Novelty preference in the presence of the 2-day sample object occurred at the 3-h

(P < 0.05) and 5-day delays (P < 0.001), but not the 1-h delay. The lack of novelty preference when pigs

were tested with the 10-min sample object may have been due to failure to habituate to the sample object.

Testing in a different location from the initial sample object exposure and retroactive interference from

exposure to the 10-min sample object may have contributed to a temporary lack of novelty preference when

pigs were tested with the 2-day sample object at the 1-h delay. The finding that pigs retained a memory for

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Applied Animal Behaviour Science 107 (2007) 206–217

* Corresponding author. Tel.: +1 509 335 2956; fax: +1 509 335 1082.

E-mail address: [email protected] (A.K. Gifford).

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

doi:10.1016/j.applanim.2006.10.019

mailto:[email protected]

http://dx.doi.org/10.1016/j.applanim.2006.10.019

the 2-day sample object for at least 5 days suggests that restricting object exposure to less than 2 days may

help to preserve the exploratory value of objects rotated among pens.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Pig; Cognition; Exploratory behaviour; Animal welfare; Environmental enrichment

1. Introduction

An important non-spatial memory ability not well described in pigs is memory for objects.

Knowledge of the robustness of object recognition memory in the pig, including when and

how recognition fades, would be useful for pig producers using objects in an environmental

enrichment program. The use of objects has produced inconsistent effects in the environmental

enrichment literature (Newberry, 1995). For example, Schaefer et al. (1990) and Moore et al.

(1994) found reduced aggression and tail-biting when pigs were provided with objects

whereas Schaefer et al. (1987), Pearce et al. (1989), and Pearce and Paterson (1993) found no

effect on aggression. Habituation to ‘‘toy’’ objects occurs rapidly in pigs (Apple and Craig,

1992), reducing the object’s usefulness in initiating exploration (Wemelsfelder and Birke,

1997). Nevertheless, use of solid, indestructible objects is of interest to producers because

such objects can be inexpensive to purchase and maintain, there are fewer hygiene concerns

than with provision of rooting substrates such as straw and soil, and they are compatible with

slatted flooring and liquid waste management systems (Mench, 1998; Van de Weerd et al.,

2003). While it seems clear that substrates for rooting are utilized by pigs for a greater

duration and frequency than objects (Van de Weerd et al., 2006; Scott et al., 2006), and have a

greater effect on welfare as indicated by decreased aggression and tail-biting (reviewed by

Bracke et al., 2006), objects of all types can provoke some exploration (Van de Weerd et al.,

2003).

If objects are to be provided as enrichment, it is important to find ways to make the objects

appealing to pigs. Novelty is an important property involved in initiating exploration (Berlyne,

1960) that has been reported to be intrinsically rewarding to pigs (Wood-Gush and Vestergaard,

1991). Incorporating novelty into the design of objects could be accomplished by using objects

with a variety of different complex properties that offer a level of unpredictability (Van de Weerd

et al., 2003). Novelty can also be attained by replacing familiar objects with new objects.

Realistically, pig producers do not have an endless supply of new objects to use, and would most

likely rotate objects among pens such that pigs would be exposed to the same object

intermittently. If pigs recognize a repeatedly encountered object as familiar, they would probably

not interact with it as they would a novel object. Little is known, however, about how long a pig

remembers objects. Therefore, it is the focus of this paper to address object recognition memory

in the domestic pig.

A specific test of object recognition memory exists in the rodent, non-human primate, and

human literature. This test is based on a spontaneous behaviour, whereby the subject will focus

on or explore a novel object for a longer duration than a familiar object (Berlyne, 1950; Ennaceur

and Delacour, 1988; Fagan, 1992). Since the behaviour is spontaneous, it is not necessary to train

the animals to learn a rule (i.e. choose ‘‘same’’ or choose ‘‘not-same’’) before testing. This

reduces the amount of time needed to obtain results.

While several investigators have looked at the exploratory behaviour of pigs towards novel

objects presented alone (e.g. Wood-Gush et al., 1990; Hemsworth et al., 1996), only two previous

A.K. Gifford et al. / Applied Animal Behaviour Science 107 (2007) 206–217 207

studies have specifically investigated the exploratory behaviour of pigs when both a novel and a

familiar sample object are presented together. Wood-Gush and Vestergaard (1991) provided 5-

week-old pigs with the opportunity to explore side pens attached to the home pen where they

could find and interact with objects placed there. One side pen contained a highly familiar object

while the other side pen contained a novel object. The authors found that, following experience in

this paradigm, pigs showed a preference for investigating the side pen containing the novel object

first, and spent more time exploring the novel object than the highly familiar object. From this

study, it seems that pigs can exhibit a spontaneous preference to explore novel objects over more

familiar objects. Using a test more closely related to Ennaceur and Delacour’s (1988) test of

rodent object recognition memory, Moustgaard et al. (2002) demonstrated that 13-month-old

Gottingen minipig boars could recognize previously seen objects after a delay of 1 h. In the test

trial, pigs explored a novel object more than an object they had seen previously for 10 min. These

studies point to the feasibility of using a spontaneous object recognition memory test to assess the

novelty value of objects used in enrichment programs for pigs.

In the rodent studies (Ennaceur and Delacour, 1988; Sik et al., 2003; Clark and Martin,

2005), two main factors affect recognition of a previously encountered sample object in a

memory test. The first is the initial amount of time a subject is exposed to the object. The

second is the delay between the initial exposure and a subsequent exposure. As initial

exposure time increases, a subject is able to remember an object for longer delays whereas, as

the delay interval increases, subjects show decreased recognition of the sample object. Both

of these factors could be manipulated in an enrichment program for swine facilities. Shorter

exposure times and longer delays between reintroduction of the same objects should increase

an object’s novelty at reintroduction and, therefore, an object’s effectiveness at stimulating

exploration.

To better understand the effect of exposure time and delay intervals on pig object recognition

memory, we exposed pigs to sample objects for a short exposure time (10 min) and a long

exposure time (2 days), and then tested them at different delay intervals (1 h, 3 h, 5 days, 6 days).

Their response to a novel object and a copy of a sample object was recorded in the test phase. We

predicted that pigs would show a preference for the novel object over the sample object

(indicating recognition of the sample object) at short delays (1 h and 3 h) for both exposure times,

but only for the long-exposure (2 days) object at longer delays (5 days or 6 days).

2. Methods

2.1. Subjects, housing and management

Subjects were 36 crossbred domestic piglets (sows of Large White � Yorkshire � Landrace lineage,

boars of Duroc � Hampshire lineage) from 9 different litters housed at the Washington State University

Swine Center. These litters were recruited from three different farrowing windows over the course of 1 year,

forming three batches of test litters (three litters, two litters, and four litters in Batches 1, 2, and 3,

respectively). After farrowing, sows and litters were kept in fully slatted farrowing crates (2.1 m

long � 1.8 m wide). According to standard practices in the United States, piglets were weighed at birth,

and had their teeth clipped, tails docked, and ears notched on day 1. Males were castrated at 7 days of age.

Litters were weighed and weaned at approximately 21 days of age, and four randomly selected piglets per

litter, two males and two females, were moved to fully slatted nursery pens (1.5 m � 2.4 m), where they

were housed as a litter group. Standard starter food (23% crude protein, 1.5% lysine, 3405 kcal DE/kg) and

water were available ad libitum. The temperature in the nursery room averaged 26 � 5 8C. The average light

intensity from the fluorescent bulbs was 416 lx and the photoperiod was 10L:14D, with lights on at 7 a.m.,

A.K. Gifford et al. / Applied Animal Behaviour Science 107 (2007) 206–217208

although heat lamps were left on continuously. At the end of the experiment (approximately 42 days of age),

all pigs were weighed and remained in the herd until they reached market weight.

2.2. Test pens

Initial presentation of sample objects occurred in the home pen of the pigs. Tests of object recognition

were conducted in one of two test pens (1.5 m � 1.7 m) made of plywood, painted black. Test pens were

located in the same room as the nursery pens. Black rubber mats formed the floor of the test pens. The mats

were covered with a layer of fresh straw, which we have previously observed to enhance exploration and

reduce freezing and escape attempts by pairs of pigs in these pens. The front wall of each test pen was

slanted outwards to allow for a clear view of the entire pen by a video camera suspended from the ceiling

directly above that wall. The pigs were habituated to the test pens with straw for nine, 15-min sessions (four

before weaning, five after weaning) prior to being placed in the test pens for the object recognition test.

During habituation, they were marked on the back with individual identification numbers using wax

livestock markers.

2.3. Object recognition memory tests

The experiment consisted of two phases, an initial presentation phase, where pigs were exposed to

sample objects for the first time, and a recognition test phase, where pigs were re-exposed to the sample

objects along with a completely unfamiliar object. The initial presentation phase began when pigs were

approximately 35 days old. Two identical sample objects were secured to the front wall of the nursery home

pen of each litter with plastic electrician’s ties. The objects were placed approximately 15 cm apart at pig

snout level. Within each batch of litters, two different sample objects were used, with no object being used

for more than two litters. The objects were left in the home pen for approximately 45 h (2 days), and became

the ‘‘long exposure’’ sample objects, designated LE. Two additional identical sample objects, of a different

type than the first two objects, were secured next to the LE objects in the home pens for the last 10 min of the

45-h period. These were labelled the ‘‘short exposure’’ sample objects (SE). At the end of the 45-h period, all

four objects were removed. Objects used during initial presentation and testing are listed in Table 1.

The first recognition test (Delay 1) began 1 h after the removal of all four sample objects from the home

pen. A duplicate of one of the sample objects, either LE or SE, was attached securely to one side of a test pen

at snout level with an electrician’s tie. One test pen was set up with LE, while the other was set up with SE. A

completely novel object was attached similarly to the opposite side of the pen. All four pigs from a litter

were tested simultaneously in one of the two test pens in the following way: one male and one female from

the litter were marked with wax livestock markers with their respective identification numbers, and placed

simultaneously on opposite sides of the test pen, facing a wall without objects. At the same time, the other

male and female from the litter were placed in the other test pen in an identical fashion. The side of the pen


Table 1

Objects used in exposure and test phases

Long exposure samples (LE) Short exposure samples (SE) Novel objects used in test phase

Garden hose, Cotton rope,

Red juice bottle,

Strip of tire inner tube,

Plastic grocery bag,

White dishcloth

Pink plastic utensils,

Wooden spoons with

coloured tops, Tiki Punch

soda can, Plastic grocery bag,

Cereal box half, Hefty EZ

foil pie tin

Newspaper roll, Cardboard

paper towel roll, Garden hose,

Cotton rope, Plastic grocery bag,

White dishcloth, Pink plastic utensils,

Squirt soda box, Safeway Apple Cider

packets cardboard box, Squirt soda can,

Hefty EZ foil pie tin, Strip of tire inner

tube, Red juice bottle, Wooden spoons

with coloured tops

on which the novel versus sample object was located, and the test pen that received LE versus SE in Delay 1,

was counterbalanced across test pens and litters. We chose to test pigs in pairs instead of singly due to a high

level of social reinstatement behaviour (vocalizations, escape attempts, freezing) and lack of object

exploration previously observed when we tried placing pigs into the pens alone, which persisted over

habituation sessions.

Once pigs were placed into the pens, video recording was started and experimenters left the room. Test

sessions ran for 10 min. At the conclusion of the test session, the video-recorders were stopped, pigs were

placed back in their home pens, and new sample and novel objects were secured in place of the ones just

used. Then a new litter was tested in an identical fashion to the first litter in a predetermined random order,

until all litters within the batch had been recorded. The timing of the initial presentation phase and the

recognition tests was staggered for the different litters within a batch to maintain a 1-h delay for all pairs.

Delay 3 tests were carried out 3 h after the end of the initial presentation phase (i.e. 2 h after the Delay 1

tests). The litters were tested in the same sequential order, following the same procedure as described above.

At this delay, pairs of pigs that had received the LE sample object in the first delay received the SE object,

and vice versa.

Delay 5 tests were conducted 5 days after the end of the initial presentation phase. The procedure on this

day was essentially the same except that only the LE sample object and a novel object were used for all pairs.

A subset of pigs (n = 16 out of 36) was also tested on the sixth day (Delay 6) after initial exposure to the

sample objects. During this test, all pigs received the SE sample object and a novel object in the test pen, and

were tested according to the procedure described above.

During all tests, clean gloves were used to handle objects when placing them in the test pens to avoid

contamination with pig and human odours. Duplicates of the sample objects were used for each litter at each

delay interval rather than the original objects so that relative attraction to the sample and novel objects was

not confounded by pig odours deposited on the sample objects in the home pen or during tests at earlier

delays. Multiple objects differing in colour, shape, and texture were chosen as LE, SE, and Novel objects

(Table 1) so that the reaction to novelty could be tested rather than the reaction to a specific object. While the

sample and novel objects were not matched with respect to ‘‘object type’’ (e.g. cloth, wood, rubber, plastic,

etc.), they were all ‘‘chewable’’ and most were ‘‘deformable’’, both characteristics found to be preferred by

pigs (Van de Weerd et al., 2003).

2.4. Video analysis

Videotapes of each pig-pair test were analysed to determine the duration of exploration of the sample and

novel objects. The 10 min of each video session were analysed in real time using a hand-held event recorder

(Workabout, Psion, PLC Inc., UK) and The Observer Software Package (Noldus Information Technology,

Wageningen, The Netherlands). The behaviour of each pig in a pair was analysed separately, and the amount

of contact with each object recorded to the nearest tenth of a second. Contact (i.e. object exploration) was

defined as touching the object with any part of the snout in front of the eyes. Contact was ended when the pig

turned away and took two steps, or when 5 s had passed since the last contact, as the bout criterion interval

was calculated to be 5 s using a log survivorship curve. All behaviour data were collected by the same

observer (AKG). Intra-observer reliability was calculated to be 95.1%. Data were also compiled for all pigs

concerning birth weight, weaning weight, and growth rate from weaning to the end of the experiment.

2.5. Statistical analysis

Behaviour towards the objects in the tests was averaged for pairs of pigs due to lack of statistical

independence between pigs of each pair. Variables calculated from measures of duration of contact with the

novel and sample object in the test pen are described in Table 2.

The variables D1 and D2 are difference scores measuring the amount of discrimination between the

novel and sample objects, with D2 correcting D1 for differences in overall exploratory activity (Ennaceur

and Delacour, 1988; Bussey et al., 1999; Sik et al., 2003). S2 is the total amount of snout contact with the two


objects in the test phase, also referred to as total exploration time. Since the two test pens were on opposite

sides of the nursery room, two separate measures of location preference were calculated. Side preference

within the pen was described by A1, and room orientation bias by B1.

For each exposure time, preference for either the novel or sample object at each delay was tested using

the Wilcoxon signed-ranks test for the variable D1. Preference for one side of the pen or one side of the room

over the other was also investigated using this method for the variables A1 and B1.

The effects of delay interval and order of testing with the LE versus SE sample objects were investigated

with a mixed model repeated measures analysis of variance (SAS Institute Inc., 1999). Order 1 pairs

received SE in Delay 1 and LE in Delay 3, and vice versa for Order 2 pairs. Order was the main factor in the

model, delay was the repeated measure, litter was a random effect and the subject effect was pair within

litter. Because the residuals for the variable D1 were not normally distributed, we applied the mixed linear

model to log10 transformed data for this variable although graphs and tables depict untransformed data.

Pairwise means comparisons for delay and order effects were made based on differences in least-squares

means, with P-values adjusted for multiple comparisons using the Tukey option in Proc Mixed. To examine

the effects of exposure time across delays, a priori planned contrasts were conducted.

3. Results

Piglets had an average birth weight of 1.84 � 0.06 kg, an average weaning weight of

6.88 � 0.17 kg and a growth rate from weaning to the end of the experiment (approximately 42

days of age) of 0.28 � 0.01 kg/day.

Wilcoxon signed-ranks tests revealed no preference for the novel or sample object at the 1-h

delay in pairs tested with either the LE (2 days) or the SE (10 min) sample object. At the 3-h

delay, only pairs tested with the LE sample object showed a significant preference for the novel

object (S = 18.5, N = 9, P = 0.03). Pairs tested at the 5-day delay showed a preference for the

novel object over the LE sample object (S = 60, N = 16, P = 0.0008), while pairs displayed no

preference between the novel and SE sample object at the 6-day delay (Fig. 1). No side bias or

room orientation bias was found for any delay or exposure time (Table 3; P > 0.05).

No significant main effects of Order or Delay were found for the difference in exploration

between the novel and sample object (D1) using the mixed model analysis of variance, although

Delay was almost significant (F3,44 = 2.65; P = 0.06). Delay was significant for the difference in

exploration between the novel and sample object after correction for total exploration time (D2)

(F3,44 = 2.98; P = 0.04). D2 scores in Delay 1, regardless of Order (or sample object exposure

time), were lower than D2 scores in Delay 5 (Table 3). More specifically, planned comparisons

revealed that D2 scores for pairs tested with the LE sample object in Delay 1 were significantly

lower than the same pairs’ D2 scores with the same sample object in Delay 5 (t44 = �3.53;

P = 0.001). This same response was seen when comparing D1 scores from pairs tested with the


Table 2

Variables calculated from contact with the objects in the test phase

Variable Description

D1 (Duration of contact with novel object) � (duration of contact with sample object in test phase)

S2 (Duration of contact with novel object) + (duration of contact with sample object in test phase)

D2 D1/S2, to control for differences in total exploratory activity

A1 (Duration of contact with object on left side of pen) � (duration of contact with object

on right side of pen)

B1 (Duration of contact with object nearest entry door into room) � (duration of contact

with object nearest back of room)

LE sample object at Delay 1 and Delay 5 (t44 = �3.12; P = 0.002). No significant results were

found for the variables side preference (A1) or room orientation bias (B1) (Table 3; P > 0.05).

No main effects were found for total object exploration time during testing (S2), but there was

a significant Order by Delay interaction (F3,44 = 3.26; P = 0.03). Pairs of pigs tested with the LE

sample object in Delay 1 (Order 2) explored the novel and sample objects for less time than pairs

tested with the SE sample object in Delay 1 (Order 1; t44 = �2.49; P = 0.02), and for less time

than when tested with the SE object in Delay 3 (t44 = �2.82; P = 0.01) and the LE object in Delay

5 (t44 = �2.48; P = 0.02; Fig. 2).

4. Discussion

Contrary to our predictions, our results show that pigs failed to display a novelty preference

when tested with the SE (10 min) sample object at any delay interval. One possible reason for this

result might be because the 10-min exposure time was insufficient for pigs to habituate to and

become familiar with the sample object. Studies of object recognition using novelty preference in

rodents and infants have generally used exposure times of a few minutes, with reliable novelty or

familiarity preferences at delays up to 24 h in rodents (Ennaceur and Delacour, 1988; Mitchell


Fig. 1. Wilcoxon signed-ranks test results for the discrimination score, D1 (mean � S.E.), at each delay for each sample

object exposure time. Values above zero indicate greater time spent with the novel object; below zero, more time spent

with the sample object. Asterisks indicate that the difference in exploration of the novel vs. sample objects is significantly

different from zero (*P < 0.05, ***P < 0.001).

Table 3

Effects of exposure time and delay on sample object discrimination (D2), pen side bias (A1), and room orientation bias

(B1) in seconds; mean � S.E.

Variable Long exposure sample object Short exposure sample object

Delay Delay

1 h 3 h 5 days 1 h 3 h 6 days

D2 �0.2 � 0.20a 0.4 � 0.10ab 0.5 � 0.09b 0.2 � 0.20 0.1 � 0.20 0.1 � 0.14

A1 �3.8 � 16.47 �1.8 � 20.88 �3.7 � 28.15 �44.2 � 26.20 52.6 � 39.26 �9.0 � 10.54

B1 11.8 � 15.99 21.2 � 19.49 36.8 � 26.51 �17.2 � 29.90 10.0 � 43.30 �11.6 � 10.17

Different letters indicate that results were significantly different (P < 0.01).

and Laiacona, 1998) and 3 months in infants (Courage and Howe, 1998). However, in these

studies, subjects were alone and alert when initially exposed to stimuli. Pigs in our experiment

were initially exposed to the sample objects while undisturbed in their home pen with their

littermates, which may have affected contact time with the objects. Whereas all pigs would likely

have noticed and contacted the LE objects over the course of 2 days, it is possible that some pigs

were resting during the 10-min exposure to the SE objects. Also, exposing pigs to objects in

groups may have stimulated play, which could have distracted some pigs from exploring and

learning about the objects. Wood-Gush and Vestergaard (1991) noted scampering and sparring

behaviour by pigs during tests which increased as inspection of the novel object decreased. An

increase in play has also been noted in children interacting with novel objects (Hutt, 1966). Since

we did not record pigs’ behaviour towards the sample objects in the home pen, it is impossible to

say how much of the exposure time was spent in contact with the objects versus engaging in other

activities such as playing and resting.

Our finding of a lack of novelty preference in the SE condition at the 1-h delay is inconsistent

with the results of Moustgaard et al. (2002) using Gottingen minipigs. In their experiment,

minipigs preferred a novel object over a sample object previously seen for 10 min after a delay

interval of 1 h. However, their experiment differed from ours in several key ways. First, the

minipigs were exposed to sample objects alone, which may have improved habituation to the

sample objects as mentioned above. Second, the minipigs were tested alone, whereas our pigs

were tested in pairs and the presence of one pig at an object may have sometimes limited

interaction with the same object by the other pig. Third, the minipigs were much older than our

pigs (13 months versus 5–6 weeks) and were likely more used to being handled. We chose 5-

week-old pigs for our experiment because Wood-Gush and Vestergaard (1991) showed that pigs

this age were capable of spontaneous novelty preference and object discrimination, and because

McLeman et al. (2005) showed that pigs as young as 6 weeks old could learn to discriminate

between individuals in an operant task, which requires more complex rule-learning than object

discrimination based on novelty preference. Despite their qualifications for a test of recognition

and memory, our pigs may have been too young to fully assimilate the sample object in a 10-min

period. In human infant recognition studies, as infants age, they require less familiarization time

to show novelty preference at a set delay, and show novelty preference for longer delays (Rose


Fig. 2. Effects of delay and sample object exposure time on mean � S.E. total time spent exploring (i.e. in snout contact

with) the novel and sample objects in the test phase. Differences in least squares means between exposure times and across

delays are denoted by different letters (P < 0.05).

et al., 2004). Future studies of object recognition should investigate how pig age affects the

amount of time it takes to completely familiarise with an object, as well as how long recognition

lasts. If significant differences are found, rotational programs of enrichment may need to be

modified to optimise object use for each age group.

While pigs failed to express novelty preference in the presence of SE sample objects, they did

show a significant preference for the novel object when tested using the LE (2 days) sample

object at the 3-h and 5-day delays, indicating recognition of the sample object. These results fit

our prediction that pigs would be able to recognize a sample object, previously experienced for 2

days, after long delays. However, pigs showed no preference for the novel object over the LE

sample object at the shortest delay interval, 1 h. In most of the rodent, non-human primate, and

human infant literature, this null result would be interpreted as a failure to recognize the sample

object. Failure to show a novelty preference at the 1-h delay may have resulted from a

discrepancy between the exposure environment and the testing environment. Human adults

exposed to visual stimuli in one environment and tested in another show impaired performance

on a visual recognition task (Richmond et al., 2004). Also, relocating a familiar object to a novel

location causes it to regain some novelty (Galani et al., 1998; Platt and Novak, 1999). Pigs in our

experiment were exposed to the sample objects in their home pens, and tested in a different test

environment, which could have impaired performance at the 1-h delay. Since pigs were re-

exposed to the sample object in the test environment at the 1-h delay, this may have prevented

impairment at later delays. On the other hand, pigs receiving the LE sample object at the 3-h

delay had not previously experienced this sample object in the test environment, because they

were tested with the SE sample object at the 1-h delay; yet they showed a novelty preference.

Another explanation for the lack of novelty preference over the LE sample object at the 1-h

delay could be retroactive interference, due to the presentation of the SE sample object in the

home pen 1 h prior to testing. Due to the similar nature of the stimuli, pigs may have been

impaired in their retrieval of the information about the LE sample object in the test situation. In

tests of spatial memory, pigs were susceptible to retroactive interference when the interfering

stimulus was similar to the task stimulus (Laughlin et al., 1999). Also, in a test of short-term

social memory in rats, disturbances during the delay interval, including the introduction of a new

juvenile rat, disrupted recognition of the original juvenile stimulus rat (Burman and Mendl,

2000). As the effects of retroactive interference can be transient and fade with time (Fagan,

1977), this may explain why pigs were able to show a novelty preference at the 3-h and 5-day

delays. The possibility of interference in the retrieval of an object’s memory raises some

interesting questions about the effect of presenting multiple objects to the pigs during the delay

period, as would occur with a rotational enrichment system. It is possible that interference could

shorten the time before an object could be reintroduced and treated as novel by the pigs.

Interestingly, Wood-Gush and Vestergaard (1991) noted a return of interest in the familiar object

after the pigs had interacted with the novel objects in the test sessions. This may be an area for

future study.

Pigs receiving the LE sample object at the 1-h delay explored both the sample and novel object

for significantly less time than their counterparts receiving the SE sample object at the same

delay. They also explored less at the 1-h delay than they did when tested at later delays of 3 h and

5 days. While it is unclear why pigs responded less to the objects in this condition than the others,

a decrease in the motivation to explore objects in general could have contributed to the low

interaction with the novel object even if the pigs recognized the sample object as familiar.

Overall, our prediction that increasing exposure time would result in novelty preference at

longer delays was supported. We found that pigs preferred a novel object over a sample object


that they had previously encountered over a 2-day period, at delays up to 5 days, but not one they

had previously encountered for only 10 min, even when tested only 1 h later. This implies that

rotational programs of environmental enrichment using objects should be most effective when

the exposure time to the objects is less than 2 days and the delay before re-exposure is greater than

1 week, although we were unable to determine from our experiment when recognition of the long

exposure sample object would have faded.

Our second prediction, that we should see decreasing novelty preference over increasing

delays, was unsupported by our results. The persistence of the response to novelty 5 days after

initial exposure suggests strong memory for the sample object following a 2-day exposure time.

However, multiple exposures to the sample object on discrete occasions could have strengthened

the memory trace. Mumby et al. (2000) found that multiple discrete exposures to the sample

object increased rats’ abilities to discriminate between novel and familiar objects from a few

hours to weeks. It is plausible that combined with the long initial exposure, the second exposure

to the 2-day sample object at the 1-h or 3-h delay served to enhance the pigs’ memory for the

object at the 5-day delay. This could be problematic for a rotational enrichment system, as each

exposure to a particular object would strengthen the memory for that object and facilitate

recognition at longer delays.

In a standard production setting, rather than being given a choice between a familiar object

and a novel one, pigs may only be given one object at a time. It will be necessary to determine if

interaction times with this object are correlated with novelty preference. If so, then we could be

confident that results from object recognition tests to assess memory of objects are applicable to

commercial enrichment programs.

As mentioned previously, future studies could look at the effect of age on object recognition

and memory, as well as how the presentation of different objects in the delay phase would

influence recognition, and the memory-enhancing effects of multiple presentations of the same

object on discrete occasions. Following the methodology from the cognitive literature more

closely (test pens separate from the home pen, initial exposure and recognition tests conducted in

test pen, short exposure and delay times) may make results more comparable to other cognitive

studies. This would be useful if we want answers to basic questions about pig memory and

recognition. To avoid confusion in the interpretation of null results, it would be beneficial to

delegate pigs to treatment groups receiving only one sample object for one exposure time.

However, this may make interpreting the results in terms of environmental enrichment for

commercial pigs more difficult, due to the different factors at play (i.e. multiple pigs, long

exposure times, long delays, multiple exposures to the same object). In this case, since our results

suggest that the memory interference at short delays was only temporary, testing pigs at multiple

delay periods will differentiate between null results indicating recognition failure due to

insufficient habituation or memory decay over time versus those indicating a temporary

disruption in memory retrieval due to special circumstances such as retroactive interference.

5. Conclusions

We conclude that a 10-min exposure to a sample object was not enough time to familiarise

pigs to the object under the conditions of our study, possibly because exposing young pigs to the

object in groups while undisturbed in their home pen resulted in insufficient interaction with the

object. A 2-day exposure (with a 10-min re-exposure after 1-h or 3-h delays) was enough time to

familiarize pigs with a sample object for at least 5 days. This implies that pig producers should

aim for object exposure times of less than 2 days to retain pig interest in exploring objects upon


reintroduction of the objects to the pen following rotation to other pens. We also found that when

a long exposure period is followed by the introduction of a different object and then testing in a

different location after a short delay, it is possible to observe a temporary lack of novelty

preference. With some refinements in methodology, the spontaneous object recognition test

could prove valuable for assessing factors affecting object recognition in the domestic pig and

contribute to improved object enrichment programs.

Acknowledgements

We thank T.M. Donaldson, T. McGinn, J. Tilton, and J. Powers for assistance with data

collection and the staff of the Washington State University Swine Center for assistance with care

and handling of animals. This research was supported by a grant from the Washington State

University (WSU) Alcohol and Drug Abuse Program to RCN and Tracy L. Skaer and by an

Undergraduate Research Scholarship from the WSU Alcohol and Drug Abuse Program to AKG.

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