Vocal and locomotor responses of piglets to social isolation and reunion

Vocal and LocomotorResponses of Piglets to SocialIsolation and Reunion

Valentina Colonnello1,2

Paolo Iacobucci1,2

Ruth C. Newberry1

1Department of Animal Sciencesand Department of Veterinary

and Comparative AnatomyPharmacology and Physiology

Center for the Study ofAnimal Well-being

Washington State UniversityPullman, WA 99164-6351

E-mail: [email protected]

2Department of PsychologyUniversity of Rome ‘‘Sapienza’’

Via dei Marsi 78, 00185 Rome, Italy

ABSTRACT: Potentiation of infant isolation calls following a brief reunion withthe mother is considered an index of filial bonding in altricial rodents. Weinvestigated potentiation of isolation and reunion responses in 15-day-oldunweaned domestic piglets (Sus scrofa domesticus). When piglets were re-isolatedfollowing a brief, comforting reunion with their mother and littermates in theirhome pen, they displayed a persistence (relative potentiation) of calling andjumping. In contrast, when re-isolated following a brief interaction with theirmother or an unfamiliar sow in a familiar or unfamiliar location, or with littermatesalone, calling rate and locomotion dropped. Subsequently, piglets spent more timenear their mother’s face if they had previously interacted with an unfamiliar sowrather than their mother, consistent with maternal recognition. Although we did notdetect maternal potentiation as described in altricial rodents, filial attachmentbonding was clearly evident in piglet responses, especially during reunions. � 2009Wiley Periodicals, Inc. Dev Psychobiol 52: 1–12, 2010.

Keywords: maternal potentiation; filial attachment; social bonds; vocalizations;domestic pig; swine

INTRODUCTION

In humans, a filial attachment bond can be distinguished

from other kinds of social relationships by the selective

seeking of proximity to a caregiver to obtain security and

comfort, in conjunction with emotional distress during

periods of involuntary separation from the caregiver,

emotionally significant reunions, and a persistent as

opposed to transitory bond (Ainsworth, 1989; Bowlby,

1973; Cassidy, 1999). In other mammals, some degree of

filial attachment of an infant to its mother is needed for

nurturance of the infant. However, there is variation across

species in the strength and selectivity of social attachment

depending on life history variables (Newberry &

Swanson, 2008), and not all filial relationships meet the

criteria for an attachment bond as described in humans.

Filial attachment in humans has been investigated

by means of separation-reunion procedures, such as the

‘‘strange situation’’ test (Ainsworth, 1989; Polan & Hofer,

1999). Infant responses to separation have also been

investigated extensively in rodent models (Herman &

Panksepp, 1978; Hofer, Brunelli, & Shair, 1993; Hofer &

Shair, 1978; Moles, Kieffer, & D’Amato, 2004; Muller,

Brunelli, Moore, Myers, & Shair, 2005; Panksepp,

Nelson, & Bekkedal, 1997; Pettijohn, 1979). Analysis of

vocalizations following separation or isolation has been of

particular interest for gaining insights into rodent filial

attachment (Brunelli & Hofer, 2007; Iacobucci, Colon-

nello, Pavan, & Ricceri, 2007; Shair, 2007).

Studies exploiting a repeated isolations test, which is

a three-session procedure involving a first isolation

followed by a brief reunion with the caregiver and

then a second isolation, have revealed a ‘‘potentiation’’ of

calls by infant laboratory rats during the second isolation

(Hofer, Brunelli, Masmela, & Shair, 1996; Hofer,

Brunelli, & Shair, 1994; Hofer, Masmela, Brunelli, &

Developmental Psychobiology

Received 4 February 2009; Accepted 10 August 2009Valentina Colonnello and Paolo Iacobucci contributed equally to this

work.Correspondence to: R. C. NewberryContract grant sponsor: National Council of the University of Rome

‘‘Sapienza,’’ ItalyPublished online 22 September 2009 in Wiley InterScience

(www.interscience.wiley.com). DOI 10.1002/dev.20406

� 2009 Wiley Periodicals, Inc.

Shair, 1998; Shair, 2007; Shair, Masmela, Brunelli, &

Hofer, 1997). Specifically, whereas control pups that

remain isolated in the second session of the test show a

reduction in calling during the third session, pups that

are re-isolated after experiencing a brief reunion with

their mother call at over two times the rate observed in the

first isolation, an effect attributed to a reward expectancy

violation (Hofer et al., 1996; Polan & Hofer, 1999).

This phenomenon, dubbed ‘‘maternal potentiation,’’ is

selectively induced by reunion with the mother and not

by littermates or home cage shavings. Nevertheless,

interaction with an unfamiliar adult female during session

2 of the test provokes a similar increase in calling rate

indicating that, despite the terminology, the potentiation is

not elicited solely by the rat’s mother. Furthermore,

when rat pups are reared in the presence of an adult

male, potentiation of calling also emerges after a

brief interaction with an unfamiliar adult male (reviewed

by Shair, 2007). A ‘‘contact quieting’’ effect, whereby

the rate of calling decreases dramatically during reunions

with the mother, has also been reported in rats (Hofer &

Shair, 1978; Shair, 2007). This effect is less selective

than maternal potentiation, being evoked by many

other factors that could be perceived as comforting

including exposure to littermates, warmth, a furry sub-

strate and home cage bedding (Hofer & Shair, 1978; Shair,

2007).

The human filial attachment bond is a unique

psychological relationship of the infant to the caregiver

that is highly emotionally significant during both

separations and reunions (Ainsworth, 1989). Data do not

robustly support the existence of this kind of bond in infant

laboratory rats. Among several critical aspects (for a

review, see Panksepp, 2003), we consider the lack of

specific greeting responses upon reunion with the dam or

littermates as a main issue. Even so, the rat studies suggest

that the phenomenon of maternal potentiation may be

useful for characterizing the emotional content of social

bonds in species showing more selective filial attachment.

Research using the repeated isolations procedure in

the guinea pig provides some support for this idea. In

the guinea pig, exposure to the mother does not increase

the rate of calling by infants in the second isolation, as

found in rats, but it does prevent the decrease in the

rate of calling observed in control pups (Hennessy, Miller,

& Shair, 2006). This relative, although not absolute,

potentiation is selective for the mother and is not observed

following interaction with littermates or other adult

females. Although a promising finding, the external

validity of maternal potentiation as an index of infant

emotional attachment to the mother (and other caregivers)

would be strengthened by evidence for this phenomenon

in other mammalian species exhibiting filial attachment

bonds.

In the present study, we investigated maternal poten-

tiation in the domestic pig, Sus scrofa domesticus, a

widely available precocial species that is endowed with a

sophisticated social life commencing with the develop-

ment of maternal recognition soon after birth (Morrow-

Tesch & McGlone, 1990; Newberry & Wood-Gush, 1985,

1986; Parfet & Gonyou, 1991; Schon, Puppe, Gromyko, &

Manteuffel, 1999). Piglets and sows are highly vocal

during typical social interactions, such as suckling bouts

and reunion episodes, and during brief periods of

involuntary isolation (Algers, 1993; Illmann, Schrader,

Spinka & Sustr, 2002; Puppe, Schon, & Wendland, 1999;

Spinka, Stehulova, Zacharova, Maletinska, & Illmann,

2002; Weary, Appleby, & Fraser, 1999; Weary, Ross, &

Fraser, 1997). When isolated, pigs usually begin

emitting relatively quiet, low-pitched grunts interspersed

with silence (listening). If a reunion is not immediately

forthcoming, isolation-induced calls escalate in rate,

pitch, volume, and duration (Fraser, 1975), correlated

with activation of a physiological stress response

(Schrader & Todt, 1998). As in reunions between infants

and caretakers in humans (Ainsworth, Blehar, Waters, &

Wall, 1978), reunions between piglets and sows are

characterized by an active ‘‘greeting’’ interaction. Imme-

diately upon reunion with their mother, piglets typically

emit a rapid series of ‘‘quack’’ calls near the sow’s face

(Illmann et al., 2002). Young piglets direct these greeting

calls specifically towards their mother, although occa-

sionally older piglets may also direct these calls towards

other familiar adults in the social group (Newberry,

personal observation). Piglets show signs of individual

recognition of their mother’s voice, responding to her

nursing calls by running directly towards her rather than to

other sows emitting nursing calls during synchronized

nursing bouts (Newberry & Wood-Gush, 1985). There is

also evidence that sows are able to recognize their own

piglets by voice (Appleby, Weary, Taylor, & Illmann,

1999; Illmann et al., 2002; Maletinska, Spinka, Vichova,

& Stehulova, 2002; Weary, Lawson, & Thompson, 1996).

From these findings, it can be inferred that domestic

piglets form a selective attachment bond with their

mother.

The aim of our study was twofold: (1) to investigate the

face validity of the domestic pig for studies of filial

attachment bonding, and (2) to investigate whether the

level of maternal potentiation detected in laboratory rats

can be found in a nonrodent species exhibiting filial

attachment bonding. We focused on two criteria charac-

terizing infant attachment bonds: responses to involuntary

separation and responses to reunion. Since reunion calls

are evident in piglet–sow interactions (in contrast to rat

infant–mother interactions), we decided to observe the

reunion subsequent to the second as well as the first

isolation session, introducing a fourth session into the

Developmental Psychobiology2 Colonnello, Iacobucci, and Newberry

classic repeated isolations procedure. To establish

whether young piglets exhibit an emotional response to

involuntary displacement from, and reunion with, their

mother in the absence of an immediate need for warmth

or nourishment, we conducted the research in a warm

environment, excluded relatively small piglets from our

sample, and tested piglets after completion of nursing

episodes. We took these steps to rule out potential

confounding effects as it is known that small, cold, and

hungry piglets call more when isolated, and elicit a

stronger response from their mother, than larger, warmer

and more satiated piglets (Weary & Fraser, 1995; Weary

et al., 1996, 1997).

The study comprised four experiments. In Experiment

1, we evaluated both male and female piglets for the

presence of maternal potentiation. We predicted that a

brief reunion with the mother and littermates in the home

pen following a temporary separation would increase (i.e.,

potentiate) the rate of calling during a second isolation

whereas control piglets not experiencing the reunion

would show a decrease in calling rate during the second

isolation period. If a brief reunion increases the aversive-

ness of a subsequent isolation, it is possible that it would

also increase the rewarding nature of the following

reunion. We predicted, therefore, that the reunited piglets

would show a stronger vocal response during a second

reunion than the control piglets.

The results of Experiment 1 indicated a persistence

of isolation calls after reunion with the mother and

littermates. To understand whether this effect was induced

specifically by interaction with the mother, in Experiment

2, we focused on the vocal and locomotor responses of

piglets when re-isolated following a brief interaction

with their mother or an unfamiliar adult female alone in

an unfamiliar location. We hypothesized that piglet

responses to re-isolation are specifically influenced by

the brief interaction with their mother. Our prediction was

that piglets briefly reunited with their mother, but not an

unfamiliar sow, would call at a greater rate in the second

than the first isolation. By contrast, we predicted that

interaction with an unfamiliar female would produce a

decline in call rate during the second isolation. We also

expected a difference in the rate of calls emitted during the

reunions. In particular, we predicted a stronger response in

piglets exposed to the mother during both the reunion

sessions. There was an absence of maternal potentiation in

Experiment 2, possibly because the sows were agitated in

the unfamiliar location used for reunions. Therefore, in

Experiment 3, we exposed piglets to their mother or an

unfamiliar sow alone in the sow’s home pen. Predictions

were as for Experiment 2. In Experiment 4, we

investigated whether the persistence of calling detected

in Experiment 1 could be induced by exposure to siblings,

or the familiar home pen, alone. We hypothesized that

neither of these conditions would be sufficient to elicit a

potentiation effect.

Because we found no sex differences in Experiment 1,

we conducted Experiments 2, 3, and 4 with females only.

We were especially interested in female responses

because, in a natural context, pigs live in a matrilinear

society comprising several sows and their young, and

female offspring tend to remain in the natal group as adults

and maintain long-term relationships with their mother

whereas males disperse (Gonyou, 2001; Graves, 1984;

Newberry & Wood-Gush, 1986).

All testing was carried out on postnatal day 15. At this

age, the mother-young relationship is well established and

nursing episodes occur approximately once per hour. In a

natural context, the piglets would be actively exploring

their environment at this age, resulting in brief voluntary

separations from the mother and the use of vocalizations

and locomotion to relocate the mother in different

locations within the home range (Newberry & Wood-

Gush, 1985, 1986).

METHODS

Subjects, Housing, and Husbandry

Subjects were 15-day-old crossbred domestic piglets (genetic

background: sows predominantly Large White and boars from

Landrace, Yorkshire, Duroc and Hampshire lineages) housed

with their mother (1st to 6th parity) and littermates in 2.1 m

long� 1.8 m wide farrowing pens with porous floors. The pens

were located in farrowing rooms containing 12 pens within the

Washington State University Swine Center. Average litter size

was 11 piglets (range 8–14 piglets). In accordance with standard

practices in the United States, piglets were weighed at birth,

tooth clipped, tail docked, ear notched, and vaccinated against

atrophic rhinitis on postnatal day (PND) 2, and males were

castrated on PND 7. Room temperature was 17� 1�C, and a heat

lamp in each pen provided supplementary heat for the piglets.

Fluorescent lighting was provided for 11 hr daily, with lights on

at 0530 hr. Sows were fed a standard lactation diet twice daily

and provided with water ad libitum.

Treatments

Experiment 1—With Mother and Littermates in Home Pen

Versus Empty Pen. Four piglets (2 males and 2 females) of

similar body weight at birth, from each of eight litters born

within a 12-day period, were selected for testing. Small piglets

(runts) were excluded from the study. Of the four selected

subjects per litter, one male and one female were randomly

assigned to a Home Pen (HP) treatment group and the other male

and female to an Empty Pen (EP) treatment group (within litter

design). They were marked on the back with a wax livestock

marker 48 hr prior to testing to facilitate identification. Each

subject (n¼ 32) was subjected to a four-session test on PND 15:

(1) a 7-min isolation session (Iso1), (2) a 1-min reunion session

Developmental Psychobiology Isolation and Reunion Responses of Piglets 3

(R1), (3) a second 7-min isolation session (Iso2), and

(4) a second 1-min reunion session (R2). During the two

isolation sessions, piglets were individually isolated in an empty

1.7 m� 1.5 m observation arena with a concrete floor, located in

an empty observation room. During R1, piglets in the HP group

were placed in their home pen containing their mother and

littermates and piglets whereas piglets in the EP group were

placed alone in an empty farrowing pen of the same size and

features as their home pen, located in an empty farrowing room.

During R2, piglets from both groups were reunited with their

mother and littermates in their home pen. The same procedures

were used in all subsequent experiments with the following

exceptions.

Experiment 2—With Mother Versus Stranger in Unfamiliar

Pen. One female from each of eight litters was assigned to a

Mother in Unfamiliar Pen (MUP) treatment group and a second

female per litter was assigned to a Stranger in Unfamiliar Pen

(SUP) treatment (within litter design). For the test, each piglet

was: (1) isolated for 7 min (Iso1), (2) placed in a farrowing pen

alone with her biological mother (MUP group) or an unfamiliar

lactating sow (SUP group) in an empty farrowing room for 1 min

(R1), (3) re-isolated for 7 min (Iso2), and (4) reunited with her

mother and littermates in the home pen for 1 min (R2). The

mother or stranger was moved temporarily into the empty

farrowing room and placed alone in a farrowing pen with

food and water 2–9 min before R1. The unfamiliar sow was

genetically unrelated to the piglet being tested (i.e., no aunts or

adult sisters were used) and, to ensure that the sow’s appearance,

odor and vocalizations were unfamiliar to the piglet, was from a

different farrowing room to that in which the piglet resided. A

different unfamiliar sow was used for testing the SUP piglet of

each litter. After the piglet was removed for Iso2, the sow was

returned to her home pen for R2.

Experiment 3—With Mother Versus Stranger in Sow’s Home

Pen. In this experiment, one female from each of eight litters

was assigned to a Mother in Home Pen (MHP) treatment group

while a second female was assigned to a Stranger in her

Home Pen (SHP) treatment (within litter design). Each piglet

was: (1) isolated for 7 min (Iso1), (2) placed in her own farrowing

pen alone with her biological mother (MHP) or alone with an

unfamiliar lactating sow in the stranger’s home pen (SHP) for

1 min (R1), (3) re-isolated for 7 min (Iso2), and (4) reunited with

her mother and littermates in the home pen for 1 min (R2). All

piglets from the home pen of the mother or stranger were

removed prior to R1 (placed in an empty farrowing room as a

littermate group), and returned prior to R2. The stranger sow was

genetically unrelated to the piglet being tested, but was from the

same farrowing room to that in which the piglet resided. A

different stranger sow was used for testing the SHP piglet of each

litter.

Experiment 4—With Littermates in Home Pen Versus Empty

Home Pen. Two female piglets from each of eight litters were

randomly assigned to a Littermates in Home Pen (LHP) or

Empty Home Pen (EHP) treatment group, respectively (within

litter design). Each subject was tested in: (1) a 7-min isolation

session (Iso1), (2) a 1-min reunion session (R1) in the home

pen with her littermates (LHP) or in the home pen alone (EHP),

(3) a second 7-min isolation session (Iso2), and (4) a second

1-min reunion session (R2) with her mother and littermates in the

home pen. Mothers in LHP, and mothers and littermates in EHP,

were removed to a farrowing pen in an empty farrowing room

prior to R1, and returned prior to R2.

General Procedures

Subjects from each litter were tested in counterbalanced order

for sex (Experiment 1) and experimental treatment. All testing

was carried out between 0900 and 1500 hr. Because different

litters within a farrowing group were born on different days, tests

at PND 15 were conducted over multiple days. The durations of

the isolation and reunion sessions were selected taking into

consideration the frequency of nursing episodes (about one per

hour) and our intention to observe separation responses without

inducing excessive stress or fatigue in piglets. The reunion

sessions were particularly brief given that ‘‘greeting’’ calls are

emitted only briefly and immediately upon reunion with the

mother (Illmann et al., 2002).

It took approximately 40 s to transport piglets between

farrowing rooms and the observation room where Iso1 and Iso2

occurred. Piglets were carried in a clean opaque gray box

(61 cm� 40 cm� 42 cm), used to minimize stress related to

handling. Preliminary observations indicated that piglets emitted

few calls when transported in the box (data not reported). During

reunion sessions, piglets were introduced from the back of the

pen to minimize any disturbance to the sow resulting from

human presence. The temperature in the farrowing rooms and

observation room was set at an equivalent level and adjusted

prior to each test if needed. After each isolation session, the floor

of the observation arena was cleaned with paper towels and a

diluted alcohol solution, and two fans were activated to eliminate

odor. The empty farrowing room used for reunion sessions in

Experiment 2 was cleaned with a pressure hose at the end of each

reunion session.

To avoid testing when piglets were hungry, piglets were not

disturbed during nursing bouts. Since nursing occurred at

intervals of approximately 1 hr, we were able to test two piglets

per inter-nursing interval, starting after the litter completed

the post-letdown teat massage phase of the nursing bout

(Algers, 1993; Jensen, Gustafsson, & Augustsson, 1998). During

Experiment 1, the sow started to nurse her piglets during R1 on

three occasions. In these cases, the test was terminated and a

substitute piglet from that litter, of the same sex and approximate

birth weight as the original subject, was tested after the nursing

bout had finished.

Recording Equipment

During isolation sessions, data were collected using a video

camera (Sony DCR-HC21 Handycam MiniDV Camcorder,

Sony Electronics Inc., San Diego, CA) and a uni-directional

(cardiod) microphone (Sennheiser/Microphone Madness

MM-HLSC-Lapel; working range 30–20,000 Hz; Microphone

Madness, Inc., Palm Coast, FL) suspended from the ceiling. The


camera and microphone were connected to a video monitor and

computer, respectively, located in an adjacent room. The

computer was equipped with a Creative Sound Blaster 16 PCI

sound card (recording sampling rate 48 kHz, 16 bit; Creative

Labs, Inc., Milpitas, CA) and ‘‘SeaPro’’ sound recording

software (CIBRA, http://www.unipv.it/webcib/res_software_

uk.html, University of Pavia, Pavia IT). To avoid the recording

of calls associated with handling during introduction to the

arena, recording started 10 s following placement of the piglet

into the arena. A Sony DCR-HC21 Handycam MiniDV

Camcorder was used to collect audiovisual recordings during

the reunion sessions.

Data Collected

We recorded both vocalizations and locomotor activity to

elucidate whether the hypothesized maternal potentiation in pigs

was restricted solely to calling as in rats (Hofer et al., 1996;

Myers et al., 2004; Shair et al., 1997), or extended to activity as

reported in guinea pigs (Hennessy et al., 2006). In addition to

determining the number of calls uttered by the piglet during the

7-min isolation sessions, we assessed two measures of locomotor

activity: (1) the number of crossings of virtual lines dividing the

observation arena into five equal squares as viewed on a monitor

during videotape analysis, where a crossing was counted when a

line was crossed with all four trotters, and (2) the number of

jumps, defined as jumping up against the wall with all four

trotters leaving the floor. During the 1-min reunion sessions, we

determined the rate of calling and the time spent in proximity to

the sow’s face, defined as the total number of seconds spent with

the piglet’s head within 10 cm of the sow’s mouth. All behavioral

data were collected by trained observers blind to the treatments,

and exhibiting high inter-observer concordance (>95%).

In Experiment 1, we recorded piglet body temperature just

before Iso1 and just after Iso2 using an infrared thermometer to

confirm whether body temperature of piglets in the two treatment

groups remained unaffected by exposure to different rooms

during R1. We did not collect body temperatures in the other

experiments because R1 sessions were conducted in the same

room for all piglets.

Statistical Analysis

Statistical analyses were conducted using Statview II software

(Abacus Concepts, Inc., Berkeley, CA). Because the isolation

and reunion sessions differed in duration and context, the data on

responses to isolation and reunion were analyzed separately for

each experiment. Except where noted, data were analyzed using

ANOVA, with litter as a blocking factor. Jumping frequencies

during isolations were not normally distributed and, therefore, an

SQRT transformation was performed prior to analysis. Post-hoc

means comparisons were performed using Tukey’s Honestly

Significant Differences test.

For Experiment 1 isolation sessions, we analyzed treatment

and sex effects on vocalizations, line crossing, jumping, and

body temperature, with test session (Iso1 vs. Iso2) as a repeated

measure. In R1, piglets in the EP treatment were isolated and,

therefore, their behavior was not comparable with that of HP

piglets during R1, or behavior in R2. Therefore, we compared

vocalizations and time spent near the sow’s face during R1

versus R2 sessions by piglets in the HP treatment only, with sex

as a main effect and test session (R1 vs. R2) as a repeated

measure. For R2, we analyzed treatment and sex effects on these

variables. There were no main effects or interactions involving

the factor ‘sex of piglet’ and so sex differences were not

considered further.

In Experiments 2 and 3 we determined treatment effects on

vocalizations, line crossing, and jumping during isolations, and

vocalizations and time spent near the sow’s face during reunions,

with test session (Iso1 vs. Iso2 or R1 vs. R2) as the repeated

measure.

In Experiment 4, we determined treatment effects on

vocalizations, line crossings, and jumping during isolations,

with test session (Iso1 vs. Iso2) as the repeated measure. Because

EHP piglets were isolated during R1, their behavior was not

compared with that of LHP piglets in R1, or their own behavior in

R2. We compared piglet vocalizations by LHP piglets during R1

(sow absent) versus R2, and vocalizations and time spent near the

sow’s face by EHP versus LHP piglets in R2, using paired t-tests.

RESULTS

Experiment 1—With Mother and Littermates inHome Pen (HP) Versus Empty Pen (EP)

Isolation Sessions. A brief interaction with the mother

and littermates during R1 affected the number of calls

emitted during Iso2 (Treatment: F(1, 7)¼ 6.1, p¼ .04).

The number of calls was significantly lower in Iso2 than

Iso1 in the EP group; by contrast, the HP group showed no

change in rate of calling (Session: F(1, 7)¼ 11.7,

p¼ .011; Treatment� Session: F(1, 7)¼ 19.5, p¼ .003;

post-hoc comparison EP-Iso1 versus EP-Iso2, p< .01;

Fig. 1A).

There was a treatment� session effect on jumping

(F(1, 7)¼ 5.8, p¼ .047). Piglets in the HP group jumped

more than piglets in the EP group during Iso2 (p< .05),

whereas there was no difference between treatments in

Iso1 (Fig. 1B). For the HP group, the post-hoc comparison

between Iso1 and Iso2 was p¼ .051. There was no

treatment effect on line crossings in the isolation sessions

(p> .05). Fewer line crossings (n/7 min) occurred in Iso2

(40.9� 6.2) than Iso1 (86.2� 6.3; Session: F(1,

7)¼ 102.9, p< .001) but this decrease was not treatment

specific (Treatment� Session: p> .05).

Piglet body temperature was stable from Iso1

(32.7� .15�C) to Iso2 (33.5� .26�C) in both treatment

groups (main effects and interaction, p> .05).

Reunion Sessions. In the HP group, the rate of calling

(R1: 7.9� 1.0; R2: 6.5� 1.4 calls/min) and time spent

in proximity to the sow’s face (R1: 13.1� 1.1 s; R2:

10.6� .9 s) did not differ across reunions sessions


(p> .05). In R2, EP piglets uttered more calls than HP

piglets when reunited with their mother and siblings

(Treatment: F(1, 7)¼ 6.9, p¼ .03; Fig. 1C). Furthermore,

EP piglets spent more time near their mother’s face than

HP piglets when reunited in R2 (Treatment: F(1, 7)¼ 5.8,

p¼ .047; Figure 1D).

Experiment 2—With Mother (MUP) VersusStranger (SUP) in Unfamiliar Pen

Isolation Sessions. An overall decrease in the rate of

calling was exhibited in Iso2 compared with Iso1

(Session: F(1, 7)¼ 16.0, p¼ .005; Fig. 2A). Line crossing

also decreased (Iso1: 84.3� 7.3; Iso2: 37.7� 6.2;

F(1, 7)¼ 59.2, p< .001), whereas rate of jumping

(untransformed mean, 4.5� .8 jumps/7 min) was stable,

across isolation sessions. There were no treatment, or

treatment� session, effects on any of these variables

(p> .05; Fig. 2B).

Reunion Sessions. The sows were agitated when isolated

in the empty farrowing room. They tried to escape from

the pen and vocalized repeatedly. During the reunions, the

piglets emitted not only the ‘‘quack’’ calls typically

emitted during reunions but also a range of other calls.

There was no significant effect of treatment, session,

or treatment� session on total calls emitted (p> .05;

Fig. 2C) but there was a significant treatment� session

interaction for time spent near the sow’s face (F(1,

7)¼ 11.8, p¼ .011); SUP piglets spent more time near

their mother’s face than MUP piglets in R2, and more time

near their mother’s face in R2 than the stranger’s face in

R1 (p< .05 in post-hoc comparisons; Fig. 2D).

Experiment 3—With Mother (MHP) VersusStranger (SHP) in Sow’s Home Pen

Isolation Sessions. Both MHP and SHP piglets

decreased their rate of calling in Iso2 compared with

Iso1 [Session: F(1, 7)¼ 18.8, p¼ .003] and no significant

treatment, or treatment� session, effects were revealed

(Fig. 3A). The number of line crossings was also lower in

Iso2 (38.6� 5.7) compared to Iso1 (85.5� 8.7) [Session:

F(1, 7)¼ 43.8, p< .001] in both treatments, whereas the

number of jumps was stable across isolation sessions in

both treatments (Fig. 3B).

Reunion Sessions. The sows appeared calm when left

alone in their own farrowing pen after removal of their

piglets for R1. The analysis revealed a significant main


FIGURE 1 Mean (�SE) responses of piglets in Experiment 1

during a four-session test: Iso1, isolated for 7 min; R1, reunited

with mother and littermates in the home pen (HP) or placed in an

empty pen (EP) for 1 min; Iso2, isolated for 7 min; and R2,

reunited with mother and littermates in the home pen for 1 min.

(A) Calls in isolation sessions (n/7 min; EP-Iso1>EP-Iso2).

(B) Jumps in isolation sessions (SQRT transformed n/7 min;

HP-Iso2>EP-Iso2). (C) Calls in R2 (n/min; EP>HP). (D) Time

spent near mother’s face (s) in R2 (EP>HP). Post-hoc

comparisons, �p< .05; ��p< .01.



in an unfamiliar pen with mother (MUP) or stranger (SUP) for

1 min; Iso2, isolated for 7 min; and R2, reunited in home pen with

mother and littermates for 1 min. (A) Calls in isolation sessions

(n/7 min; Iso1> Iso2 for both MUP and SUP). (B) Jumps in

isolation sessions (SQRT transformed n/7 min). (C) Calls in

reunion sessions (n/min). (D) Time spent near sow’s face (s) in

reunion sessions (SUP-R2> SUP-R1; SUP-R2>MUP-R2).

Post-hoc comparisons, �p< .05, ��p< .01.

6 Colonnello, Iacobucci, and Newberry

effect of session on calling [F(1, 7)¼ 14.9, p¼ .006], with

both MHP and SHP piglets calling less in R2 than R1.

Treatment, and treatment� session, effects on calling

were nonsignificant (Fig. 3C). However, SHP piglets

spent more time near their mother’s face than MHP piglets

in R2, and more time near their mother’s face in R2

than the stranger’s face in R1 [Treatment� Session:

[F(1, 7)¼ 8.2, p¼ .02; p< .01 in post-hoc comparisons;

Fig. 3D].

Experiment 4—With Littermates in Home Pen(LHP) Versus Empty Home Pen (EHP)

Isolation Sessions. Piglets in both LHP and EHP groups

called less in Iso2 compared with Iso1 [Session: F(1,

7)¼ 29.2, p¼ .001; Fig. 4A], and crossed fewer lines

[Iso1: 85.1� 6.2; Iso2: 34.9� 5.1; Session: F(1,

7)¼ 55.2, p< .001], but no significant treatment, or

treatment� session, effects were revealed. The rate of

jumping was stable across isolation sessions in both

treatments (p> .05; Fig. 4B).

Reunion Sessions. LHP piglets emitted more calls

during reunion with their mother and littermates in

R2 (10.1� 2.9 calls/min) than during reunion with

littermates alone in R1 (3.9� 1.2; Session: T(7)¼�2.81, p¼ .026). They also called less in R1 than piglets

in an empty home pen in R1 (50.1� 11.4). No differences

in rate of calling (Fig. 4C), or time spent near the mother’s

face (Fig. 4D), were detected between the LHP and EHP

piglets during the second reunion (p> .05).

DISCUSSION

Responses to Isolation

Based on previous findings in rats (Shair, 2007), we

predicted that a brief reunion with the mother

and littermates in the home pen during R1 would result

in a higher rate of calling during Iso2 than Iso1 whereas,

in the absence of a reunion during R1, calling rate

would be lower in Iso2 than Iso1. We also hypothesized

that potentiation of calling would be specific to

the mother rather than being elicited by other social

stimuli such as littermates and unfamiliar sows. Thus, we

predicted that reunion with the mother would potentiate

calling whereas interaction with an unfamiliar sow

would produce a decline in call rate during the second

isolation.




in sow’s home pen with mother (MHP) or stranger (SHP) for

1 min; Iso2, isolated for 7 min; and R2, reunited in home pen with


(n/7 min; Iso1> Iso2 for both MHP and SHP). (B) Jumps in

isolation sessions (SQRT transformed n/7 min). (C) Calls in

reunion sessions (n/min; R1>R2 for both MHP and SHP).

(D) Time spent near sow’s face (s) in reunion sessions

(SHP-R2> SHP-R1; SHP-R2>MHP-R2). Post-hoc compari-

sons, �p< .05, ��p< .01.



in home pen with littermates (LHP) or alone (EHP) for 1 min;

Iso2, isolated for 7 min; and R2, reunited in home pen with


(n/7 min; Iso1> Iso2 for both LHP and EHP). (B) Jumps in

isolation sessions (SQRT transformed n/7 min). (C) Calls in R2

(n/min). (D) Time spent near mother’s face (s) in R2. Post-hoc

comparisons, �p< .05, ��p< .01.

Isolation and Reunion Responses of Piglets 7

Contrary to our predictions, piglets did not show the

classic form of potentiation described in rats (elevated

calling in Iso2 relative to Iso1) in any of the four

experiments. We expected, and found, less calling and line

crossing in Iso2 than Iso1 in the absence of a reunion with

the mother in R1, including when placed in an empty

unfamiliar pen, alone in the home pen, with a stranger sow,

or with littermates in the absence of the mother. However,

unexpectedly, we found that less calling and line crossing

also occurred in Iso2 than Iso1 when piglets were reunited

specifically with their mother in R1. In Experiment 2, we

thought that this weakened response in Iso2, antithetical to

maternal potentiation, could have been due to R1 taking

place in an unfamiliar location. The sows appeared

agitated and the piglets displayed a high rate of calling

under this condition, suggesting that the R1 reunion was

not comforting. However, the results of Experiment 3

show that, even when the R1 reunion occurred with an

apparently calm mother in the home pen, fewer calls and

line crossings occurred in Iso2 than Iso1. Therefore, we

were not able to detect a maternal potentiation effect

specific to reunion with the mother, contrary to our

prediction based on the rat literature.

Despite the absence of maternal potentiation, when

piglets were reunited with their whole family (mother and

littermates) in their familiar home pen in R1, they

exhibited a persistence, rather than a drop, in calling from

Iso1 to Iso2, unlike their response in any other condition

that we tested. This finding suggests that reunion with

a calm mother and littermates in the home pen was

maximally reassuring, thereby stimulating, or perhaps

physically enabling (due to relative preservation of

energetic reserves in R1), the relatively strong reinstate-

ment behavior in Iso2. This outcome makes sense from an

evolutionary perspective because it would presumably be

adaptive to call in an attempt to reinstate contact when

conditions favor a safe reunion, and to be quieter when

sows have recently been signaling distress, as in the MUP

and SUP conditions, or when a potentially dangerous

change in the environment has recently been detected

(e.g., pen or room is different, stranger is present, or

mother and/or littermates are missing, in R1).

Hennessy et al. (2006) observed a similar persistence

rather than potentiation of calling in Iso2 in guinea pigs,

which they referred to as a relative potentiation, but the

response was specific to the mother. Although the piglets

exhibited maternal recognition (see below), it appears that

they did not discriminate the mother alone as the primary

source of comfort under the conditions of this study,

possibly because the piglets were confined in farrowing

pens and littermates were always present along with the

mother. If so, one might expect a similar lack of maternal

specificity in laboratory rodents, which are confined in

cages. At least under confined housing conditions, the

difference between piglet and rodent responses may relate

to the fact that rodent maternal care is more individu-

alized; unlike rodent mothers, sows do not lick individual

piglets or retrieve them in their mouth. Nevertheless,

housing sows and litters in get-away pens that allow sows

to leave their piglets voluntarily for brief periods (Pajor,

Kramer, & Fraser, 2000), or under free-range conditions,

would allow piglets to develop a more individualized

response to isolation and reunion from their mother.

Observations of pigs under free-range conditions suggest

that it is the mother who is the most important determinant

of the movements and social groupings of unweaned

piglets (Newberry & Wood-Gush, 1986). Although 15-

day-old piglets also direct affiliative behavior towards

their littermates and spend more time in close proximity

with their littermates than with their mother, they do not

exhibit strong preferences for specific littermates at this

age whereas they clearly have a selective attachment to

their mother (Newberry & Wood-Gush, 1986).

In contrast to the strong potentiation of calling in rats,

the lesser persistence response exhibited by piglets and

guinea pigs during a second isolation may be related to

their precociality, making them better equipped to cope

with short separations from their mother and littermates in

an unfamiliar location than relatively helpless rat pups. By

15 days of age, piglets are capable of navigating among

different nest sites as well as exploring new areas and

playing out of visual, and sometimes auditory, contact

with their mother (Donaldson, Newberry, Spinka, &

Cloutier, 2002; Newberry & Wood-Gush, 1985, 1986;

Newberry, Wood-Gush, & Hall, 1988). Under commercial

swine production conditions, they are also able to survive

weaning at this age.

In altricial laboratory mice subjected to the repeated

isolation paradigm (Iacobucci et al., 2005; Scattoni,

Crawley, & Ricceri, 2009), the extent of calling given

by infants in a second isolation can vary according to

genetic strain, age, and methodological details. Therefore,

we cannot rule out the possibility that pigs might exhibit a

potentiation of calling, equivalent to that observed in rats,

under some circumstances.

We took multiple steps to ensure that our piglets were

not hungry or cold during testing, thereby minimizing

the piglets’ immediate need for resources to maintain

physiological homeostasis, a factor known to influence

calling rate in piglets (Weary & Fraser, 1995; Weary et al.,

1996, 1997). The persistence of calling in Experiment 1,

in the absence of pain or urgent physiological needs,

points to the importance of psychological comfort derived

from contact with the mother and littermates in the safety

of the nest (home pen) in eliciting a relatively strong

response in Iso2. Although we found no treatment-

specific potentiation of line crossing in the observation

arena from Iso1 to Iso2 in any experiment, in agreement


with findings in rats (Shair, 2007), we did observe a

persistence (and almost a potentiation, p¼ .051) of

jumping in Iso2 of Experiment 1 following reunion with

the mother and littermates in the home pen. The brief

reunion may have stimulated renewed attempts to escape

from the observation arena in anticipation of reinstating

contact with the family. An active response by piglets can

be explained by their precocial nature, unlike that of

altricial, relatively immobile rat pups whose calls elicit a

maternal retrieval response. Likewise, exposure to the

mother prevented a drop in motor activity during a second

isolation in another precocial species, the guinea pig

(Hennessy et al., 2006). However, in piglets, jumping

responses were persistent across both isolation sessions

regardless of treatment. In contrast, line crossings

probably dropped in Iso2 because the relatively small

arena had already been explored in Iso1 and, now, activity

was focused on escape from the arena.

It remains unclear whether the degree of potentiation

following re-isolation accurately depicts the strength of

filial attachment, given that both piglets and guinea pigs

show a relative rather than absolute potentiation of calling

despite having a more selective filial attachment bond than

rats.

Responses to Reunion

Although piglets called and moved around the arena less

in Iso2 than Iso1 regardless of whether they had just met

their mother alone, or another adult female, in R1, these

results were not due to failure to recognize their mother.

Piglets spent more time near their mother’s face during R2

than a stranger’s face during R1, and more time near their

mother’s face in R2 if they had just met another sow rather

than their own mother in R1, regardless of whether R1

occurred in a relatively familiar or unfamiliar location.

These results confirm that the piglets were able to

distinguish between their mother and the unfamiliar

sow, as reported in other studies of maternal recognition

by piglets (Illmann et al., 2002; Morrow-Tesch &

McGlone, 1990; Parfet & Gonyou, 1991; Puppe et al.,

1999).

We predicted that piglets reunited with their mother in

the presence or absence of their littermates during R1

would show a stronger vocal response during R2 than

piglets placed in an empty pen or exposed to an unfamiliar

sow during R1. In contrast to our prediction, the rate of

calls emitted by piglets during R2 was greater for EP than

HP piglets in Experiment 1 and comparable across the

pairs of treatments evaluated in the other experiments.

Looking at all treatments together, it appears that there

was a numerical tendency for piglets to call more in R2 if

they had encountered an unfamiliar pen or sow in R1 (EP,

MUP, SUP, SHP) than if they had been placed in their own

home pen in R1 (HP, MHP, LHP, EHP). Modulation of

reunion calling as a function of exposure to novel

conditions indicates that these calls were not emitted in

a fixed, predetermined pattern but varied according to the

context of the social reunion. Time spent close to the

mother’s face in R2 was significantly higher for piglets

that had been placed in a novel pen or with another sow

(EP, SUP, SHP) rather than with their own mother (HP,

MUP, MHP) in R1, suggesting that piglets that experi-

enced a longer separation from their mother, especially in

a novel location, were more motivated to seek proximity

to her face.

The rate of calling during the reunions was strongly

affected by the quality of the interaction with the sow. In

Experiment 1, the mean call rate during the 1-min

reunions (for R1 of the HP group and R2 of both the HP

and EP groups) was 14.3� .8 calls/min whereas the mean

rate of calling during the 7-min isolations (for both the HP

and EP groups across both isolation sessions) was

49.6� 2.9 calls/min. Although these numbers are not

directly comparable because the reunion sessions were

shorter than the isolation sessions, piglets usually vocalize

only briefly during reunions and so prolonging the reunion

sessions would have resulted in a lower, rather than higher,

mean calling rate/min. Our data are, thus, indicative of a

dramatic ‘‘contact quieting’’ effect during the reunions in

Experiment 1, as previously described in rats (Hofer &

Shair, 1978; Shair, 2007). ‘‘Contact quieting’’ was also

evident in Experiment 4, when the presence of littermates

in R1 lowered calling compared to Iso1 or exposure to the

empty home pen. By contrast, in Experiment 2, the mean

rate of calling during reunions (for both MUP and SUP

groups in R1 and R2) was 75� 5.4 calls/min, comprising

a variety of vocalizations and not just the ‘‘quack’’ calls

typical of face-to-face interaction with the sow. This value

was even higher than the mean rate of calling during

isolations in Experiment 2 (50.1� 3.7 calls/min, for both

MUP and SUP groups across Iso1 and Iso2), supporting

the interpretation that the reunions were less comforting in

the presence of a sow alone. A high rate of calling in R1

also occurred when piglets met a relatively calm sow

alone in her home pen in Experiment 3, suggesting that it

was the absence of littermates that prompted the elevated

levels of calling. Calling was reduced following reunion

with the whole family in R2 in Experiment 3 but not in

Experiment 2, possibly due to greater disturbance from

the R1 reunion with an agitated sow in an unfamiliar room.

The absence of sex differences in responses to reunion

in Experiment 1 is interesting given that, theoretically, one

would expect that, under good conditions, mothers of

polygynous species should show greater maternal invest-

ment in sons than daughters (Trivers & Willard, 1973).

The high prolificacy of sows and rapid growth of piglets

under intensive farm management (as in the present study)


could be interpreted as conditions favoring male-biased

investment. One mechanism by which male offspring

could command greater maternal investment than females

would be to perform more calling (a form of ‘‘begging’’

behavior) than females when reunited with their mother.

However, this was not observed, probably because piglets

suckle as a litter rather than individually and differences in

milk provisioning by the sow to individual piglets within a

litter are primarily determined by direct competition

among piglets for high-yielding teats and, following

establishment of the teat order, by the amount of teat

massage performed by each piglet towards ‘‘its’’ teat

(Dostaikova, Spinka & Kindlmann, 2002).

CONCLUSIONS

The combined gestalt of the mother and littermates in their

familiar location induced a optomistic persistence of

reinstatement responses (protest) following re-isolation,

whereas any unfamiliar conditions encountered during the

first reunion provoked despair-like responses when

piglets were re-isolated. We refer to despair rather than

habituation to the isolation because, especially for EP and

SUP piglets, responses in R2 were suggestive of having

missed the mother and siblings. Findings on proximity-

seeking towards the mother, expressed by calls and

physical proximity, show the value of adding the second

reunion to the classic isolation–reunion–isolation proce-

dure.

Our results, in combination with those of Hennessy

et al. (2006) in guinea pigs, suggest that the potentiation

paradigm is extendable to precocial species but these

species may be more likely to exhibit persistence rather

than the potentiation observed in rats. The observation

that piglets exhibited emotional responses to separation

from, and reunion with, both their mother and littermates

indicates the importance of careful evaluation of

responses in relation to the biology of individual species.

We have demonstrated that the domestic pig can provide

useful insights into aspects of attachment, such as

production of ‘‘greeting’’ calls and seeking of maternal

proximity upon reunion, that cannot be addressed in rat

models. Our data extend understanding of filial attach-

ment bonding in the domestic pig, and reveal similarities

between piglet and human infant responses to both

isolation and reunion.

NOTES

V.C. was supported by a scholarship from the National Council

of the University of Rome ‘‘Sapienza,’’ Italy. The authors are

grateful to Professor Gianni Pavan (University of Pavia, IT) for

providing access to the SeaPro Sound Emission Analyzer

software for recording and analysis of audible and ultrasonic

vocalizations, Winnie Chan, Nicole Dossey, Joe Gallegos,

Chesica Jones, Satomi Kaneko, Jacob Larson, Brooke Reed,

Rachel Reynolds, and Kaori Tokuhisa for help with data

collection, Asa Timm and the staff of the WSU Swine Center

for animal care, and two anonymous reviewers for helpful

comments on the manuscript.

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Documents

Vocal and locomotor responses of piglets to social isolation and reunion