Hormones and Behavior 52 (2007) 130 – 138

www.elsevier.com/locate/yhbeh

Stress, behaviour and reproductive performance in female cattle and pigs

Eberhard von Borell a,⁎, Hilary Dobson b , Armelle Prunier c
a
Institute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin-Luther-University Halle-Wittenberg, 06108 Halle, Germany
b
Department of Veterinary Clinical Sciences, Faculty of Veterinary Science, University of Liverpool, Leahurst, Neston, Wirral CH64 7TE, UK
c
INRA, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, 35590 Saint-Gilles, France
Received 26 March 2007; revised 27 March 2007; accepted 27 March 2007
Available online 31 March 2007

Abstract

Female farm animals are exposed to a great variety of environmental and management related stressors. As a consequence, their reproductive
and maternal abilities may be compromised through mechanisms acting on the hypothalamic, pituitary, ovarian and uterine function. Responses to
short- and long-term stressors may differ as short-term stressors often fail to affect reproduction or even may have stimulatory effects. Thus, the
stress response induces diverse neuroendocrine reactions that can either increase or decrease the probability of an animal reproducing depending
on the specific situation. The aim of the present review is to summarise the current knowledge on the stress concept and its implications on
behaviour and reproductive performance in cows and female pigs as phenomena reported in laboratory animals are unable to explain all effects
encountered in domesticated farm animals.
© 2007 Elsevier Inc. All rights reserved.

Keywords: Stress; Reproduction; Behaviour; Regulation; Cows; Pigs

Concept of stress and its implications for reproductive
performance
Stress is defined as a biological response elicited when an
individual perceives a threat to its homeostasis and the threat
that causes stress is referred to as a stressor (Moberg, 2000).
Others define stress as the inability of animals to cope with their
environment (Broom and Johnson, 1993) or even unfitness to
adapt to the environment and reproduce effectively (Ewing et
al., 1999). The response to stressors requires a progression of
events beginning with sensing and signalling the animal's
various biological mechanisms that a threat exists. These events
are followed by activation of neurophysiologic mechanisms to
resist and prevent major damage. The various sensory detectors
not only receive information but transform that information into
neural signals that are transmitted to either cognitive and/or
non-cognitive centres of the nervous system to generate a co-
ordinated response to the challenge. This response may be
behavioural, autonomic, neuroendocrine and/or immunological.
⁎ Corresponding author. Fax: +49 345 5527106.
E-mail address: eberhard.vonborell@landw.uni-halle.de (E. von Borell).
0018-506X/$ - see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2007.03.014
Rapid responses to stressors are mediated by the sympathetic
adrenal medullary system (SAM) which involves the central
nervous system (CNS); these neural pathways activate release
of epinephrine by the adrenal medulla and norepinephrine by
peripheral sympathetic nerves. The hypothalamic–pituitary–
adrenocortical (HPA) stress-response system mediates a longer-
term, sustained response with the involvement of major adrenal
cortical hormones such as glucocorticoids and mineralocorti-
coids. Two classical stress response systems result in different
temporal and context specific coping patterns whereby the
sympathetic nervous system is primarily activated in situations
of threat, whereas the HPA system is involved during loss of
control (Henry and Stephens, 1977). Koolhaas et al. (1999)
correlated the type of stress response of animals to individual
coping styles. Proactive coping involves low HPA-axis
reactivity, but high sympathetic reactivity (increased concentra-
tions of catecholamines) and reproductive hormones. In
contrast, reactive coping animals have heightened HPA axis
reactivity and elevated parasympathetic reactivity.
The detailed ways in which stress influences reproduction
are still not well understood, but may involve a number of
endocrine, paracrine and neural systems (Rivier and Rivest,
1991; Tilbrook et al., 2000). Stress has an impact on the
 E. von Borell et al. / Hormones and Behavior 52 (2007) 130–138
reproductive axis at the hypothalamus (to affect GnRH
secretion) and the pituitary gland (to affect gonadotrophin
secretion) mainly via corticotrophin-releasing hormone (CRH),
arginine vasopressin (AVP) and opiates, with the direct effects
of ACTH and adrenal hormones on the gonads being less
important. High concentrations of cortisol suppress LH pulse
frequency by acting centrally to suppress pulsatile GnRH
secretion in follicular-phase ewes (Breen et al., 2005). The
reduction in endogenous GnRH/LH secretion ultimately
deprives ovarian follicles of adequate gonadotrophin support
leading to reduced oestradiol production by growing follicles
(Dobson and Smith, 2000). Responses to short and long-term
stressors may differ as short-term stressors often fail to affect
reproduction or even may have stimulatory effects (Liptrap and
Raeside, 1983). Thus, the stress response mediates diverse
responses to various stressors (environmental, physical, or
psychological) that can either increase or decrease the
probability of an animal reproducing depending on the specific
situation (Moore and Jessop, 2003). Control and perception of a
stressful situation may also depend on health, immune and
reproductive status. Besides individual and context specific
factors, sex steroids and species specific responses also need to
be considered, although HPA activation associated with a
reduced LH secretion during chronic stress has been reported
for most of the domestic animal species (Moberg, 1991). Recent
studies in rodents indicate that stress-induced suppression of
GnRH release is partly mediated by prostaglandins in the brain
and that glucocorticosteroids may even play a protective role in
maintaining the hypothalamic–pituitary–gonadal (HPG) activ-
ity during infectious stress by suppressing cyclooxygenenase-2
activity and, thus, prostaglandin synthesis (Matsuwaki et al.,
2006; Maeda and Tsukamura, 2006). Altogether, these
observations indicate that a variety of stressors and stress
pathways can impact directly or indirectly GnRH neurons to
influence the reproductive axis.
Implications of stress on the hormonal control of sexual and
maternal behaviours
The occurrence of sexual behaviour of the female depends
on variations of gonadal hormones oestradiol and progesterone.
Maternal behaviours also depend on a variety of sensory stimuli
but are mainly facilitated by three hormones: oestradiol,
progesterone and prolactin (Poindron, 2005). Nest-building in
sows specifically depends on progesterone (before parturition)
and prolactin (after parturition). Oxytocin release during
parturition seems to facilitate this process and induces maternal
behaviour and social bonding. Central (ICV) stimulation with
oxytocin elicits maternal behaviour (Kendrick et al., 1987);
however, there is some doubt on whether oxytocin is in general
essential for eliciting maternal behaviour after birth (Young et
al., 1997). Abundant scientific papers refer to the effects of
prenatal stress on sexual and maternal behaviours as reviewed
by Kaiser and Sachser (2005). Recent research in rodents
demonstrates that stress during gestation alters postpartum
maternal care at the neuroendocrine level and that the effects of
environmental adversity can be transmitted across generations
131
through a nongenomic (epigenetic) mechanism (Champagne
and Meaney, 2006).
The aim of the present review is to highlight the literature on
stress, behaviour and reproductive performance in female cattle
and pigs as phenomena reported in laboratory animals are
unable to explain all effects encountered in domesticated farm
animals.
Consequence of stress on reproductive performance in cows
Farmers use signs of oestrus in cows to determine the correct
time for artificial insemination, and there lies the importance of
understanding the factors that affect oestrus behaviour. There
are no bulls kept on many farms and the farmer must use refined
skills to detect oestrus in order to artificially inseminate (AI)
cows at the best time. It is essential that semen is deposited in
synchrony with oocyte release for optimum fertility. Stress leads
to reduced fertility by interfering with mechanisms controlling
both the intensity of oestrus behaviour and fertile oocyte
production (Dobson and Smith, 2000).
Immediate postpartum maternal behaviour is important for
the survival of the calf as calves on a typical dairy farm are
weaned within a few hours after birth as the milk is used for
human consumption. The onset of proceptive maternal
behaviour in cattle, including sniffing, licking, and protection
of the neonate, and formation of a selective maternal bond
fortunately requires only a few minutes to complete, and the
sensitive period during which the neural circuitry of the dam is
capable of responding to inductive stimuli lasting no more than
a few hours (Williams et al., 2001). There are reports that
multiparous dairy cows respond relative mildly to the removal
of their calves (Hopster et al., 1995). Indeed, during centuries of
domestication, less intense maternal behaviours have developed
in dairy breeds compared to typical beef breeds in which calves
are suckled for up to six months (Le Neindre, 1989).
Sexual behaviour and ovulation
In cattle, there is considerable variation within the literature
concerning the duration of oestrus behaviour: 0.2 to 12 h in
Lopez et al. (2002), 6–33 h in Lyimo et al. (2000) for example.
The time lag between the onset of ‘standing to be mounted’ and
ovulation is 24–38 h (range 18–60 h; Lopez et al., 2002; Walker
et al., 1996). The coincidental occurrence of oestrus and the
preovulatory LH surge is due to the fact that both phenomena
depend, at least in part, on similar regulatory mechanisms.
Currently there are few studies suggesting that some stressors
contribute to the above-mentioned large variations in the
duration of oestrus.
The stresses involved in maintaining a social structure
certainly influence sexual behaviour. Social dominance
reduces both the number of cows in oestrus at any one time,
and the duration of oestrus (review: Orihuela, 2000).
Dominant cows come into oestrus earlier after the decline in
progesterone values (16 versus 30–34 h) and display signs of
oestrus for longer (20 versus 12 h; Landaeta-Hernández et al.,
2004). However in another study, neither ‘dominance value’,
132 E. von Borell et al. / Hormones and Behavior 52 (2007) 130–138
nor antagonistic interaction, is associated with the number of
mounts received, nor the duration of oestrus (Kabuga et al.,
1992). As herd size increases, more cows exhibit abnormally
short ovarian cycles with the young inexperienced cows being
more susceptible, mainly because they are recipients of
aggression from more mature animals (review: Moberg, 1985).
Age probably combined with dominance also disrupts normal
signs of oestrus.
In cattle, the stress of elevated environmental temperature
reduces oestrus duration and intensity with smaller follicles
and lower oestradiol and progesterone concentrations (Wol-
fenson et al., 2000). Silent ovulations (unaccompanied by
oestrus) are more frequent during very hot times of year (26
versus 9%; Rodtian et al., 1996). However, it has also been
observed that the duration of oestrus is longer in summer than
in winter (17.6 versus 15.5 h) but with lower mounting activity
(43 versus 59 mounts; White et al., 2002). The optimum
temperature for displaying oestrus in cattle is 30 °C (Orihuela,
2000).
Undernutrition can be considered a metabolic stress. It may
influence oestrus and ovulation. Indeed, if animals treated for
anoestrus with progesterone (CIDR) did subsequently come
into oestrus, they had better body condition scores, greater
insulin-like growth factor concentrations and higher percentage
of milk proteins but lower β-hydroxybutyrate concentrations
than the cows not showing oestrus (McDougall and Compton,
2005). However, Lopez et al. (2004) reported that in one high-
producing herd (> 40 kg milk per day), oestrus is shorter than in
less productive herd mates (duration: 7 versus 11 h), and,
although the maximum follicular diameter is similar (∼18 mm),
plasma oestradiol concentrations are lower in high producing
animals (6.8 ± 0.5 versus 8.6 ± 0.5 pg/ml). It has been suggested
that the increased food consumption to produce this amount of
milk boosts liver blood flow which, in turn, enhances steroid
catabolism (Lopez et al., 2004). Furthermore, the time to the
first post-partum oestrus increases with increasing milk
production i.e., the interval from ovulation to oestrus is
30 days longer, and there is a higher incidence of ‘silent’
ovulations (Harrison et al., 1989).
As far as clinical conditions are concerned, lameness is
associated with even worse reproductive performance, as up to
40 days are lost to get lame cows in-calf again even though the
lameness has been treated (Collick et al., 1989). Luteal activity
and hence the onset of oestrus commences later in post-partum
cows treated for mastitis (8–4 days) or lameness (18 days;
Petersson et al., 2006). If cows have mastitis around the time of
the first ‘silent’ oestrus (15–28 days postpartum), commence-
ment of luteal activity and the onset of oestrus behaviour occur
later (39 versus 32 days and 91 versus 84 days, respectively;
Huszenicza et al., 2005). Furthermore, cows with mastitis have
smaller follicles than healthy herd-mates (GM Lloyd, pers.
comm.).
From early pharmacological studies, oestradiol has been
deemed important in the expression of oestrus. However, the
reduced intensity of oestrus observed in lame cows is not
associated with altered milk oestradiol profiles (Walker et al.,
2006). Once a threshold concentration of oestradiol has been
achieved, oestrus will be displayed (Allrich, 1993). Prevailing
progesterone concentrations are also crucial for the expression
of oestrus. The duration and quantity of prior exposure to
progesterone is important, with lame cows having lower
progesterone values for up to 9–12 days prior to oestrus of
lowered intensity (Walker et al., 2006). Furthermore, slight
elevations (suprabasal) of progesterone during the follicular
phase prolong oestrus (Duchens et al., 1994).
The emotional state of an animal can affect neuroendocrine
responses. Chronically stressed cattle, induced by 3 weeks of
isolation or deprivation of lying down, had similar baseline
cortisol and ACTH concentrations. However, these stressed
individuals had an excessive increase in cortisol when exposed
to a novel stimulus (Munksgaard and Simonsen, 1996).
Similarly, when lame cows are repeatedly exposed to a novel
stimulus, they do not habituate as readily as non-lame herd-
mates (Walker et al., 2006).
Very high doses of ACTH or cortisol delay the onset of the
LH surge and the onset of oestrus (Stoebel and Moberg, 1982;
Hein and Allrich, 1992) although the role of cortisol is con-
troversial. Indeed, Cook et al. (1987) were unable to influence
oestrus in ovariectomised progesterone-primed oestradiol-
treated cows with exogenous cortisol.
Fecundation, embryo and foetal development
Dobson and Smith (2000) ranked individuals in a dairy herd
at the start and end of the breeding period; those cows with a
high social status were more fertile (calving to conception: 97
versus 143 days; inseminations per pregnancy: 1.6 versus 2.2)
and had better milk production figures (+ 0.58 versus − 1.03 kg
milk/day; − 183 versus + 3713 somatic cells/ml milk).
Elevated environmental temperature severely reduces ferti-
lity in cows with pregnancy rates decreasing to as low as 10% in
environmental temperatures of 33 °C (Hansen and Arechiga,
1999). The stress of succumbing to clinical production diseases
also results in poor fertility. For example, the calving-to-
pregnancy interval is extended by 7, 8, 26 and 31 days in cows
treated for mastitis, retained foetal membranes, milk fever or
endometritis, respectively, compared to healthy herd-mates
(Borsberry and Dobson, 1989).
Previous positive handling and gentle interactions with
humans reduce stress reactions in cows, including a lower heart
rate and less restless behaviour during ovarian palpation per
rectum and sham artificial insemination (Waiblinger et al.,
2004). Moreover, the approachability of cows is correlated with
pregnancy rate to first AI (Hemsworth et al., 2000).
Maternal behaviour and young survival
The literature on the effects of stress on maternal behaviour
and young survival in cattle is scarce. Some studies have related
temperament (defined as fearfulness and reactivity of an animal
to humans and novel environments) to maternal abilities and
found that less fearful heifers tend to exhibit superior maternal
abilities and higher reproductive performance (Phocas et al.,
2006).
 E. von Borell et al. / Hormones and Behavior 52 (2007) 130–138
Consequence of stress on reproductive performance in
female pigs
Sexual and maternal behaviours are usually strongly re-
stricted in commercially farmed pigs. Indeed, female pigs are
often bred by artificial insemination and oestrus detection is
performed by the back-pressure test (females immobilise in a
rigid position in response to human hand pressure on the back)
in absence of the boar. Around parturition (farrowing) and
during lactation, sows are usually restrained from movement by
crates and do not have materials (grass, straw…) for nest
building. These farrowing crates have been developed to
facilitate human intervention during parturition and to reduce
death of piglets due to crushing by the mother (review:
Edwards, 2002). Such behavioural restriction may be a source
of stress. Reproductive pigs may encounter other types of
stressors: feed restriction in prepubertal or pregnant females,
extreme ambient temperatures, social restriction or instability. It
is commonly accepted that reproduction is impaired in those
pigs experiencing stress (reviews: Varley and Stedman, 1994;
von Borell, 1995; Einarsson et al., 1996) even though recent
reviews from Turner et al. (2002, 2005) have disputed this and
suggest that sows are resistant to the effects of single or repeated
acute stressors. We will focus on the influence of stressors with
a strong psychological component discarding the influence of
nutrition and ambient temperature that have been reviewed
elsewhere (temperature: Prunier et al., 1996; Farmer and
Prunier, 2002; nutrition: Foxcroft, 1998; Prunier and Quesnel,
2000).
Puberty attainment
Social and movement restriction due to tethering are
supposed to induce a chronic elevation in cortisol (Becker et
al., 1985; Barnett et al., 1985) but age at first ovulation and
ovulation rate at the second oestrus are similar in tethered and
group-penned females reared in isolation from the boar (Prunier
and Meunier-Salaun, 1989). However, when nulliparous young
sows (gilts) are submitted to daily boar contacts, first ovulation
is delayed in tethered compared to group-penned animals
(Jensen et al., 1970) probably because boar stimulation is
reduced (Prunier and Meunier-Salaun, 1989). Paterson and
Pearce (1989) showed unexpected better boar stimulation in
gilts that were supposed to be chronically stressed. Females
were submitted to brief electric shocks in order to induce fear of
humans but hypertrophy of the adrenal cortex did not occur as
expected. Hemsworth et al. (1986a) also failed to observe a
negative effect of an unpleasant treatment (electric shocks
whenever the pig approaches the experimenter) compared to a
pleasant one (gentle strokes whenever the pig approaches the
experimenter) on puberty attainment despite chronic elevation
in plasma cortisol.
Acute stress associated to transport, new environment, social
mixing with or without boar exposure induces puberty in
prepubertal females (Dumesnil du Buisson and Signoret, 1962;
Martinat et al., 1970). This complex stress response induces an
increase in plasma cortisol that continues for several hours but
133
its role in stimulating puberty is not well understood (Wodzicka-
Tomaszewska et al., 1985). The positive effect of cortisol on
basal secretion of LH as observed by Pearce et al. (1988) may
explain this stimulation. In contrast, numerous studies have
demonstrated that corticosteroids or ACTH inhibit the basal
secretion of LH (Fonda et al., 1984; Estienne et al., 1991;
Schneider et al., 2004) and the preovulatory LH surge (Barb et
al., 1982; Paterson et al., 1983; Turner et al., 1999). Direct
effects of corticosteroids on ovarian follicles may also occur as
some in vitro studies have shown negative effects (Danisova et
al., 1987), although others have demonstrated positive effects
such as increased secretion of androstenedione and oestradiol
by granulosa cells (Ryan et al., 1990).
Sexual behaviour and ovulation
When males and females can interact freely, their sexual
behaviour is very rich and complex. Prooestrus and oestrus last
for about 2 days with variations between females being higher
for prooestrus (0 to 12 days) than for oestrus (1 to 4 days)
(Sterning et al., 1998). Repeated observations of the ovaries by
ultrasonography show that ovulation usually occurs about two-
thirds into oestrus (Soede et al., 1992). Mating stimuli advance
the timing of ovulation and reduce the duration of ovulation
(Signoret et al., 1972).
Oestrus detection and/or mating may induce stress reactions.
Indeed, transfer of oestrus females to a mating pen followed by
boar exposure and mating is followed by an increase in plasma
cortisol higher than relocation alone (Barnett et al., 1982).
In dioestrus females, plasma cortisol 15 min after transient
relocation in a new pen and back-pressure is higher in the pre-
sence of a boar than when the pen is empty (Turner et al.,
1998a). However, repeated acute adrenal stimulation prior to
and during oestrus by boar exposure has no clear effect on
ovulation rate, length of oestrus cycle or sexual behaviour
during oestrus (Turner et al., 1998a,b). Similarly, brief elec-
troshocks are without effects (Hemsworth et al., 1986a).
In contrast, overcrowding (1 m2/gilt instead of 3 m2/gilt)
chronically increases plasma cortisol with a negative influence
on sexual behaviour as shown by an absence of detected oestrus
at the expected time in some cyclic gilts (Hemsworth et al.,
1986b). Relocation of mid-luteal gilts from outdoors to indoors
may delay oestrus and ovulation (Kraeling et al., 1982). When
comparing housing, Soede et al. (1997) observed a shorter
duration of oestrus in tethered than in individual loose-housed
sows, but similar ovulation rate and periovulatory patterns of
plasma LH, oestradiol-17β and progesterone. In this latter
study, tethering was accompanied by an increased level of
stereotypies suggesting that animals were experiencing chronic
stress but plasma cortisol was not modified.
Chronic elevation of corticosteroids after repeated intramus-
cular injections of ACTH or synthetic glucocorticoids at an
appropriate period during the oestrus cycle inhibits sexual
behaviour (Barb et al., 1982; Paterson et al., 1983; Turner et al.,
1999). In some of these studies, oestrus did not occur due to a
lack of preovulatory oestrogen increase whereas, in others,
oestrus was inhibited in oestrogen-treated ovariectomised
134 E. von Borell et al. / Hormones and Behavior 52 (2007) 130–138
females. Thus, corticosteroids may directly inhibit sexual
behaviour of females. In studies without an increase in
oestrogen, the preovulatory surge of LH is also absent. In
contrast, repeated acute elevation of cortisol by intravenous
injections of ACTH has no clear influence on preovulatory
surges of oestradiol and LH as well as on ovulation rate (Turner
et al., 1999; Brandt, 2006). A shorter oestrus was observed only
in one study (Brandt, 2006).
Fecundation, embryo and foetal development
Looking at stereotypic behaviours that are supposed to be
indicative of chronic stress, von Borell and Hurnik (1990)
observed that pregnant sows with stereotypies give birth to
fewer piglets born alive but litter weight at 3 weeks post-
partum (p.p.) is similar. Lower pregnancy rates also occur in
cyclic gilts submitted to repeated electric shocks (Hemsworth
et al., 1986a). On-farm observations reveal negative correla-
tions between the level of fear from humans and the number
of piglets born per sow and year (such criteria integrate effects
on fertility and prolificacy), farrowing rate or litter size at birth
(review: Hemsworth, 2003). If we accept that fear from
humans induces a state of chronic stress as suggested by
Hemsworth, this supports that stress has detrimental effects on
fertility. Alternatively, it can be assumed that a high level of
fear is associated to an impaired quality of management and
handling that have negative consequences on the efficiency of
oestrus detection and artificial insemination. Lower reproduc-
tive performance in female pigs with a high level of fear is not
always observed (Hemsworth et al., 1990). Intense noise due
to repeated explosive detonations (92 to 102 dB) and
construction work seems to induce infertility and abortions
in sows from a commercial herd (YongJun et al., 1999). This
could be due to stress since intense noise is aversive to pigs
and may stimulate the adrenal axis (Talling et al., 1998; Otten
et al., 2004).
In experimental situations, Soede et al. (1997) did not
observe any difference in the fertilization rate and the early
embryonic development in tethered or individual loose-housed
sows. Comparing housing systems for pregnant sows, McGlone
et al. (2004) concluded that tethering has more detrimental
effects than individual penning on the adrenal axis, stereotypies
and reproductive performance but overall effects are not very
profound.
Synthetic ACTH was injected intravenously in a pulsatile
manner for 48 h in order to mimic the effects of pituitary–
adrenal hormones on ovulation, fecundation and embryonic
development (Razdan et al., 2002, 2004a,b; Brandt et al., 2006a,
b). Starting the treatment a couple of hours before ovulation
increases progesterone before ovulation and tends to accelerate
the transport of semen and ovocytes/embryos but has no clear
effect on early embryo development (Brandt et al., 2006a,b).
Starting the treatment 6 h after ovulation seems to slow down
the early embryonic development, to decrease baseline levels of
prostaglandins but has no clear effect on progesterone after
ovulation or on the oviductal transport of embryos (Razdan et
al., 2004a). Treatment of sows on day 13 p.p. at the time of
embryo attachment has no clear effect on embryo survival and
development (Razdan et al., 2004a,b).
Whether stress applied to the pregnant sow impairs foetal
development has received some attention. Mendl et al. (1992)
observed high levels of salivary cortisol in pregnant sows with a
low rate of success in agonistic and avoidance interactions and,
those sows produced the lowest weight of piglets born alive,
suggesting a detrimental effect of chronic social stress on foetal
development. However, live weight at birth or at weaning is
similar in control piglets and in piglets born from sows
submitted to social mixing twice at 1-week intervals either
during mid or late gestation (Jarvis et al., 2006). Similarly, Otten
et al. (2001) did not observe any difference in live weight at
birth between control piglets and those piglets born from sows
submitted to a daily acute stressor (5 min of snaring) during the
last month of gestation.
Parturition, lactation and piglet survival
Parturition and early lactation are periods of profound
behavioural and physiological changes that are highly sensitive
to stressors. Since any factor influencing parturition and
maternal behaviour may have strong negative effects on piglet
survival, the influence of the environment on the adrenal axis of
periparturient female pigs has been thoroughly examined.
Detailed observations of maternal behaviour in domestic pigs
kept on commercial farms have shown that numerous elements
existing in semi-natural environments are still present. How-
ever, as animals are restrained in crates, nest-site seeking is
abolished, nest-building and maternal interactions with the
piglets are restricted, social integration of the offspring in the
group is also abolished and weaning is an abrupt rather than a
progressive process. Such behavioural restrictions may be a
source of frustration for the animals with consequences on
neuroendocrine pathways controlling parturition, colostrum and
milk production by the sow, and vitality of the piglets.
In tethered or crated sows, parturition lasts for a couple of
hours, lying is more frequent whereas nest-building related
activities are less frequent than before farrowing but some bouts
may still occur (Vestergaard and Hansen, 1984; Cronin et al.,
1993; Biensen et al., 1996). When sows change position during
parturition or shortly after they may crush their piglets. The
efficiency of farrowing crates to reduce death by crushing seems
to be related to the slowing of sow movements and to the
reduction in the amount of rolling from ventral to lateral
position that is more risky for the piglets than transitions
between standing, sitting and lying (Weary et al., 1996).
Prolonged duration of farrowing is associated with increased
risk of anoxia and intrapartum foetal death (Fraser et al., 1997).
Plasma cortisol and ACTH increase in sows around
parturition (Molokwu and Wagner, 1973; Baldwin and
Stabenfeldt, 1975; Jarvis et al., 1997, 2002). Plasma and
salivary cortisol start to increase around 12 h before farrowing
and remain elevated for about 24 h (Fig. 1). Just before
parturition, the increase in ACTH and cortisol is higher in sows
housed in crates without any bedding than in pens with straw
(Lawrence et al., 1994; Jarvis et al., 1998, 2001, 2002).
 E. von Borell et al. / Hormones and Behavior 52 (2007) 130–138
Fig. 1. Behavioural and hormonal (PRL: prolactin, Cort: cortisol) changes
observed in crated sows around farrowing (drawn from data of Meunier-Salaün
et al., 1991; Devillers et al., 2004).
Restriction in movement in crates seems to have a more
profound effect on cortisol and ACTH than the lack of nesting
material, gilts being able to redirect their nest-building
behaviour to floor exploration (Jarvis et al., 2002). Sows with
previous experience in a farrowing crate probably have a
diminished adrenal axis reaction to crating than gilts during
their first farrowing (Jarvis et al., 2001). During parturition
itself, housing has very little influence on plasma cortisol and
ACTH (Jarvis et al., 1998, 2001). Plasma prolactin, oxytocin
and β-endorphin also increase before farrowing and remain
elevated during parturition (Meunier-Salaün et al., 1991; Jarvis
et al., 1997, 2000, Fig. 1). However, expulsion of individual
piglets does not seem to influence plasma concentrations of
cortisol, ACTH nor β-endorphin during the 10 following
minutes (Jarvis et al., 1999). Peaks of oxytocin often occur
around birth of piglets but not always (Ellendorff et al., 1982;
Castren et al., 1993). Transferring parturient sows from their
farrowing pen to a crate in an adjacent room disrupts parturition
(Lawrence et al., 1992). An inhibition of oxytocin release
mediated by endogenous-opiate release is probably involved in
this disruption of parturition (Lawrence et al., 1992; Jarvis et al.,
2000). In agreement with that, lower basal and peak concentra-
tions of plasma oxytocin during farrowing occur in sows with
naturally prolonged parturition (Castren et al., 1993). Crating
the sows may result in longer duration of farrowing (Biensen et
al., 1996) but not always (Jarvis et al., 2000).
Environmental disturbance such as moving the sow and her
litter to a new pen leads to unsuccessful nursings (no milk
135
ejection) probably due to a lack of oxytocin release (Rushen et
al., 1995). Significant correlations between nursing behaviour
(piglets and sows), hormone release (prolactin, oxytocin,
insulin) and milk production (estimated from piglet growth)
occur (Algers et al., 1991; Valros et al., 2003) suggesting that
any stressful event that disturbs suckling behaviour may reduce
milk production.
In a series of studies in commercial herds, Hemsworth et al.
(1990, 1999) tried to relate the level of fear from humans to the
percentage of stillborns or death during lactation. No effect was
observed on stillborns in the first study. A significant correlation
between the percentage of stillborns and the level of fear occurs
when fear was evaluated 16–18 days p.p. (Hemsworth et al.,
1990) but not 2–4 days p.p. (Hemsworth et al., 1999).
Therefore, it is difficult to use these data to support the effect
of stressful situations on piglet survival. Intense noise during
pregnancy and farrowing is associated with an increase number
of stillborn (YongJun et al., 1999).
Otten et al. (2001) induced repeated acute stress and
observed that morbidity and mortality during the suckling
period are higher in piglets born to the stressed sows despite
similar growth rates. However, such negative effects of prenatal
stress were not observed by Jarvis et al. (2006) using social
stress during pregnancy.
Conclusion
Passing genes on to the next generation is extremely
important, but all species can temporarily suspend reproductive
activity if the situation becomes unfavourable (stress-induced
subfertility). Thus, if an animal is unable to cope (e.g., becomes
lame, experiences social problems or environmental stress), a
variety of mechanisms are activated to suppress reproductive
efficiency and maternal abilities as hypothalamic, pituitary and
ovarian function in stressed cattle and pigs may be compro-
mised. On the other hand, there are incidences where stress may
influence reproductive performance positively as shown by
early induced puberty in prepubertal female pigs. This poses
questions about the interpretation and context specific welfare
implications of these phenomena observed in domesticated farm
animals.
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