Stress, Behaviour And Reproductive Performance In Female Cattle And Pigs

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 coordinated response to the challenge. This response may be behavioural, autonomic, neuroendocrine and/or immunological.

⁎ Corresponding author. Fax: +49 345 5527106. E-mail address: [email protected] (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 longerterm, sustained response with the involvement of major adrenal cortical hormones such as glucocorticoids and mineralocorticoids. 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 concentrations 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

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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) activity 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.

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.

Implications of stress on the hormonal control of sexual and maternal behaviours

Sexual behaviour and ovulation

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

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).

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’,

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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 (Wolfenson 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 highproducing 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), commencement 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 herdmates (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 controversial. Indeed, Cook et al. (1987) were unable to influence oestrus in ovariectomised progesterone-primed oestradioltreated 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 fertility 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-topregnancy 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).

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Consequence of stress on reproductive performance in female pigs Sexual and maternal behaviours are usually strongly restricted 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

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its role in stimulating puberty is not well understood (WodzickaTomaszewska 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 twothirds 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 presence 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 electroshocks 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 intramuscular 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

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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 postpartum (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 correlations 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 reproductive 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. However, 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).

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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. 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 concentrations 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

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 compromised. 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. References Algers, B., Madej, A., Rojanasthien, S., Uvnas-Moberg, K., 1991. Quantitative relationships between suckling-induced teat stimulation and the release of prolactin, gastrin, somatostatin, insulin, glucagon and vasoactive intestinal polypeptide in sows. Vet. Res. Commun. 15, 395–407. Allrich, R.D., 1993. Estrous behavior and detection in cattle. Vet. Clin. North Am., Food Anim. Pract. 9, 249–262. Baldwin, D.M., Stabenfeldt, G.H., 1975. Endocrine changes in the pig during late pregnancy, parturition and lactation. Biol. Reprod. 12, 508–515. Barb, C.R., Kraeling, R.R., Rampacek, G.B., Fonda, E.S., Kiser, T.E., 1982. Inhibition of ovulation and LH secretion in the gilt after treatment with ACTH or hydrocortisone. J. Reprod. Fertil. 64, 85–92. Barnett, J.L., Hemsworth, P.H., Cronin, G.M., 1982. The effect of mating on plasma corticosteroids in the female pig and the influence of individual and group penning on this response. Gen. Comp. Endocrinol. 47, 516–521. Barnett, J.L., Winfield, C.G., Cronin, G.M., Hemsworth, P.H., Dewar, A.M.,

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