Maternal Behavior In Pigs

Hormones and Behavior 52 (2007) 78 – 85 www.elsevier.com/locate/yhbeh

Maternal behavior in pigs Bo Algers ⁎, Kerstin Uvnäs-Moberg Department of Animal Environment and Health, Swedish University of Agricultural Sciences, PO Box 234, 532 23 Skara, Sweden Received 27 March 2007; accepted 28 March 2007 Available online 1 April 2007

Abstract When sows kept under commercial conditions were put into crates in the early 1960s, the neuro-endocrine regulation of the maternal behavior in these domestic animals was disputed. Thus, the study of sow maternal behavior intensified and today a significant body of knowledge has accumulated to support the hormonal regulation of sow maternal behavior. The onset of nest building is associated with a periparturient decline in progesterone, an increase in prolactin and a major rise in plasma concentrations of PGF2α the day before parturition. Some nest building behaviors, such as pawing and gathering straw, have been found to correlate with changes in the levels of progesterone, prolactin and somatostatin. The duration of the birth process correlates negatively with peripheral oxytocin levels. During lactation, the stimuli from the piglets affect the release of several hormones which not only regulate the let down of milk but also sow metabolism and mammary milk production. The sow's nursing behavior ensures an even distribution of milk to her piglets. The piglets suckling behavior, in turn, is mainly a way to communicate their individual nutritional needs. © 2007 Elsevier Inc. All rights reserved. Keywords: Pigs; Sows; Maternal; Behavior; Hormones; Nursing; Suckling; Lactation; Metabolism; Communication

Introduction The nursing behavior of sows has attracted the interest of researchers since the 1950s. Much of this research was aimed at increasing the knowledge to better understand how piglets could be provided with milk from the sow in order to increase weight gain. The pig (Sus scrofa) is an omnivore living in groups of about 8–10 adult sows, some young individuals and, in the periphery, single males (Jensen, 1986). Under natural conditions, a day or so before the onset of parturition or farrowing, the sow separates herself from the group and seeks a suitable nest site with some shelter from rain and wind, well-drained soil and with possibilities to root a shallow hole in the ground (Grundlach, 1968; Frädrich, 1974; Jensen, 1986). Nest building occurs during the last 24 h before the onset of farrowing and is most intensive during 12 to 6 h before farrowing (e.g., Vestergaard and Hansen, 1984; Jensen, 1986). Nest building is performed in phases: first, the sow digs a shallow hole in the ground after which she gathers branches of bushes etc. and arranges them ⁎ Corresponding author. Fax: +46 511 67204. E-mail address: [email protected] (B. Algers). 0018-506X/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2007.03.022

along the edges of the nest. The nest building ends with the sow gathering softer material such as grass that she distributes throughout the nest by nodding head movements and pawing with front legs (Jensen, 1986). Thus, the nest can provide some comfort, thermoregulation and shelter for the piglets. Nest building can be divided into two distinct phases; an initial phase with rooting and pawing in the ground and a subsequent phase with collecting, carrying and arranging nest material (Jensen, 1993). Under commercial conditions the sow is usually bred at 7–8 moths of age, is pregnant for 133 days, and transferred to gestation and farrowing crates where she is kept individually without possibilities to turn around. This practice was suggested to reduce piglet mortality due to crushing by the sow. In some countries, gestating sows are instead kept in groups. The sows are moved to a facility where they give birth — a farrowing unit. This can either be equipped with farrowing crates where there is some space for the piglets outside the crate or the sow can be kept loose in a pen with a creep area for the piglets where they are protected from being crushed by the sow. Since the development of farrowing crates to house sows in confinement in the late 1950s, it has been argued that the modern pig does not necessarily build nests when approaching

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the time of farrowing due to a high degree of domestication and that it, therefore, does not need an environment which allows it to do so. However, increasing evidence has accumulated to challenge that assumption. Studies on nest building of domestic sows were first investigated under semi-natural conditions in the 1980s (Stolba and Wood Gush, 1989; Jensen, 1986; Algers and Jensen, 1990). They showed that, e.g., Swedish landrace sows, with experience from four prior farrowings in confinement crates, were perfectly able to locate suitable nest sites and to build farrowing nests, a behavior more or less identical with that of the wild boar (Gustafsson et al., 1999). Since then, the study of maternal behavior has intensified, such that, to date a significant body of knowledge has built on the hormonal regulation of sow maternal behavior. Nest building The onset of nest building is associated with a periparturient decline in progesterone from about 50 to 20 nmol/l and increase in prolactin (Ash and Heap, 1975; Taverne et al., 1978/1979; Widowski and Curtis, 1989; Meunier-Salaün et al., 1991; Castrén et al., 1993a). Prolactin concentrations are highly variable among sows on the day before farrowing and increase from about 15 ± 4 nmol/l (n = 10) 3 days before farrowing to reach maximum levels of about 72 ± 27 nmol/l (n = 10) at 8 to 12 h before the onset of parturition (Castrén et al., 1993a). A major rise in plasma concentrations of PGF2α on the day before parturition in sows has been demonstrated (Watts et al., 1988) and PGF2α metabolite (measured as 13,14-dihydro-15-ketoPGF2α) levels have been shown to increase from 1–2 nmol/l to about 50 nmol/l (Gilbert et al., 2002). An injection of prostaglandin (PGF2α) leads to an immediate increase in prolactin concentration and a rapid onset of nest building (Widowski et al., 1990). In contrast the prostaglandin analogue Cloprostenol led to a delayed increase in prolactin and delayed nest building which would suggest that it is the rise in prolactin, rather than the changes in prolactin concentrations that is important to trigger nest building behavior (Widowski et al., 1990). Indomethacin treatment specifically inhibits nest building in sows by a mechanism that may involve an inhibition of endogenous PGF2α synthesis, independently of circulating oxytocin, cortisol and progesterone levels. This points to a major role of PGF2α in prepartum nest building in the sow (Gilbert et al., 2000). Indeed, PGF2α given as a single dose to cyclic nulliparous sows (gilts) induces rooting, pawing at the ground and gathering straw, behaviors characteristic of nest building in the sow (Burne et al., 2000a). Pawing and gathering straw have been shown to be dependent on the dose of PGF2α (Burne et al., 2000a), pawing and duration of rooting are modulated by the provision of straw (Burne et al., 2000b) and rooting and lying are modulated by environmental temperature (Burne et al., 2001). Some nest building behaviors have been found to correlate with levels of specific hormones. Thus, the time spent carrying and depositing straw correlated significantly with prolactin (r = 0.65, n = 9, p = 0.05), tended to be positively correlated with progesterone (r = 0.60, n = 9, p = 0.08) and tended to correlate

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negatively with somatostatin concentrations (r = − 0.65, n = 9, p = 0.06). However, only progesterone and somatostatin were independently correlated with the time spent carrying straw (Castrén et al., 1993a). Damm et al. (2002) found a negative correlation between plasma oxytocin concentrations and nosing (r = − 0.8, p < 0.01) and arranging nest material (r = − 0.9, p < 0.001). Several factors may influence the motivational systems regulating nest building in the sow. The onset of nest building is suggested to be regulated by the increase in prolactin levels (e.g., Castrén et al., 1993a) although in sows that gave birth for the first time (i.e., gilts) there was either no increase or only moderate rise in prolactin levels (Lawrence et al., 1994). The authors suggested that with an increasing parity there is a closer temporal relationship between rise in prolactin and nest building. However, older parity sows tended to have a lower prolactin concentration 2 days before farrowing (Castrén et al., 1993a). The gathering of nest material appears to be regulated by external stimuli such as temperature or udder comfort, whereas a softer texture, such as abundance of grass, would inhibit further gathering of soft material (Algers and Jensen, 1990; Jensen, 1993). This is supported by the findings that changes in the sow farrowing environment had greater effects on the gathering of straw than on rooting and pawing behavior (Jensen, 1993; Arey et al., 1991) and that these behaviors are not correlated (Castrén et al., 1993a). In addition, the finding that the time spent carrying and depositing straw was independently correlated with high progesterone and low somatostatin concentrations 2 days before farrowing (Castrén et al., 1993a) suggests that not only sensory cues from the environment but also endocrine mechanisms take part in the control of these aspects of nest building behavior. Somatostatin is a gastrointestinal hormone which exerts inhibitory effects on gastrointestinal and metabolic functions. Somatostatin levels are under inhibitory vagal nerve control, i.e., somatostatin levels are decreased by vagal nerve activity. When vagal nerve activity is increased, as e.g. during lactation (Uvnäs-Moberg, 1994) somatostatin levels fall and consequently gastrointestinal and metabolic functions are enhanced leading to increased nutrient assimilation and growth (UvnäsMoberg, 1994) (for a more detailed description see paragraph on integration between maternal behavior, physiology and metabolism during lactation). The findings by Castrén et al. (1993a) indicate that somatostatin plays a role also in maternal behavior, decreasing from approximately 15 nmol/l on day 3 to 10 nmol/l 1 day before farrowing. It is, in fact, possible that the relationship between low levels of somatostatin and the time for carrying and depositing straw is a reflection of a variant of ingestive behavior occurring during nest building. The sows take nest building material into their mouths but instead of swallowing it they place the material in their nests. However, it cannot be ruled out that the presence of straw in the oral cavity per se leads to an activation of the vagal nerves and a consequent decrease of somatostatin levels. Estrogen levels (estradiol and estrone) remain low during the first half of pregnancy (< 100 pg/ml levels) but rise rapidly (2–

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4000 pg/ml) during the second half of pregnancy (K'nchev et al., 1975; Velle, 1976). No relationships between estradiol levels and nest building have been demonstrated although levels are extremely high in the periparturient period. Most of the production of estrogens occurs in the placenta and therefore estrogen levels drop abruptly after birth to reach the same levels as in the beginning of pregnancy. Estradiol and estrone levels remain low during location but increase slightly before estrus (Hultén et al., 2006). The cessation of nest building has been suggested to occur when udder comfort is sufficient (Baxter, 1983). The provision of a preconstructed nest led to a quicker cessation of nest building but straw carrying was not eliminated: instead there was an increase in the amount of rooting behavior (Arey et al., 1991). In contrast, the removal of nest material every 4th h until parturition has been shown to increase plasma cortisol and heart rate in gilts in comparison to sham removal whereas plasma oxytocin was unaffected by such a procedure indicating a more complex regulation of oxytocin release (Damm et al., 2003). However, moving sows in early parturition from a crate to a pen has been shown to decrease oxytocin concentrations (Lawrence et al., 1992). Nest building stops at about 4 h before the onset of parturition and a dramatic elevation of oxytocin levels starts at about 6 h before the onset of parturition, a change that seemed to end the nest building phase (Castrén et al., 1993a). At that time, uterine contractions increase in frequency (Taverne et al., 1979). Electric activity of the uterine muscles coincides with oxytocin release (Forsling et al., 1979) and spontaneous contractions occur only when oxytocin concentrations are elevated (Taverne et al., 1979). Sows with high oxytocin concentrations 8 h prepartum stopped nest building earlier than other sows (Castrén et al., 1993a). Whether the peripheral effect of oxytocin in generating uterine contractions is the cause of the cessation of nest building or whether oxytocin acts to stop nest building at a central level remains to be investigated. A direct effect on the central nervous system as a result of the increase in oxytocin release cannot be ruled out. In summary, it can be concluded that there is strong evidence to suggest that the onset of nest building in sows is triggered by a rise in prolactin levels, which is itself related to decreased progesterone and increased prostaglandin concentrations. Further, some nest building activities such as carrying and depositing straw seem to be related to changes in somatostatin and progesterone levels. Nest building ends when oxytocin levels begin to rise. Farrowing Farrowing involves the expulsion of fetuses which takes place when the sow lays down in the farrowing nest. It has been suggested that oxytocin release is of importance for effective contractions of the uterus and rapid birth of the piglets (Forsling et al., 1979; Taverne et al., 1979; Lawrence et al., 1997; Gilbert et al., 2000). Sows give birth to 4–7 offspring (wild boar) (Harris et al., 2001) and, under commercial conditions, typically

to 10–12 (domestic sow, van Dijk et al., 2005). The duration of parturition is 166 min (26–505) with some variability (130–245 min) among strains (van Dijk et al., 2005). During farrowing, oxytocin plasma baseline concentrations are elevated and oxytocin is further released in a pulsatile pattern (e.g., Forsling et al., 1979). Baseline levels of oxytocin before farrowing are around 5–6 fmol/l, increasing to about 10 fmol/l just before farrowing and to 45 fmol/l at 3 h after the start of farrowing, whereafter it decreases to approximately 5 fmol/l (Castrén et al., 1993b). Research on several species such as miniature pigs, rabbits, rats, goats, and horses (Forsling et al., 1979; Haldar, 1970; McNeilly et al., 1972; Allen et al., 1973; Higuchi et al., 1986) suggests that the expulsion of each fetus is related to a peak release of oxytocin. Studying pigs and the pulsatile release of oxytocin in detail, however, Castrén et al. (1993b) were unable to relate the expulsion of fetuses to a peak release of oxytocin. Only about 50% of piglets were born during an oxytocin peak and the first piglets in the litter were born at much lower oxytocin levels than those born later when increased oxytocin peaks were observed. It may well be that the vaginal distension, occurring as a result of the first pigs being born may, in turn, increase the circulating levels of oxytocin as suggested by Ellendorff et al. (1979). The release of oxytocin during farrowing in sows may also be stimulated by the udder massage performed by already born littermates since it has been shown that udder stimulation during established lactation causes release of oxytocin (e.g., Algers et al., 1990). Moreover, as oxytocin also is released into the brain, it stimulates its own release (Hatton and Tweedle, 1982; Theodosis, 2002). This positive feed back may explain the increase of oxytocin over time during farrowing. Cortisol concentrations rise at farrowing (Taverne et al., 1979; Lawrence et al., 1994, 1997; Jarvis et al., 1998), probably as a result of physical strain or as a response to a psychological factor(s). A short duration of the farrowing process is of importance for piglet survival and a delay can result in anoxia or stillbirth (Randall, 1972; Bille et al., 1974). Low oxytocin levels may cause a prolongation of the farrowing time (Castrén et al., 1993b) and a negative correlation between plasma oxytocin levels and duration of parturition (r = − 0.7, p < 0.01) has been shown (Damm et al., 2002). Parturition is prolonged in rats if oxytocin secretion is inhibited by opioids (Russell et al., 1989) and an environmental disturbance could cause the same effect in pigs (Lawrence et al., 1992). Sows with long farrowing times had lower basal as well as lower peak levels of oxytocin during farrowing in comparison to sows with short farrowing times (Castrén et al., 1993b). However, in that study, long farrowing times could not be predicted from prepartum oxytocin, prolactin, progesterone or somatostatin levels or from the prepartum behavior of the sows. Lactation The sow is rather unique in that she gives birth to a large number of behaviorally well-developed young. Each piglet is

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very capable suckling on its own, but for the fitness of the sow it is important to distribute her bodily resources through milk to all of her piglets. Therefore, an array of different behavioral elements has evolved allowing for the piglets to communicate their needs of energy and the sow to distribute her resources evenly to all her piglets (Algers, 1993). Unlike cows, sows have no teat cisternae, which is why a piglet cannot obtain milk without there being an increase in the intramammary pressure mediated by oxytocin release. The increase in pressure lasts for approximately 15 s. Piglets are called to the udder by the sow milk grunt (Castrén et al., 1989) and the increase in grunting frequency causes the piglets to switch from massaging behavior to sucking on a teat (Algers and Jensen, 1985).

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is triggered by a release of oxytocin from the posterior pituitary (Folley and Knaggs, 1966; Ellendorff et al., 1982). As the sow does not have a teat cistern, milk is only available during milk ejection, which is stimulated by the piglets massaging each udder segment (Whittemore and Fraser, 1974) for 1–3 min (Fraser, 1980; Algers and Jensen, 1985; Algers et al., 1991). In most mammals, such as humans and cattle, this period is much shorter and milk ejection can be conditioned by other stimuli that do not involve mechanical stimulation of the udder (Schmidt, 1971). Fraser (1980) suggested that the function of the pre let-down phase is an adaptation that ensures all the members of a large litter are present at nursing. Indeed, when fewer piglets are massaging the udder, it takes longer for oxytocin release to occur (Algers et al., 1990).

Early lactation The first milk ejections can appear even before farrowing is complete. Although it has been suggested that during the first hours, colostrum would be available continuously (Lewis and Hurnik, 1986), a further release of colostrum release requires a discrete release of oxytocin (Fraser, 1984). Basal levels of oxytocin increase during 7–8 h after the onset of farrowing to about 45 fmol/l (Castrén et al., 1993b). Some, but not all, of the early milk ejections are associated with a pulsatile oxytocin secretion with peaks reaching about 100 and sometimes 200 fmol/l. During the first 8 h, discrete milk ejections appear at shorter intervals and with a higher variability, 5–40 min., than during established lactation, when they approach 1 milk ejection per hour (Fraser, 1984; Castrén et al., 1993b; Fraser and Rushen, 1992). Piglets compete with their littermates for access to teats during the first day but gradually the suckling rhythm synchronizes within the litter and a “teat order” is established (McBride, 1963; Hemsworth et al., 1976; Lewis and Hurnik, 1985; De Passillé and Rushen, 1989). The sow recognizes her own piglets by olfactory cues (Frädrich, 1974) and she is often aggressive towards intruding piglets although cross suckling occurs frequently in the domestic pig (Newberry and WoodGush, 1986). Established lactation Initiation Either the piglets initiate the nursing by approaching the sow's udder and emitting a “high/deep grunt” (Jensen and Algers, 1984) or, as is more common during the first week, the sow lays down, exposes her udder and emits a typical nursing grunt (Algers and Jensen, 1985; Jensen et al., 1991). The sound of the sow grunting attracts the piglet to the udder (Jeppesen, 1982; Castrén et al., 1989) which ensures that all piglets, each having the capacity to produce a let down, assemble at the udder to be prepared for the short time that milk is available to them. Pre let down When lactation is established, let down and suckling occur at regular intervals of 45–60 min when all piglets in the litter suckle at the same time (Barber et al., 1955; Fraser, 1977). This

Let-down phase The grunting of the sow increases in frequency just before let down which Fraser (1980) suggested to be a signal for the piglets to change from massaging the udder segment to sucking on the teat. If high-level fan noise is used to mask the vocal signals from the sow in early lactation (days 1–3), suckling behavior is much less synchronized and the time when piglets switch from massaging to sucking is more variable, which results in less milk ingestion by the piglets (Algers and Jensen, 1985). The fast grunting starts at about 23–25 s before the rise of the intramammary pressure (Ellendorff et al., 1982; Fraser, 1975). There is an increase of oxytocin in the blood starting at about 15 s after the increase of the grunt rate (Algers et al., 1990). A latency of 15 to 25 s for the released oxytocin to reach the udder can be expected (Whittlestone, 1953, 1954a,b), which may be why it is the sharp increase, rather than the peak of the grunt rate that seems to occur simultaneously with oxytocin release (Algers, 1989). Ellendorff et al. (1982) suggested that oxytocin facilitates grunting. Oxytocinergic fibers, which originate in the paraventricular nucleus, project to the dorsal and dorsomedial vagal nucleus (Swanson and Sawchenko, 1980) which also innervates larynx. It could be hypothesized that there is a facilitatory effect of oxytocin on grunting mediated either by the activation of oxytocinergic fibers or by an increase of oxytocin in plasma. It has been shown that the peak grunt rate level is influenced by the time and number of piglets massaging but no such effects could be demonstrated in response to the integrated grunt rate response (Algers et al., 1990). Thus, the volume of grunting seems to be rather constant but distributed differently depending on the number of piglets stimulating. Post let down After the milk is consumed, pigs resume massaging the udder of the sow, an activity that can go on for several minutes. The longer time spent by the litter massaging the udder, the more milk was produced by the sow (Gill and Thomson, 1956). Indeed, piglets showed a decrease in weight gain following periods where the post let-down massage was prevented experimentally (Barber et al., 1955). As piglets keep to their “own” udder segment through lactation, Algers and Jensen (1985) presented the so-called “restaurant hypothesis” postu-

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lating that the piglets in a litter individually “order” the size of their future meals by performing more or less post let-down massage onto their “own” udder segment. The idea was that the final massage acts as a regulator of sow milk production which allows her to adjust this parameter to the number of vital piglets suckling. Tactile stimulation and hormonal release Several studies have shown that piglet udder massage results in the release of prolactin (e.g., van Landeghem and van de Wiel, 1978; Algers et al., 1991) which reaches its highest concentrations in plasma 10–20 min after nursing (Einarsson et al., 1992; Rojkittikhun et al., 1993b; Spinka et al., 1997). An increase in plasma prolactin concentration is associated with an increase in lactational performance of the sow (Smith and Wagner, 1980). Prolactin increases the number of insulin receptors in the mammary gland (Uvnäs-Moberg, 1989) and decreases these receptors in maternal fat stores. This directs energy to the mammary glands rather than to fat deposits, thereby promoting lactation. Daily ergocryptine treatment of sows 2 days before estimated farrowing date significantly reduced mean plasma levels of prolactin before and after farrowing, resulting in an absence of milk production (Whitacre and Threlfall, 1981). Bromocriptine treatment of sows from day 25 of lactation until weaning 9–17 days later suppressed prolactin serum levels but did not affect piglet weight gains until 6 weeks after birth (Benjaminsen, 1981). Further, a similar treatment for 5 days, starting on day 21 in lactation did not affect litter body weight (Mattiolo and Seren, 1985) indicating that prolactin seems to be most important for milk production in the early stages of lactation. Integration between behavior, physiology and metabolism during lactation In addition to releasing oxytocin and prolactin, piglet udder stimulation promotes the release of several gut hormones such as gastrin, somatostatin and vasoactive intestinal polypeptide (VIP) and of pancreatic hormones such as insulin and glucagon in several species including pigs (Lindén et al., 1987; UvnäsMoberg et al., 1984; Algers et al., 1991). The suckling/massage-

related release of hormones is due to an activation of the vagal nerves. These hormones play an important role in adapting maternal physiology and metabolism to the demands of lactation. The release of gastrin during nursing leads to growth of the intestinal mucosa (Lankisch, 1980). This release is facilitated by the vagally induced decrease of somatostatin levels, since this hormone inhibits gastrointestinal functions (Efendic et al., 1980). Thus the digestive tract adapts to a larger feed intake and the digestive processes are optimized to meet the increased need of energy during lactation. VIP is produced in the gastrointestinal tract and in blood vessels of the udder. Since VIP acts locally to dilate blood vessels it helps allocate nutrient and hormone-rich blood to the udder. In addition, udder skin temperature is increased as a consequence of the increased blood flow. Stimulation of an udder segment increases the skin temperature at the base of this segment by more than 0.5 °C in comparison to the unstimulated udder segments (Welch and Baxter, 1986; Algers, 1989). The higher temperature caused by the increased blood flow may also serve to increase sucking behavior. The massage/suckling-induced release of insulin and glucagon may serve to facilitate metabolic processes and transfer of nutrients from maternal stores to the mammary gland. Glucagon seems to be of particular importance as a catabolic agent during lactation, since the activity of the hypothalamic–pituitary–adrenal axis and the sympatho-adrenal system, normally associated with catabolic processes, is partially repressed during lactation (Uvnäs-Moberg, 1996). The finding of a quantitative relation between teat stimulation and the release of prolactin, glucagon, VIP and (inverted) somatostatin reported by Algers et al. (1991) supports the concept of the restaurant hypothesis. Measuring the duration and intensity of teat stimulation of each piglet on each udder segment showed that both of these parameters influenced the milk production during the first 3 days of lactation (Algers and Jensen, 1991). Further, nursing frequency is shown to influence piglet weight gain (Spinka et al., 1997; Auldist et al., 2000; Valros et al., 2002). Valros et al. (2002) found that the duration (200–250 min/day) and frequency (20–24 times/day) of nursing was rather stable for

Table 1 Hormonal regulation of specific maternal behavior activities

Estradiol Oxytocin Prolactin Progesteron PGF2α Somatostatin Glucagon Insulin Gastrin

Initiation of nest building

Nest building

Termination of nest building

Initiation of farrowing

Farrowing

Lactation, nursing

Lactation, not during nursing

+? 0 + + + 0

+? 0 + +

+? + 0 0

+? + 0 0

+? + 0 0

0 + + 0

0 0 0 0

+

0

+ + + +

+ +

+ = Significant activity, 0 = no activity.

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each sow throughout lactation indicating the existence of a stable individual nursing behavior pattern. This is probably due to the amount of bodily resources that the sow can access. Under commercial conditions, weaning usually takes place when the piglets are 3–6 weeks of age depending on the management practices applied, but under natural conditions weaning is gradual and finishes at 14–20 weeks after birth (Jensen and Recén, 1989). Maternal metabolism during lactation To allow for an increased energy demand during milk production, the sow mobilizes her body reserves (see Quesnel and Prunier, 1995). After parturition, the sow has to switch from an anabolic to a catabolic state which prioritizes the mammary gland energy output (Collier et al., 1984). This, of course, is also related to feeding level and quantity of milk output, but individual variations have been reported (Rojkittikhun et al., 1993b). Peak milk production occurs at 2–3 weeks post partum (Toner et al., 1996) when blood glucose levels are low due to milk production (Rojkittikhun et al., 1993a; Kraetzl et al., 1998). Measuring body weight loss, however, Hultén et al. (1993) found a peak during the first week of lactation but Rojkittikhun et al. (1993a) were unable to demonstrate a correlation between prefeeding glucose levels and body weight loss in the sow. However, sows are normally fed diets rich in starch which is why glucose levels usually do not reach low values (Kraetzl et al., 1998). As non-esterified fatty acids (NEFA) are a product of fat metabolism and only small amounts of them can be derived from feed intake, they can be used as a sign of catabolic state (Armstrong et al., 1986; Baidoo et al., 1992; Hultén et al., 1993). NEFA levels in sows rise at the end of gestation and are highest during mid- and late lactation (Kraetzl et al., 1998) although studies are inconsistent (see e.g. Hultén et al., 1993; Rojkittikhun et al., 1993b; Le Cozler et al., 1998). Valros et al. (2003) found that sows differ in their metabolic state and milk production. Sows with low piglet mortality were found to switch to a catabolic state early in lactation in comparison to those with high mortality and low litter weight gain, in which high NEFA concentrations were found in the third week, when the demand for milk production is at its maximum. Further, it was shown that high baseline plasma oxytocin concentrations as well as a high nursing-induced release of oxytocin were associated with greater mobilization of bodily reserves of the sow and faster piglet growth (Valros et al., 2004). Interestingly, the milk ejecting hormone oxytocin has been shown to stimulate several aspects of maternal behavior such as caring behavior and bonding in several mammalian species (for review, see Lim and Young, 2006). Oxytocin also adapts maternal physiology and metabolism to the demands of lactation. These effects are exerted in the brain and are caused by a release of oxytocin from oxytocinergic neurons originating in the paraventricular nucleus of the hypothalamus. In sows the oxytocin-related increase in grunt rate occurring before milk ejection is an expression of the oxytocin-related maternal behavior. An oxytocin mediated increased secretion of VIP from blood vessels in the udder, may dilate blood vessels in

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the udder, thus increasing udder temperature and also facilitating transportation of oxygen and nutrients to the mammary glands. In addition, the vagally mediated increased activity of the gastrointestinal tract as well as the increased release of glucagon and increased catabolic activity are expressions of oxytocin-mediated effects aiming at integrating maternal behavior, physiology and metabolism in the lactating sow. The relations between the individual sow, its genetic background and capacity to release hormones that influence metabolism and milk output is complex and not completely understood. Moreover, additional research is needed to better understand all aspects of maternal behavior in pigs. Conclusions This review shows that much of the maternal behavior in sows is governed by the release of specific hormones (see Table 1), but mechanisms seem complex and most likely involve many other nervous and hormonal systems. The sow's nursing behavior ensures an even distribution of milk to her piglets. The piglets' suckling behavior, however, is mainly a way to communicate their individual nutritional needs. This communication is mediated through tactile stimulation of hormonal release. References Algers, B., 1989. Vocal and tactile communication during suckling in pigs. Aspects on functions and effects of continuous noise. Doctoral thesis. Swed. Univ. Agric. Sci., Dept. of Anim. Hyg. Report 25. Algers, B., 1993. Nursing in pigs: communicating needs and distributing resources. J. Anim. Sci. 71, 2826–2831. Algers, B., Jensen, P., 1985. Communication during suckling in the domestic pig. Effects of continuous noise. Appl. Anim. Behav. Sci. 14, 49–61. Algers, B., Jensen, P., 1990. Thermal microclimate in winter farrowing nests of free-ranging domestic pigs. Livest. Prod. Sci. 25, 177–181. Algers, B., Jensen, P., 1991. Teat stimulation and milk production during early lactation in sows: effects of continuous noise. Can. J. Anim. Sci. 71, 51–60. Algers, B., Rojanasthien, S., Uvnäs-Moberg, K., 1990. The relation between teat stimulation, oxytocin release and grunting in the sow. Appl. Anim. Behav. Sci. 26, 267–276. Algers, B., Madej, A., Rojanasthien, S., Uvnäs-Moberg, K., 1991. Quantitative relationships between suckling-induced teat stimulation and the release of prolactin, gastrin, somatostatin, insulin, glucagon and VIP in sows. Vet. Res. Commun. 15, 395–407. Allen, W., Chard, T., Forsling, M., 1973. Peripheral plasma levels of oxytocin and vasopressin in the mare during parturition. J. Endocrinol. 57, 175–176. Arey, D.S., Petchey, A.M., Fowler, V.R., 1991. The preparturient behaviour of sows in enriched pens and the effect of pre-formed nests. Appl. Anim. Behav. Sci. 31, 61–68. Armstrong, J.D., Britt, J.H., Kraeling, R.R., 1986. Effect of restriction of energy during lactation on body condition, energy metabolism, endocrine changes and reproductive performance in primiparous sows. J. Anim. Sci. 63, 1915–1925. Ash, R., Heap, R., 1975. Oestrogen, progesterone and corticosteroid concentrations in peripheral plasma of sows during pregnancy, parturition, lactation and after weaning. J. Endocr. 64, 141–154. Auldist, D.E., Carlson, D., Morrish, L., Wakeford, C.M., King, R.H., 2000. The influence of suckling interval on milk production of sows. J. Anim. Sci. 78, 2026–2031. Baidoo, S.K., Lythgoe, E.S., Kirkwood, R.N., Aherne, F.X., Foxcroft, G.R., 1992. Effect of lactation feed intake on endocrine status and metabolic levels in sows. Can. J. Anim. Sci. 72, 799–807.

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