13. Nursing behavior

The gestating and lactating sow

edited by:

Chantai Farmer

Wageningen Academic

P u b l i s h e r s

EAN: 9789086862535 e-EAN: 9789086868032

ISBN: 978-90-8686-253-5 e-ISBN: 978-90-8686-803-2

DOI: 10.3920/978-90-8686-803-2

Photo cover: Joël Boudreau

First published, 2015

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13. Nursing behavior

M. Šp inka* and G. Illm annInstitu te o f A n im a l Science, D epartm ent o f Ethology, Pratelstvi 815, 104 00 Prague Uhrineves, Czech Republic; spinka.m arek@ vuzv.cz

Abstract

Nursing behavior in domestic pigs differs between the colostral period and later lactation. D uring the initial period of colostrum production, the sow passively exposes her udder and thus gives new born piglets the opportunity to freely harvest colostrum by moving from teat to teat. Nursing behavior in swine is particularly complex because of specific features including nursing synchronization, non-nutritive nursings, the potential for allo-suckling, ontogenetic shifts in nursing initiation and term ination, and the balance between the sow-litter and piglet-piglet cooperation and conflict. Acoustic, olfactory and tactile com m unication play pivotal role in the nursing interactions. The physiological control m echanism s of m ilk production and milk ejection determ ine many aspects of nursing behavior but, on the other hand, nursing behavior has a strong feedback influence on physiology, including the horm onal state, o f the lactating sow. The functional view on nursing behavior, based on the evolutionary theory-inspired question ‘what survival/ reproduction benefit does the behavior bring to the anim al?’ can provide im portan t insights into the links between different features of nursing behavior.

Keywords: suckling, m ilk intake, vocalization, m aternal behavior, weaning

13.1 Introduction

N ursing behavior in domestic pigs is among the m ost complex of the nursing interactions described in mammals (Fraser, 1980; Špinka et a l , 2002). Indeed, pig nursing interactions contain several unique features, including high nursing frequency, very brief milk ejection, regular non-nutritive nursings and richly structured tactile and vocal com m unication between the m other sow and the piglets. The current chapter reviews the m echanism s and functions of the interactions between sows and piglets during nursings and focuses on the changes in nursing behavior taking place during the course of lactation.

Nursing interactions occurring during the first day after parturition differ behaviorally and physiologically from later nursing behavior. Early nursing interactions also have the specific function of providing colostrum , starting the process of teat order establishm ent am ong the piglets, and securing - or not - the survival o f the individual piglets. This brief but dynamic early period is therefore treated separately in the first section of this chapter. The second part is devoted to the fully established nursing pattern that commercially- kept dom estic sows m aintain from the tim e when cyclic nursing is established, at the end of the first postpartum day, until the (artificially im posed) end of lactation at 3-6 weeks

C hantai Farmer (ed.) The gesta tin g an d lacta tin g sow 2 9 7

D O I 10.3920/978-90-8686-803-2_13, © W ageningen Academ ic Publishers 2015

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M. Špinka and G. Illm ann

postpartum . Nevertheless, this nursing pattern changes gradually from the second week onwards as sows tend to restrict their nursing investm ent into the litter, and this process of gradual weaning’ is the topic of the th ird part of this chapter.

13.2 Nursing during the postpartum period

13.2.1 Peri-parturient changes in sow activity

Domestic sows are not particularly active m others during the parturition itself and the early postpartum hours. After the conspicuous prepartum nest building activity (Jensen, 1986; Thodberg et al, 1999), sows calm down as parturition approaches. D uring the parturition , sows generally lie im m obile and rather unreactive in lateral recum bency (Jarvis et al, 1999; Jensen, 1986; Thodberg et al, 1999), although in the initial stage of parturition posture changes may be m ore frequent than in the later stages (Jarvis et al, 1999; Thodberg et al, 1999). Through the lasting lateral recumbency, sows expose the udder for ‘teat sam pling’ by the piglets, as described below. Sometimes, sows rise to sniff the first few piglets as they are born (Jensen, 1986). A new increase in activity coincides w ith an increase of m aternal responsiveness to naso-nasal contacts around 10 h postpartum (Pedersen et al, 2003). D uring such contacts the sow responds by sniffing w hen a piglet approaches her snout (Illm ann et al, 2001; Jensen, 1988).

13.2.2 Early colostrum availability and m ilk ejections

D uring parturition , colostrum (early m ilk rich in energy and im m unoglobulins) is available almost continuously, as supported by high oxytocin concentrations (Devillers et al, 2007; Farmer and Quesnel, 2009). However, individual discrete ejections of colostrum are already occuring during partu rition (Castrén et al, 1993; de Passillé and Rushen, 1989; Fraser and Rushen, 1992; Rushen and Fraser, 1989). Gradually, m ore and m ore of the colostrum becomes available in cyclic discrete ejections caused by pulsatile oxytocin bursts separated by periods with little or no release of colostrum . At 5 h after the onset of birth , these ejections are brief and frequent, occurring at irregular intervals about three times per hour (Castrén et al, 1989b; Fraser, 1984). Then they decline in frequency and from about 8-11 h after the start of farrowing, milk is available only during discrete ejections occurring at the stable rate of approximately 1.5 per hour. These ejections occur spontaneously, w ithout the need of piglet teat massaging. As of 12-16 h postpartum , the piglets start to include teat massaging (rubbing the vicinity of teats with their snouts) into their suckling behavior, and the m ilk ejections gradually become dependent on the tactile stim ulation of the udder by piglets.

Teat sampling by piglets and transition to synchronized sucklings

New born piglets struggle to their feet w ithin one or two m inutes, and move to the udder mainly by staying in contact with the vertical surface of the recum bent sow. Once a piglet has suckled a teat, it moves along the udder sampling from different teats and biting or pushing littermates to obtain other teats (de Passillé and Rushen, 1989). This teat sampling

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13. N ursing behav io r

behavior lasts for about the first 8 h postpartum (de Passillé et al, 1988a; Graves, 1984). D uring this period, each piglet suckles on the average 7 different teats and there is no preference for anterior teats. Piglets that suckle m ore teats during the first 8 h have greater im m unoglobulin levels (de Passillé et al, 1988b). D uring teat sampling, piglets have their individual suckling rhythm s as each o f them is active for 2-3 h after birth , then falls asleep, and resumes activity later (Castrén et al, 1989b). The teat sampling by individual piglets gradually transform s into synchronized suckling bouts over the first 12 postnatal hours (de Passillé and Rushen, 1989). Already during parturition, there is a certain degree of synchrony in suckling and in weight gains by piglets (de Passillé and Rushen, 1989; Fraser and Rushen, 1992; Rushen and Fraser, 1989). However, these early suckling bouts occur at short intervals and tend to involve few piglets. At 10 h postpartum , m ilk intake occurs during cyclical suckling bouts; however, less than half o f the litter is present in these bouts (de Passillé and Rushen, 1989). By day 1 postpartum , 85% of piglets take part, on average, in each suckling and complete suckling synchronization of 100% is achieved on day 3.

13.2.3 Early nursing vocalizations by the sow

Post-parturient sows em it deep rhythm ic grunts w hen they lie in the lateral nursing position. Peaks in grunting are present already from the onset of farrowing. D uring the first 5 h postpartum , the peaks become m ore frequent and are related to m ilk ejections. However, piglets suck the teats also when grunting rate is low (Castrén et al, 1989b), so it seems that the grunting might mainly attract the piglets to the udder in this period rather than signal m ilk ejection. As the cyclic character of nursings gets established over the first 12 h, the distinctive grunting peaks get linked with synchronous piglet suckling, and grunting no longer occurs outside the nursing episodes. This pattern is well established by the 2nd day postpartum (Castrén et al, 1989b; de Passillé and Rushen, 1989).

Piglet teat competition

Piglet com petition for teats is a prom inent aspect of the neonatal behavior. Piglets are precocial, being capable of active com petition w ithin m inutes of b irth (de Passillé et al, 1988a; Rushen and Fraser, 1989). Neonatal piglets even possess specifically oriented canine and incisor teeth for the biting com petition w ith each other (Fraser and Thompson, 1991). Piglets that are born earlier sample m ore teats and win m ore of their teat disputes than later born litter-m ates (de Passillé and Rushen, 1989). Although low- b irth-w eight piglets, late-born piglets, and piglets sucking only posterior teats tend to obtain less colostrum , the differences are small and m ost piglets obtain an am ount of colostrum consistent with norm al serum im m unoglobulin concentrations (Fraser and Rushen, 1992). Birth order has little effect on im m unoglobulin G levels, except when the duration of farrowing exceeds 4-5 h, in which case late-born piglets may be at risk (Devillers et al, 2011). D uring the teat sampling period, piglets fight with each other over any functional teat as they move along the udder. The highest frequency of fighting occurs at 3 h postpartum . Already during these teat-sam pling fights, the pig with the teat in its m outh wins two thirds of the fights (de Passillé and Rushen, 1989). As individual piglets gradually restrict the num ber of teats they suckle, this ‘hom e court’ advantage develops

The gesta ting and lac ta tin g sow 299

M. Špinka and G. IU m ann

into durable teat ownership. By the first day, between 5% and 50% of piglets establish a stable ownership of one specific teat while the other piglets fight over teat ownership as they switch between several teats (de Passillé et al, 1988a; Puppe and Tuchscherer, 1999). Teat fighting decreases and teat order stability increases steadily until it reaches the level o f 85-95% by the 4th day. Teat ownership means that piglets return to the same teat at successive sucklings and fiercely defend it against siblings (de Passillé et al, 1988a; Puppe and Tuchscherer, 1999).

Piglets who fail to acquire a teat early pay a double cost; they expend energy in attempts to displace others from their teat and they often consum e less colostrum that is vitally im portant both as the initial source of energy and for im m unity (Farm er and Quesnel, 2009). Com petition, rather than a general inability to thrive, appears to be the cause of m uch starvation death (Andersen et al, 2011; Drake et al, 2008). Litter size is im portant in determ ining the seriousness of the consequences of teat com petition. Although it is unclear w hether the intensity of fighting am ong siblings increases with litter size (D’Eath and Lawrence, 2004; de Passillé and Rushen, 1989; Scheel et al, 1977) the consequences of the com petition are graver in large litters (Andersen et al, 2011). Piglets in large litters have lower b irth weight, and the am ount of colostrum ingested per piglet decreases by about 10% with each additional piglet born because the total colostrum yield is constant across different litter sizes (Devillers et al, 2007). Piglet’s birth weight is another im portant factor because heavier piglets win m ore fights over teats (Scheel et al, 1977), gain more weight (Milligan et al, 2001) and experience lower m ortality (Tuchscherer et al, 2000). M ortality of piglets due to crushing or starvation occurs mostly w ithin the first days of postnatal life and affects m ainly the low-weight piglets in large litters. This is often in direct relation to their inability to secure teat access and, therefore, to their insufficient colostrum and early m ilk intake.

13.3 Nursing during the established lactation

This second part of the chapter describes the features and the structure of sow nursing behaviour beyond the colostrum period, i.e. from the tim e w hen cyclic nursing is established until weaning.

13.3.1 Structure o f the typical pig nursing

A pig nursing episode (a nursing’) typically consists of five m ain phases (Figure 13.1): nursing initiation, pre-ejection teat massage, m ilk ejection, post-ejection teat massage and nursing term ination (Fraser, 1980; Schön et al, 1999; Špinka et al, 2002).

N ursing in itiation occurs in two ways. First, sows can spontaneously assum e the lateral lying nursing position, thereby widely exposing their udder, and start to grunt rhythmically. In reaction to these stimuli, piglets assemble at the udder and start the teat massage. Second, individual piglets can approach the sow, vocalize near the m outh of the sow and start massaging the teats w ith their snouts. This behaviour recruits further piglets to jo in the stim ulation until the sow assumes the nursing position and starts

300 The gesta ting and lac ta tin g sow

13. N ursing behavior

Figure 13.1. Structure of a pig nursing with milk ejection (adapted from Fraser, 1980).

grunting. The ensuing phase is the pre-massage, during which all or m ost of the piglets intensely rub the vicinity o f ‘their respective teats and occasionally suck at them . Some of the piglets may in terrup t the massage by going to the snout of the sow w here they em it short series of croaking vocalisations’ while in naso-nasal sniffing contact w ith the m other.

After 1 -3 m in of teat stimulation, the posterior part of the pituitary gland (neurohypophysis) discharges a surge of oxytocin which, upon reaching the m am m ary glands via the bloodstream , triggers the crucial phase of m ilk ejection (Ellendorff et ai, 1982). Milk ejection in pigs lasts only 20 sec on average. Physiologically, the burst of oxytocin makes the myoepithelial cells that surround the gland alveoli contract and the milk is ejected into m ilk ducts from where it can be w ithdraw n by the suction in the m outh of piglets. The m ilk ejection occurs simultaneously in all glands. As the sow does not have teat cisternae, both the increased intram am m ary pressure and active pum ping by the piglets’ jaws and tongue are necessary for the m ilk to be extracted. The milk ejection can be recognized by distinct piglet behavior: as the m ilk begins to flow, the piglets stop massaging the teat vicinity with their snout, they hold the teats firmly in their m outh and pull them , thereby perform ing rapid sucking j aw movements as they w ithdraw the milk from the m ilk ducts.

The gestating and lac ta tin g sow 301


After the brief m ilk ejection, piglets resum e teat massaging and may continue to do so for several m inutes, although their num ber decreases as they individually cease to be active at the udder. This is the post-ejection massage phase. Nursing term ination is triggerred either by the piglets, when they fall asleep at the udder or leave to rest elsewhere, or by the sow when she rolls on her belly or stands up while the piglets are still active with post-ejection massage.

D uring a suckling, the sow emits regular deep grunts at a rate of about one grunt every two seconds during the pre-ejection massage. About 20 sec before m ilk ejection, the grunt rate suddenly increases to a peak of about two grunts per second, and then wanes (Illm ann et al, 1999).

13.3.2 Nursing frequency

Sows nurse every 50 m in on average with a wide variation in the individual inter-nursing intervals. There is little or no difference in the nursing rhythm between day and night. The nursing rhythm is related both to the physiology of m ilk release, and to the interactions between the sow and the litter. After each m ilk ejection, there is a refractory period of about 20 m in during which it is impossible to trigger another m ilk release through teat stim ulation, no m atter how intensive. The inhibitory system is centrally located as intravenous injections of oxytocin can cause gland contraction w ithin a m inute of the natural m ilk ejection (Ellendorff et al, 1982). The o ther factor causing the rhythm ic nursing is the cycle of activity and resting in the piglets. After ingesting m ilk and the post-ejection massage, piglets mostly become inactive or go asleep, either at the udder or at the m ost comfortable resting place available, and it is usually after several tens of m inutes that they are active again at the udder and start a new nursing episode.

Nursing initiation is the decisive factor for nursing frequency. D uring the first days after parturition, the sow initiates 80 to 100% of the nursings. D uring the second week of lactation, this proportion drops below 50% and by 4 weeks o f age, less than 10% of nursings are sow-initiated (Algers and Jensen, 1985; Castrén et al, 1989b; Jensen et al, 1991; Silerová et al, 2006).

The nursing frequency changes gradually over the course of lactation, but changes are relatively m inor within the first 4-6 weeks. From the initial 24-26 nursings per 24 h, there is a slight increase to 28-30 nursings per day until the second week of lactation and a slow decline thereafter. From the second week on, sows attem pt to lim it piglets’ suckling activity in several ways possible, i.e. by spending m ore tim e resting on their sternum or by declining to lie dow n/roll on their side when piglets ask for teat access through activity at the udder ( Valros et al, 2002). Nevertheless, even around commercial weaning age at 4-5 weeks, sows still nurse alm ost 20-24 times a day (Valros et al, 2002). The nursing frequency seems to follow the same pattern over the first four weeks of lactation in very different housing systems and environm ents, ranging from the com m ercial crate, to individual and group pens and sem i-natural free-ranging (Jensen and Recén, 1989; New berry and W ood-Gush, 1985; Pajor et al, 2002; Silerová et al, 2013; W allenbeck et al, 2008). However, in systems where the sow can leave the piglets behind and access

302 The gestating and lac ta tin g sow


a ‘piglet-free area, the nursing frequency is at least 10% lower (Arey and Sancha, 1996; Pajor et al., 2002) and the inter-individual variability in sow nursing behavior is larger so that some sows even wean their litters prem aturely (Boe, 1993b). W hen suckling is allowed to continue w ithout hum an interference in sem i-natural environm ents, nursing frequency continues to decline until piglets are weaned at 10-16 weeks of age (Jensen, 1988; Jensen and Recén, 1989; N ew berry and W ood-Gush, 1985).

There is a complex relationship between nursing frequency and m ilk production of the lactating sow. Individual sows com m only increase or decrease their nursing frequency from day to day w ithout discernible external causes (Illm ann and Madlafousek, 1995; Špinka et al, 1997). These spontaneous day-to-day changes in nursing frequency are paralleled by changes in m ilk production (Špinka et al, 1997). That is, if a sow increases the num ber of nursings from one day to the next, the piglets get m ore m ilk on the next day This is due to the fact that m am m ary glands are alm ost completely refilled with newly produced m ilk w ithin 35 m in after the last m ilk ejection (Špinka et al, 1997), and further m ilk accum ulation then slows down asymptotically. If piglets succeed to suckle more frequently, they get a greater num ber of almost-full-size m ilk portions and hence greater total m ilk intake. Conversely, suckling at larger-than-usual intervals results in a fewer num ber of portions and lower m ilk intake. A reduction in nursing frequency may also lead to reduced prolactin concentrations and altered patterns of som atotropin secretion (Rushen et al, 1993), whereas m ore frequent nursings may lead to altered insulin concentrations and, thereby, to a m ore catabolic state (Špinka et al, 1999). Thus, the individual adjustm ents to nursing frequency can be seen as a bargaining between the sow and the piglets to decide the am ount of milk transferred (Špinka et al, 2011) and, thereby the use of sow body reserves.

Beside the w ithin-sow fluctuations of nursing frequency, there is also a degree of between- sow variation in nursing frequencies (Špinka et al, 2002; Valros et al, 2002), and this especially in later lactation (Wallenbeck et al, 2008). In the first week of lactation, between- sow differences in nursing frequencies do not seem to be related to m ilk production (Špinka et al., 1997), but later in lactation when sows differ in nursing frequencies because of individual behavioral profile (Valros et al, 2002), environm ental factors (freedom of movement, (Boe, 1993a) or genotype (Meishan vs. European Large W hite, (Sinclair et al„ 1998), greater litter weight gains are associated with more frequent nursings.

13.3.3 Teat m assaging

Each nursing episode, from the nursing initiation when the litter assembles at the udder and starts teat m anipulation until the nursing term ination by the sow or by the piglets, lasts several minutes. W ith the exception of the brief m ilk ejection, the whole duration of the nursing is devoted to piglet activity called teat massaging. D uring teat massaging, a piglet alternates between b rief sucking of the teat and intense rubbing of the teat surrounding with its snout. The intensity of this tactile stim ulation is often notable in the contrast between the clean skin around the teats and the dirty body surface elsewhere.



No m ilk is transferred during the teat massaging phases o f nursings, so the question arises as to what is the function of this conspicuous and tim e consum ing behaviour? The pre-ejection massage is necessary to trigger the m ilk ejection. The average tim e from the onset of teat stim ulation until the g runt rate peak (which indicates m ilk ejection) decreases from approximately 2 m in on day 1 postpartum to 1 m in on day 7 (Algers et al., 1990), and then rem ains stable. The greater the proportion of piglets participating in pre-massage, the shorter is the tim e until m ilk ejection is triggered. Since the pre-massage is accom panied by loud grunting of the sow, it seems that its function is to allow for the whole litter to assemble at the udder and for all piglets to find their teats.

The function of post-ejection massage is less clear. There is a large variation in duration and intensity of the post-ejection teat massage. At the litter level, the post-ejection massage can be considerably longer than the pre-ejection massage, but the post-ejection massage is m uch less consistently attended by individual piglets (Jensen, 1988). Algers and Jensen (1985) proposed the so-called restaurant hypothesis, according to which teat m assaging allows piglets to regulate the am ount of milk produced by the teat receiving the stim ulation. Experim ental evidence exists that piglets and whole litters that gained less weight in previous nursings and previous days perform longer and/or m ore intensive post-ejection massage (Špinka and Algers, 1995), thereby indicating that insufficient milk supply boosts subsequent teat massaging. However, the evidence that this intensified teat m assaging results in increased m ilk output is surprisingly weak (Illm ann et al, 1998; Jensen et al, 1998; Špinka and Algers, 1995). For the lack of better supported alternatives, the hypothesis that piglets signal their need for m ilk through the tactile channel o f postejection teat massaging and that the sow modifies m ilk production according to this signalling rem ains perpetuated.

Physiologically, the am ount of teat massage perform ed by the piglets is related to the release of several horm ones, including prolactin, som atostatin, som atotropin, glucagon and vasoactive intestinal polypeptide (Algers et al, 1991; Rushen et al, 1993; Špinka et al, 1999). Since these horm ones can influence m aternal behavior and /o r improve the sows digestive efficiency (Algers et al, 1991; Uvnäs-M oberg et al, 1984), teat massage can obviously have other effects beyond affecting the quantity of m ilk produced.

D uring the first days of lactation, sows allow the piglets to massage the udder as long as they want on m ost nursings and the post-ejection massage lasts, on average, three or m ore m inutes. As lactation progresses, sows term inate an ever increasing proportion of nursings, and by 4 weeks 65 to 100% of nursings are sow -term inated (D am m et al, 2003; Vahos et al, 2002). The duration of post-ejection massage therefore gets curtailed as lactation progresses (Valros et al, 2002) and the duration of the post-ejection massage drops below 90 sec by week 4 (Jensen and Recén, 1989).

13.3.4 Non-nutritive nursings

In pigs, the relationship between nursing behavior and m ilk intake is complicated by the existence of non-nutritive nursings. A non-nutritive nursing begins in the same way as a norm al nutritive nursing, i.e. w ith piglets stim ulating the teats and sows assum ing the

304 The gesta ting and lac ta ting sow


nursing position and em itting the typical grunting vocalizations (Illm ann et al, 1999). However, in non-nutritive nursings, in spite of the teat stim ulation, the sow does not increase her grunting rate (Illm ann et al, 1999), oxytocin is not released (Ellendorff et al, 1982), m ilk is not ejected and therefore there is no m ilk intake (Fraser, 1977; Illm ann et al, 1999). Behaviorally, a non-nutritive nursing can be distinguished by the absence of peak in grunting and even more reliably by the lack of piglets’ rapid m outh movements that norm ally occur during m ilk ejection (Figure 13.2).

N on-nutritive nursings are not rare exceptions and cannot be considered physiological abnorm alities or pathological disturbances. N on-nutritive nursings make up between 5% and 30% of all nursing episodes and occur with a sim ilar average frequency in all

Figure 13.2. Sow grunting rate (A) and rate of teat massaging movements by the piglets (B) in a nutritive and

a non-nutritive nursing (adapted from ilimann et al., 1999).



types of housing systems from very intensive (Fraser, 1977; Illm ann and Madlafousek, 1995; Illm ann et al., 1999; Puppe and Tuchscherer, 2000; Valros et al, 2002; W hatson and Bertram , 1980) to sem i-natural (Castrén et al., 1989a; N ew berry and W ood-Gush, 1985), and also in the wild boar (Horrell, 1997). N on-nutritive nursings start appearing w ithin the first 24 h postpartum , as soon as the cyclic pattern of m ilk release gets established (Castrén et al, 1989a; Illm ann and Madlafousek, 1995), and occur over the whole course of lactation, possibly with some peak of occurrence around week 2 (Valros et al, 2002).

N on-nutritive nursings prolong the intervals between nursings with m ilk ejections (Castrén et al, 1989a; Fraser, 1977; Špinka et al, 2011). Because the increase in milk available in the m am m ary glands with prolonged intervals is only slight (Špinka et al, 1997), the net effect of non-nutritive nursings is an overall decline in m ilk consum ption by piglets. Therefore, it could be that the absence o f m ilk ejection in som e nursing episodes is a strategy by the sow to dow n-regulate the m ilk output when piglets are initiating nursings too frequently (Špinka et al, 2011). This assum ption is supported by the fact that the probability of a nursing to be non-nutritive strongly increases if the nursing occurs soon after the last m ilk ejection, and also if the nursing was initiated by the piglets rather than by the sow (Castrén et al, 1989a). This strategy seems to be physiologically based, i.e. related to the central refractory period described above rather than cognitively guided. Experim ental evidence confirm s that in the dom estic sow, m otivation to nurse can be separated from the instantaneous (in)ability to release milk. Indeed, Fraser (1975) showed that when a sow is separated from her litter, stim ulated to exhibit the m ilk ejection oxytocin reflex (w ithout m ilk removal) by hand massage and shortly thereafter reunited with her litter, the sow starts a nursing willingly. However, the nursing is always w ithout m ilk ejection, in spite of the fact that her litter is hungry and her glands are full of milk.

W hile non-nutritive nursings do not provide any milk to piglets, they may still play a role in the horm onal state of the sow as prolactin and som atotropin are increased after non-nutritive nursings, although the concentrations are still lower than after a nutritive nursing (Rushen et al, 1993).

13.3.5 Nursing synchronization and allo-suckling

W hen lactating sows are housed in groups, their nursings become highly synchronized. For instance, in groups of 3-4 sows, the proportion of nursings occurring w ithin 1 m in of each o ther am ounted to 81% (M aletínská and Špinka, 2001). The acoustic contact is sufficient for synchronization to occur also in sows housed in individual crates (Šilerová et al, 2013; Špinka et al, 2004;). The possibility has been investigated to use this sensitivity and induce more frequent nursings (and thereby higher piglet growth) through playbacks of the nursing vocalizations. Although some studies found positive effects (C ronin et al, 2001), the m ajority found none (Farm er et al, 2004; Špinka et al, 2004; W idowski et al, 1984), so the m ethod has not been practically applied.

W hy does such a strong tendency exist am ong sows to synchronize their nursings? One possibility is that when lactating sows roam ed in small groups, nursing synchronization



served the purpose to keep a lim it on alio-suckling, i.e. non-offspring nursing. In free- ranging and group-housed sows, piglets allo-suckle either by perm anently switching to another dam, or by opportunistically suckling on other sows while staying at their own m other for regular suckling. W hen nursings are tightly synchronized, the opportunity for allo-suckling is reduced, since the opportunistic allo-sucklers cannot suckle both their own m other and another sow at the same tim e (Illm ann et al., 2005; M aletínská and Špinka, 2001).

13.4 Functions of nursing/suckling behavior during the course of lactation

The functional view of nursing behavior has its roots in evolutionary theory. It is based on the assum ption that anim al behavior has been shaped by natural selection so that it brings the behaving animals benefits such as food, security, inform ation, etc., which in tu rn contribute to the anim als’ survival and reproduction. Applying this view to the behavior of dom esticated anim als is not w ithout controversy since both the animals and the environm ent are often quite different from their wild ancestors in their natural environm ents. For instance, the domestic pig differs from the wild boar in that it has much larger litters, is generally less active (Gustafsson et al, 1999), is given free food, and its physical and social environm ents are determ ined and provided by hum ans. Nevertheless, the basic functional question ‘W hat benefit does this behavior bring to the anim al?’ proved fruitful in behavioral research on domestic animals in the last decades (Drake et al, 2008; Fraser et al, 1995; Puppe and Tuchscherer, 2000; Špinka et al, 2011).

N ursing provides the young w ith milk. The rich structure and dynam ism of the sow- piglet, piglet-piglet and sow-sow interactions imply that nursing is m uch m ore than a m echanical transfer of m ilk from the sow m am m ary glands to the offspring’s stomachs. The nursing interactions co-determ ine how m uch m ilk is provided, how this m ilk production is allocated to individual piglets, and how the m ilk provision to non- m aternal young is prevented/ regulated. These m echanism s can be seen as results of interactions between the strategies of the individual actors, i.e. the sow and the piglets. From the perspective of the sow, the best strategy is to support the survival and growth of as m any progeny as possible. However, if some of the piglets are not viable or the resources available for the sow cannot support all the progeny, it may be beneficial for her reproductive success to discard some of the progeny early and be able to provide m ore m ilk to the rem aining healthy young. Also, if the sow uses up a lot o f her body reserves during lactation or is suckled by heavier piglets, her future reproduction may be compromised. For example, the weaning to estrus interval may be prolonged and the next litter size decreased (Bierhals et al, 2012; Schenkel et al, 2010; Ten Napel et al, 1995). Thus, w ithin the nursing interactions there are features showing cooperation between the m other and the litter to ensure efficient m ilk transfer, but there may also be features reflecting the parent-offspring conflict about how many progeny to raise and how much to invest into them so that future reproduction is no t compromised.



From the point o f view of the individual piglet, it is good to cooperate with other piglets to stimulate sow m ilk production. At the same time, getting a preferential share of the milk production is a beneficial strategy since it will support faster growth. This creates space for sibling com petition over the milk allocation. Additionally, a beneficial strategy for the sow may be to allocate the m ilk equally to the viable progeny, the sow may thus behave in such a way as to suppress sibling com petition.

13.4.1 Colostrum /m ilk production and litter size

The m ost im portant function of the nursing interactions during the early postpartum teat-sam pling period is the provision of colostrum to piglets. The parturient and postparturient sows facilitate this function by exposing their udder through im m obile lateral lying, thereby enabling the piglets to sample all teats freely. Piglets fight a lot during teat sampling and the proportion of fights won by a piglet has a positive, albeit weak, influence on how frequently the piglet suckles during the first day postpartum , however it has no influence on the num ber of teats suckled (de Passillé and Rushen, 1989; de Passillé et al, 1988a). Thus, it seems that passive exposure of the udder by the sow creates an even playing field in which m ost piglets can have a p roper colostrum intake. However, the ability of the sow to provide a reliable source of colostrum for all piglets may reach a lim it as the num ber of piglets approaches or even surpasses the num ber of functional teats. The factors affecting colostrum yield are covered in Chapter 8 (Quesnel et al, 2015). W ith relation to litter size, it is known that total colostrum yield is constant across different litter sizes (Devillers et al, 2007; Quesnel, 2011), but that colostrum intake per piglet decreases with increasing litter size. Because m ilk yield am ong sows varies considerably, it is estim ated that about 35% of sows do not produce enough colostrum to adequately supply all their piglets (Quesnel et al, 2012). In addition, sows with high w ithin-litter variation in piglet birth weights produce less colostrum (Quesnel, 2011). As a result, low b irth weight piglets in large litters are at a heightened risk of not obtaining at least 200 g of colostrum , which is the am ount needed for adequate im m unoglobulin levels and m inim um growth. Andersen et al. (2011) proposed that neonatal m ortality in large litters is adaptive’, i.e. that it is a strategy for sows facing a trade-off between the offspring quality and their quality or vitality. According to this ‘litter reduction’ hypothesis, the function of m aternal passivity is to allow free course for the sibling com petition which results in discarding the weakest offspring so that m ore resources are available for the surviving m ajority of piglets. A lthough this view m ight be controversial, it highlights the fact that the intense selection for large litter size at birth results in greater piglet mortality, and thus, in ever smaller net gains in the num ber of weaned piglets (Milligan et al, 2002).

Piglet m ortality occurs mainly during the first 1-3 postnatal days so that individual litter sizes are almost stable over the rest o f lactation. This has im portant implications for milk production because unsuckled glands regress rapidly w ithin the first week (Kim et al, 2001) and total m ilk production is affected (see Chapter 4 on m am m ary developm ent for more details (Farm er and Hurley, 2015)). The established litter size determ ines to a great extent the ensuing m ilk production, as docum ented by the fact that m obilization of body protein in sows increases linearly with litter size at week 3 of lactation. In smaller litters,



some piglets are able to suckle two teats (Illm ann et al., 2007) but it is unknow n whether this increases milk production.

13.4.2 Milk production and nursing frequency

The am ount of suckling allowed by a sow can directly affect instantaneous milk production. Two m echanism s have been proposed as to how piglets can stim ulate a greater milk output. The first is teat massaging during the post-ejection phase of nursing. Empirical evidence indicates that the duration of the post-ejection massage in the last few nursings has a short-term positive effect on m ilk output during following nursings (Jensen et al., 1998; Špinka and Algers, 1995). Yet, perform ing longer post-ejection massages over days or weeks of lactation does not increase m ilk output (Špinka and Algers, 1995; Torrey and Widowski, 2007). The second, and stronger effect, is through m ore frequent initiations of nursings by the piglets, whereby the frequency of m ilk ejection is increased and the more frequent em ptying of m am m ary glands enhances m ilk production. From a functional point of view, the feedback loop from hungrier piglets through m ore frequent nursing initiation to enhanced m ilk output resembles the provisioning-begging-provisioning cycles between bird parents and their nestlings and can be understood as a case of honest signaling of need. N on-nutritive nursings may serve as a cost that the sow imposes on piglet nursing initiation if it becomes too frequent (Špinka et al, 2011). Thus, the need of the litter for m ilk is expressed in the frequency of nursing initiation and in the propensity to engage in long teat massage. The sow may consent to it by allowing nutritive nursings and perm itting long post-ejection massaging phases; or the sow can w ithstand the dem and by failing to release m ilk and/or by curtailing the post-ejection massage. This feedback loop may contribute to the stability of m ilk production at a level that is adjusted to the needs of the litter while being affordable by the sow.

13.4.3 Milk allocation to individual glands/piglets

Through their behavior at the udder, piglets can individually influence the portion of m ilk output produced by their m other that they will acquire. Stronger piglets are able to displace weaker siblings from teats, leading to the danger of very unequal milk distribution. However, neither very unequal m ilk allocation to piglets (M illigan et al., 2002) nor wastage of energy through intense sibling com petition is beneficial for reproduction of the sow. It seems that the nursing behavior and physiology of the sow were shaped by natural selection to curtail com petition among siblings. First, the pre-massage phase with loud grunting gives all piglets the opportunity to assemble at the udder and find their teat, and the increase in grunting frequency announces to all piglets the incom ing milk ejection. Second, the brief and synchronous window of m ilk availability in all teats does not give the stronger piglets a chance to usurp m ilk production of m ore than one teat. Thus, the brief m ilk ejection in com bination with acoustic signaling by the sow ensures a largely undisturbed m ilk intake for all litterm ates (Drake et al, 2008; Fraser, 1980).

Three phases of piglet com petition can be distinguished as lactation progresses. During the teat sampling phase (approximately the first 12 h), piglets compete over the num ber of teats suckled and the am ount of colostrum ingested. The short and sharply delimited



m ilk ejections get established at about 12 h after the onset of parturition, and piglets then compete over early possession of a productive teat rather than over the num ber of teats suckled. During the second phase (approximately the first three days), piglets jockey for possession of individual teats and piglets that acquire high teat fidelity early on benefit from more frequent nursing participation and faster early growth (de Passillé et al, 1988a). Teats used in the previous lactation give more m ilk on the average than previously unused teats (Farm er et al, 2012). A nterior teats tend to be preferred by piglets and produce somewhat more m ilk than posterior teats, but this is m ore due to their more consistent and more intensive use by the heavier piglets rather than due to inherent higher productivity (Fraser and Rushen, 1992; Orihuela and Solano, 1995). D uring the first, and to a lesser extent during the second, com petition phase sibling com petition contributes strongly to the disproportional m ortality of low birth weight piglets, especially in litters with a high variation in b irth weight (Milligan et al, 2002). Once the teat order is established, by the fourth day, direct com petition vanishes and indirect com petition can then take place. At this tim e piglets can possibly get extra m ilk at the expense of litterm ates if they are able to boost m ilk production in their teat, e.g. through more complete m ilk withdrawal or m ore intense teat massage. W ithin litters, piglets differ widely in their m ilk intake, and hence in body weights, but only about 20% of this variation can be explained by differences in teat fidelity and teat position (Fraser and Thompson, 1986). The fact that w ithin-litter coefficient of variation in body weights does not increase from birth until weaning (Milligan et al, 2002) indicates that com petition of piglets for teats does not exacerbate the initial differences in body weights am ong littermates.

13.4.4 Securing mother-young bond, allo-suckling regulation

Although lactating sows are housed individually in m ost commercial settings and thus do not encounter alien piglets, this is not the setting in which pig nursing behavior evolved. In natural wild boar groups, several females lactate at the same tim e and therefore allo- suckling (non-offspring nursing) is possible. If several dom estic sows are housed in indoor group pens or outdoor parks, allo-suckling occurs regularly (Kim et al, 2001; M aletínská and Špinka, 2001; N ew berry and W ood-Gush, 1985). From a functional point of view, a certain degree of non-offspring nursing may be, at least in some cases, adaptive to the m other (Roulin, 2003; Roulin and Heeb, 1999), for instance if the allo- sucklers are progeny of a genetically related female as is often the case in wild boar groups (Kaminski et al, 2005). Nevertheless, the non-offspring young will, due to their low genetic relatedness to the foster m other, dem and m ore frequent allo-suckling than is optim al for the dam. Therefore, it is beneficial for the sow to distinguish her own from alien piglets and to regulate the access of the latter to her m ilk supply.

The early sow-piglet interactions serve to quickly establish the m aternal bond with the piglets. Through sniffing the piglets, the sow quickly im prints into her m em ory the olfactory identity cues of individual piglets w ithin 24 h postpartum . This can be accomplished actively during the brief activity bouts at parturition or when piglets come to the snout of the lying sow during teat sampling or cyclic suckling, or later when the sow regains activity between nursings (M aletínská et al, 2002). The recognition of her own piglets via individual smell signatures enables the sow to identify alien piglets and



discourage allo-suckling by targeted aggressive behavior (Olsen et al, 1998). This process needs to be taken into account when cross-fostering of piglets is perform ed. Similarly, piglets also learn the olfactory identity of their m other by early exposure to her odor (Horrell and Hodgson, 1992).

Moreover, m utual recognition is possible through the acoustic channel. Individual sows differ both in the absolute rates of grunting and in frequency com position of individual grunts (Schön et al, 1999; Špinka et al, 2002). These features can serve as acoustic signatures of individual sows. Piglets are thus able to find their m other quickly even when several sows are grunting at the same tim e due to nursing synchronization. By timely arrival to the udder, own piglets are able to fight off allo-sucklers and to consume the milk. Piglets w ithin the same litter share similarities in the acoustic qualities of their calls (Illm ann et al, 2002) and sows use these cues to attend preferentially to their own piglets, e.g. when they get isolated from her.

Two other features in nursing behavior may also have the role of reducing the incidence of allo-suckling; namely, nursing synchronization and non-nutritive nursings. There exists an interesting interaction between nursing synchronization, occurrence of n o n nutritive nursings and allo-suckling. Most nursings are synchronized and in these nursing allo-suckling is hindered by the concurrent occurrence of m ilk ejections. Interestingly, w hen nursings are not synchronized, the proportion of non-nutritive nursings becomes greater (Illm ann et al, 2005), indicating that nursing synchronization and the fact of not releasing m ilk during non-synchronized nursings are two com plem entary strategies that lactating sows use to reduce allo-suckling.

13.4.5 Gradual weaning during lactation?

It was proposed that the process o f weaning, in the broad m eaning of gradual reduction of the m aternal m ilk investm ent, already starts w ithin days after b irth and continues th roughout lactation (Drake et al, 2008; Puppe and Tuchscherer, 2000). This process was interpreted as a case of parent-offspring conflict in which the progeny attem pt to w ithdraw m ore resources than the parents are prepared to give because excessive investm ent into the current young may endanger future reproduction by the parent. There are indeed prom inent changes in nursing behavior over lactation. In early lactation, alm ost all nursings are initiated by the sow and almost none are term inated by her. Thus, the sow actively prom otes milk transfer and offers unlim ited opportunity for the litter to massage the teats during their first days of postnatal life. However, already by the second week of lactation, only half of the nursings are sow-initiated and by week 4 the proportion drops to near zero. In parallel, the proportion of sow -term inated nursings increases to 50-100% by week 4. There is therefore an almost absolute reversal o f roles between very early and later in lactation. However, developm ents of o ther aspects o f nursing behavior do not indicate a clear offspring-dam conflict or weaning process as lactation advances. Nursing frequency declines by only about 10% between the 1st and 4th week of lactation (Puppe and Tuchscherer, 2000; Valros et al, 2002). N on-nutritive nursings, which are a sign of conflict between the m other and the litter over m ilk output, seem to peak at week 2-3 and then decline, instead of increasing continuously as would be expected if

The gestating and lac ta ting sow 311


the m other-litter conflict was gradually intensifying with the ongoing lactation. Hence, the num ber of nutritive nursings, w hich is the behavioral measure m ost closely related to m ilk output but which is infrequently recorded, may be alm ost stable across the first 4 weeks of lactation (Valros et al, 2002). Im portantly, daily m ilk yield of com m ercial sow breeds increases until the m id-th ird week and then rem ains stable until day 30 of lactation (Hansen et al, 2012).

It has been proposed that in housing systems that allow greater freedom of movem ent for the sow, the gradual weaning processes progress faster (Drake et al, 2008). Indeed, lactating sows housed in ‘get-away’ pens, where they can leave piglets and stay in a piglet-free area, have approximately 10% lower nursing frequencies than sows housed in regular pens (Drake et al, 2008; Pajor et al, 2002). However, preventing the piglets from approaching their m others is an unnatural restriction. Data from other types of housing do not show a clear difference in nursing frequency at week 4-6 between sows housed in individual pens, group pens and outdoor runs (Newberry and W ood-Gush, 1985; Šilerová et al, 2006).

In conclusion, there are prom inent changes in nursing initiation and term ination taking place over the first weeks o f lactation. However, the nursing frequency and lactation output indicate that m ilk transfer is not weakened by natural weaning processes before the piglets are separated from the sow at 4-6 weeks and is not substantially different in various housing systems.

13.5 Conclusions

Nursing in swine is complex because of specific features including brief m ilk ejection, long udder massage by the piglets, nursing synchronization, non-nutritive nursings and ontogenetic shifts in nursing initiation and term ination. In order to understand pig nursing fully, knowledge about the underlying physiology m ust be com bined with a thorough elucidation of the behavior of the sow and the piglets including the acoustic, olfactory and tactile com m unication. The functional view on nursing behavior, based on the evolutionary theory, is useful in highlighting the potential for both cooperation and conflict between the sow and her progeny.

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13. Nursing behavior

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