Effects of feed-back from the nest on maternal responsiveness and postural changes in primiparous sows during the first 24 h after farrowing onset

Applied Animal Behaviour Science 83 (2003) 109–124

Effects of feed-back from the nest on maternal responsiveness and postural changes in primiparous sows during the first 24 h after farrowing onset L.J. Pedersen a,∗ , B.I. Damm b , J.N. Marchant-Forde c , K.H. Jensen a a

b

Department of Animal Health and Welfare, Danish Institute of Agricultural Sciences, P.O. Box 50, 8830 Tjele, Denmark Department of Animal Science and Health, The Royal Veterinary and Agricultural University, Grønnegårdsvej 8, 1870 Frederiksberg C, Denmark c USDA-ARS, Livestock Behavior Research Unit, 219 Poultry Science Building, Purdue University, West Lafayette, IN 47907, USA Accepted 8 April 2003

Abstract In order to elucidate whether feed-back from a farrowing nest affects the sows’ activity level and responsiveness to piglets during the first 24 h after the onset of parturition, 18 primiparous Landrace × Yorkshire sows were given the opportunity to build a farrowing nest of peat, straw and branches in Schmid pens. Eight treatment sows then had their nest removed 8–10 h after the onset of nest-building and again every 4 h until farrowing began, whereas 10 control sows were allowed to keep the nest. During the first 24 h after birth of the first piglet the behaviour of the sows and piglets was observed and heart rate of the sows monitored using a transmitter belt and watch receiver. The frequency of postural changes and a maternal responsiveness index was calculated. In addition, time from birth of each piglet until it suckled for the first time was calculated. In the treatment group there was a constantly higher level of maternal responsiveness (P < 0.0001), but the frequency of postural changes did not differ from that of control sows. The timing of maternal responsiveness was not affected by treatment, but in both treatment groups maternal responsiveness was significantly higher during the first 2 h after birth of the first piglet than in the following 6 h (P < 0.0001). Hereafter (8–24 h postpartum) the maternal responsiveness significantly increased (P = 0.05). The frequency of postural changes also was higher during the first 2 h (P < 0.0001) than in the following 6 h after which it increased again (P = 0.05). Heart rate gradually declined over the first 8 h after birth of the first piglet (P < 0.0001) after which it stayed level. Piglets from treatment sows took significantly longer to suckle for the first time compared to piglets from control sows (P < 0.05). The decrease in activity and maternal responsiveness shortly after parturition has begun is likely to be advantageous for the piglets as it reduces the risk of piglet ∗

Corresponding author. Tel.: +45-89-99-13-64; fax: +45-89-99-15-00. E-mail address: [email protected] (L.J. Pedersen). 0168-1591/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0168-1591(03)00116-3

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crushing while at the same time giving early access to the udder and to warmth from the sow. The results emphasise the importance of a proper farrowing environment and the opportunity to construct a nest, particularly in loose housed sows where the survival and vigorousness of the piglets depend greatly on the behaviour of the sow because the piglets are not protected by pen features as is the case in farrowing crates. © 2003 Elsevier Science B.V. All rights reserved. Keywords: Sows; Piglets; Maternal behaviour; Responsiveness; Environmental enrichment

1. Introduction In commercial pig production, piglet mortality remains a problem in both crated and loose housed sows. Preweaning mortality varies between systems and farms but mortality rates of 10–15% in intensive systems (Pedersen et al., 1998; Cronin et al., 2000; Marchant et al., 2000) and 14–33% in systems where sows are loose housed (Bøe, 1994; Pedersen et al., 1998; Cronin et al., 2000; Marchant et al., 2000) are not uncommon. The majority of piglets dies within the first 2–4 days of life (Edwards et al., 1986; Marchant et al., 2000). Piglet starvation and crushing by the sow are the predominant causes of death, either independently or because starvation increases the risk of piglet crushing (English and Smith, 1975; Edwards et al., 1986; Dyck and Swierstra, 1987; Fraser, 1990; Marchant et al., 2000). Much of the crushing occurs during and immediately after parturition (Weary et al., 1996; Marchant et al., 2001), because the piglets are either not vigilant or mobile enough to escape risky situations (English and Smith, 1975). However, crushing also occurs later in lactation, when the piglets are especially at risk if they have been starving. Hungry pigs stay closer to the sow and do not have an effective response in risky situations, e.g. when the sow changes posture (Weary et al., 1996). Thus, it has been suggested that inactivity by the sow during parturition and the first few hours after parturition may be an important aspect of good maternal care, as it reduces the risk of crushing while at the same time allowing the piglets access to the udder, providing the piglets with both colostrum and warmth (Jarvis et al., 1999). In the initial stage of parturition, sows change posture more often than in the later stages (Jarvis et al., 1999; Thodberg et al., 1999) and they rise to sniff the first few piglets as they are born (Jensen, 1986). After the initial, more active period, sows generally lie in lateral recumbency (Jarvis et al., 1999; Thodberg et al., 1999; Jensen, 1986) and are unresponsive to their piglets (Jarvis et al., 1999). However, at some point after parturition, sows again begin to respond to the piglets when they approach the snout of their mother (Jarvis et al., 1999) and to piglet screams (Hutson et al., 1991, 1992; Herskin et al., 1998; Thodberg et al., 2002), although this is a highly variable trait (Wechsler and Hegglin, 1997). The exact timing of these changes in maternal responsiveness is not known. Several studies have demonstrated associations between maternal prepartum behaviour and activity during parturition (Thodberg et al., 1999; Damm et al., 2000a) as well as postpartum maternal behaviour such as nursing (Herskin et al., 1999) and responsiveness to play-back of piglet screams (Herskin et al., 1998; Thodberg et al., 2002). Within the last 24 h before parturition, sows are motivated to build a farrowing nest (Jensen, 1986;

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Castrén et al., 1993a; Damm et al., 2000a). The initiation of nest-building is mainly internally controlled (Widowski et al., 1990; Blackshaw, 1983; Boulton et al., 1997a,b), whereas its completion is regulated to a larger extent via environmental feed-back (Jensen, 1993; Arey et al., 1991; Damm et al., 2000a). Apparently, it is important not only for the sow to perform the nest-building behaviour per se, but also that the behaviour results in a satisfactory, functional nest, which will help bring the nest-building to an end (Castrén et al., 1993a; Damm et al., 2000a). However, when the environment does not offer the opportunity to build a satisfactory functional nest due, for example, to a lack of appropriate nest materials, the sow may continue to nest-build during farrowing and be restless while giving birth (e.g. Jensen, 1993; Thodberg et al., 1999; Damm et al., 2000a). It has not previously been studied how the timing of the sow’s responsiveness to her newborn piglets is affected by the opportunity to achieve feed-back from a functional nest. Therefore, the objectives of our experiment were: (1) to describe the timing of changes in maternal responsiveness towards piglets during the first 24 h after birth of the first piglet, and (2) to investigate whether the presence of a farrowing nest built with biologically relevant materials would affect maternal responsiveness and the piglets’ chances of getting early access to colostrum. Differences in feed-back from the presence of a farrowing nest were accomplished by removing the nest after a period of nest-building in half of the sows.

2. Materials and methods 2.1. Animals, housing and care Twenty Danish Landrace × Yorkshire primiparous sows were used. The sows came from 10 different litters and were pair-wise siblings. They were purchased in groups of four from a private farm as gilts, where they had been loose housed in pens during gestation. They were brought to Research Centre Foulum 3 weeks before expected parturition date, which was Day 116 of gestation. On arrival they were placed in four individual farrowing pens (Fig. 1), which were situated in the same room. The pens were designed to stimulate and allow natural periparturient maternal behaviour (Schmid, 1992, 1993). A 3 m × 2.6 m pen was divided into a resting area (2.6 m × 1.1 m) covered by an 8 cm layer of peat and a 5 cm layer of long cut straw and a solid floor activity area (2.6 m × 1.9 m). A piglet box was situated in the centre of the pen. A nipple drinker and a feed trough were located in the activity area. Long cut straw and fir branches (1–4 cm in diameter and 30–50 cm in length) were provided in a pile in one corner on the floor of the activity area. From Day 114, additional straw and branches were supplied several times daily and the gilts thus had unlimited access to nest-building material. The gilts were fed twice daily with a ground standard sow feed containing 1.02 Scandinavian feed unit (FU) per kg feed (1 FU = 7.719 MJ net energy) (Just, 1982). The daily ration was 2.6 kg. From farrowing and throughout lactation, the sows were fed ad libitum with the same food. The activity area was cleaned daily and the resting area was cleaned if soiled. When signs of nest-building (nest-building behaviour, materials removed from the piles or materials arranged in the resting area) had been observed, the pen was

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Fig. 1. Schematic drawing of the farrowing pen, which is slightly modified from the design by Schmid (1991, 1993).

no longer entered except when required by the experimental protocol. Room temperature varied between 19 and 22 ◦ C. The room was lit both by natural daylight and 24 h artificial lighting. 2.2. Experimental protocol 2.2.1. Treatments By random selection within gilts from the same litter, the gilts were designated to either the experimental group (n = 10) or the control group (n = 10). However, due to technical problems during video recording, the experimental group was reduced to 8 sows. In the experimental group, the nest was removed 10–12 h after the onset of nest-building and again every 4 h until the birth of the first piglet. The onset of nest-building was defined as the first occurrence of at least 5 front leg pawings within a 5 min interval or the first occurrence of carrying straw and/or branches, which ever was sooner. The 4 h time interval was determined by a pilot study, which had indicated that this was sufficiently short an interval to impair construction of a new nest prior to parturition, while at the same time not disturbing gilt behaviour to an extreme degree. The first nest removal took place as soon as the gilt was standing or walking. An experimenter entered the nest area and gently gathered together the material by hand or rake and placed them outside the pen. The nest area was evened out and covered with a 3-cm layer of new peat. The subsequent nest removals were carried out if the gilt was also lying, in which case the straw and branches were removed from the nest area including the area around the sow. The area in which the sow was lying was then evened out. Nest removal lasted approximately 1 min. In the control group an

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experimenter entered the activity area and walked slowly and without sudden movements just outside the nest for 1 min. 2.2.2. Other handling and sampling From introduction to the farrowing pens until Day 114, the gilts had been positively handled by the experimenters in order to accustomise them to the procedures. Furthermore, the experiment presented here was part of a larger project, and therefore the gilts were catheterised on Days 111–112 by a method described by Damm et al. (2000b) and approved by the Danish Animal Experiments Inspectorate. From the day after catheterisation until the day after farrowing, blood samples were taken daily. In addition, from 8 to 10 h after the onset of nest-building until parturition, samples were taken at 20 min intervals and, during parturition, after the birth of each of three piglets born within the first two-thirds of parturition. The piglets were earmarked and numbered on the back with an ink pen within the first 5 min after birth without restraining them. These procedures were carried out in accordance with a pilot study in which it was established how this could be done with no or minimal disturbance to gilt and piglet behaviour. Data on sow periparturient behaviour and physiology other than sow reactivity will be reported elsewhere (Damm et al., 2002; 2003). 2.2.3. Behavioural observations The behaviour of the sows was recorded during the periparturient period using 24 h time-lapse video, beginning 4 days before expected parturition and ending 24 h after. The behaviour of the sow and piglets was analysed from the birth of the first piglet to 24 h later. All occurrence of contacts between the sow and her piglets and the number of postural changes were recorded during each of the 24 h following birth of the first piglet. A contact was defined as taking place when the snout of a piglet was within 1 piglet length of the snout of the sow. The initiator of the contact was recorded as being either a piglet (when the piglet approached the snout of the sow) or the sow (when the sow moved towards a piglet). The behavioural observations of the sow during the contact was modified according to definitions by Jarvis et al. (1999) as being either no visible reaction to the piglet (NOR) or movement of the snout towards the piglet (NOSE). Biting was also considered a possible reaction to piglets, but this behaviour never occurred. From the observations, a maternal responsiveness index (Jarvis et al., 1999) was calculated: maternal responsiveness index (MRI) =

nose − NOR nose + NOR

The index could vary from −1, indicating that all responses were NOR, to +1 indicating that all responses were NOSE. The frequency of sow postural changes (see Table 1 for definition of postures) and the duration of time spent in lateral recumbency was recorded each hour. The duration of the interval from birth to the piglet suckled the first time was calculated for each individual piglet. The piglet was considered as having suckled when it suckled a teat for at least 5 s. 2.2.4. Heart rate recording The heart rate of each gilt was monitored continuously from Day 110 to 24 h after the birth of the first piglet, using a Polar Vantage NV (Polar Electro Oy, Kempele, Finland)

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Table 1 Postures recorded for 24 h following birth of the first piglet Posture

Description

Lying laterally Lying ventrally Sitting/kneeling Standing/walking

Lying with the udder exposed and one shoulder touching the floor/bedding Lying on the udder with neither shoulders touching the floor/bedding Leaning on the knees or forelegs without standing on hind legs Standing upright with at least three feet on the floor/bedding

heart rate monitor consisting of a transmitter belt and a watch receiver (see Methodology in Marchant et al., 1995), which was set to record and store heart rate averaged over 5 s periods. The data were then analysed for each gilt to determine the mean heart rate over the 24 h period when standing, sitting, lying laterally and lying sternally and rooting. In addition, the mean and peak heart rates during human presence and suckling bouts and the peak heart rate during piglet expulsion were determined. 2.2.5. Statistical analysis The 24 h during which the behavioural observations were carried out were divided into 12 × 2 h time intervals. The maternal responsiveness index, the number of postural changes and the mean heart rate were calculated within each time interval. The development in postural changes, the maternal responsiveness index and mean heart rate over the 12 time intervals were analysed using a mixed model for repeated measurements. The number of postural changes was square root transformed before analysis in order to obtain normally distributed residuals. Yijkl = µ + αi + Aj(il) + βk + (αβ)ik + Bl + εijkl where Yijkl is the response variable (index, square root transformed number of postural changes or mean heart rate), µ is the general mean, αi is the systematic effect of the ith treatment (i = 1, 2), Aj (il) is the random effect of the jth sow on the ith treatment of the lth litter origin (l = 1, . . . , 10), βk is the effect of the kth time interval, (αβ)ik is the interaction between treatment and time interval, Bl is the random effect of the lth litter origin, εijkl is the residual for the jth sow on the ith treatment of the lth litter origin at the kth time interval. The random effects are normally distributed with mean equal to zero and constant variance Aj (il) ∼ N(0, σA2 ), Bl ∼ N(0, σB2 ), εijkl ∼ N(0, σ 2 ). The random effects are assumed to be independent of each other. The covariance between measurements at different time intervals (k) within the same sow was allowed to vary according to an autoreggresive (order  1) structure: Cov(Yijkm (t), Yijkm (t  )) = σ 2 ρt −t . Degrees of freedom were calculated using Satterthwaites approximation (Littell et al., 1996). Comparison of time intervals was made using contrasts and t-tests. For every hour separately (Hours 0–7) the relationship between the maternal responsiveness index or square root transformed number of postural changes in the hour in question and the square root transformed accumulated number of live born piglets at the end of the hour in question was analysed using Pearson correlations. Prior to analysis the index and number of postural changes were corrected for treatment effects and effects of origin of litter.

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The average time piglets within a litter took from birth until they suckled for the first time was modelled using analysis of variance including treatment as a fixed effect and litter origin of the sow as a random effect.

3. Results 3.1. Maternal responsiveness index Analysis of the data from all 24 h after farrowing showed a significant effect of treatment on the index, indicating that overall, the index was higher for the treatment sows compared to the control sows (F1,22 = 16.5, P < 0.0005) (Fig. 2). In addition, there was a significant effect of time interval (F11,73 = 2.0, P = 0.04) (Fig. 2), whereas there was no interaction between treatment and time intervals (F11,74 = 1.0, NS). Contrast between time interval 1 (0–2 h pp) and the mean across time intervals 2–4 (2–8 h pp) also revealed that the index was significantly higher during interval 1 (0–2 h pp) compared to the next three intervals (2–8 h pp) (t1,116 = 4.0, P < 0.0001). Time interval 1 (0–2 h pp) was also significantly higher than the mean of intervals 5–12 (8–24 h pp) (t1,53 = 2.2, P = 0.03), whereas the mean of intervals 5–12 (8–24 h pp) was significantly higher than the mean of intervals 2–4 (2–8 h pp) (t1,35.2 = −2.1, P = 0.05). Estimates for the differences are shown in Table 2.

Fig. 2. Least square estimates with standard errors as Y error bars for the maternal responsiveness index during the first 24 h postpartum for the two treatments. Estimates are calculated based on model 1. Table 2 Estimates with standard errors of the differences in maternal responsiveness index (MRI), square root transformed number of postural changes and mean heart rate between various time intervals Interval 0–2 h pp vs. 8–24 h pp 0–2 h pp vs. 2–8 h pp 2–8 h pp vs. 8–24 h pp ∗

MRI

Sqrt(postural changes) 0.15∗

0.33 ± 0.56 ± 0.14∗ −0.23 ± 11∗

0.42∗

1.09 ± 2.1 ± 0.43∗ −1.0 ± 0.30∗

Indicates that estimates from the two intervals differed significantly (P < 0.05).

Heart rate 21.4 ± 3.2∗ 10.4 ± 2.1∗ 11.0 ± 2.6∗

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Table 3 Correlations of maternal responsiveness index (MRI) and frequency of posture changes with the square root transformed accumulated number of liveborn piglets during the first 8 h postpartum Hours postpartum

MRI

Posture changes

1 2 3 4 5 6 7 8

−0.11, P = 0.7 −0.53, P = 0.04 −0.10, P = 0.7 −0.57, P = 0.03 −0.34, P = 0.2 −0.06, P = 0.8 −0.11, P = 0.7 −0.24, P = 0.42

−0.27, P = 0.3 −0.45, P = 0.05 −0.32, P = 0.2 −0.46, P = 0.05 −0.42, P = 0.08 −0.35, P = 0.16 −0.31, P = 0.2 0.29, P = 0.2

There was a negative correlation between the index and the accumulated number of born piglets within each of the first 8 h. However, significant correlations were only found during Hours 2 and 4 (Table 3). 3.2. Postural changes The sows were lying in lateral recumbency during 78 ± 10% of the 24 h. Analysis of the data from all 24 h after farrowing showed no significant effect of treatment on the number of postural changes (F1,48.6 = 0.40, NS), whereas there was a significant effect of time interval (F11,117 = 3.3, P = 0.0007) (Fig. 3). There was no interaction between treatment and time intervals (F11,110 = 0.8, NS). The litter origin was removed from the model since the estimate was close to zero. Contrast between time interval 1 (0–2 h pp) and the mean across time intervals 2–4 (2–8 h pp) revealed that the number of postural changes was significantly higher during time interval 1 (0–2 h pp) compared to the next three time intervals (2–8 h pp) (t1,192 = 4.8, P < 0.0001) and compared to time interval 5–12 (8–24 h pp) (t1,150 = 2.6,

Fig. 3. Back transformed least square estimates with standard errors as Y error bars for the number of postural changes during the first 24 h postpartum for the two treatments. Estimates are calculated based on model 1.

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P = 0.01). In addition, the number of postural changes was significantly lower during time interval 2–4 (2–8 h pp) compared to time interval 5–12 (8–24 h pp) (t1,84.5 = −3.3, P = 0.002). Estimates for the differences are shown in Table 2. There was a negative correlation between the square root transformed number of postural changes and the square root transformed accumulated number of born piglets within the first 8 h pp. However, the correlations were only significant during Hours 2 and 4 (Table 3). 3.3. Time to first suckling There was a significant effect of treatment on the average time piglets within a litter took to suckle the first time. Piglets from treatment sows took significantly longer to suckle for the first time than piglets from control sows (60 ± 7 min versus 38 ± 7 min) (F1,10 = 5.0, P < 0.05). 3.4. Heart rate Analysis of the data including all 24 h after farrowing showed no significant effect of treatment on the overall mean heart rate (F1,10.8 = 1.5, NS) or mean heart rate during standing, sitting, lying laterally, lying sternally or rooting. There was also no significant effect of treatment on heart rates during person presence, suckling bouts or piglet expulsion. There was a significant effect of time interval (F11,95 = 4.8, P < 0.0001) on mean heart rate. There was no interaction between treatment and time intervals (F11,95.1 = 0.8, NS). Estimates for the 12 time intervals for each treatment are shown in Fig. 4. Contrast between time interval 1 (0–2 h pp) and the means across time intervals 2–4 (2–8 h pp) and time intervals 5–12 (8–24 h pp) revealed that the mean heart rate was significantly higher during interval 1 compared to the next three intervals (t1,135 = 4.9, P < 0.0001) and the last eight intervals (t1,47 = 6.7, P < 0.0001). The mean of intervals 5–12 (8–24 h pp) was

Fig. 4. Least square estimates with standard errors as Y error bars for the mean heart rate during the first 24 h postpartum for the two treatments. Estimates are calculated based on model 1.

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significantly lower than the mean of intervals 2–4 (2–8 h pp) (t1,49 = 4.3, P < 0.0001). Estimates for the differences are shown in Table 2. The estimates shown in Fig. 4 suggested that mean heart rate gradually declined from 0 to 8 h pp after which it remained level. In order to test this, data was reanalysed for time interval 1–4 (0–8 h pp) and for time interval 5–12 (8–24 h pp) using model 1 with the exception that time intervals were used as a covariate in the analysis. When analysing data from the first four time intervals (0–8 h pp), a negative regression coefficient for time on the mean heart rate was revealed (F1,52.2 = 33.8, P < 0.0001) with a slope estimated to −5.1 ± 0.9 per 2 h. There were no differences in the slope or intercept between the two treatments. During the last eight time intervals (8–24 h pp) the regression coefficient for mean heart rate was not significantly different from zero (F1,44 = 0.8, NS).

4. Discussion 4.1. Timing of sow responsiveness, postural changes and heart rate In general, the sows were most responsive to their piglets, changed posture more and had higher heart rates during the first 2 h of parturition. Responsiveness and frequency of postural changes decreased rapidly during the first 2 h pp, then remained level until 8 h pp after which it increased again. Furthermore, within the first 8 h postpartum responsiveness and mobility decreased the more piglets the sow had. The temporal pattern of reactivity corresponds well with previous descriptions of sow postures and investigatory behaviour of piglets during the initial stage of parturition in semi-natural environments (Jensen, 1986; Petersen et al., 1990) and in experimental studies of loose housed sows (Jones, 1966; Jarvis et al., 1999). The results reported by Jarvis et al. (1999) indicate that maternal responsiveness increases at some point between the sixth hour after onset of farrowing and the day after farrowing, but no observations were carried out in the intervening time. Similarly, when piglet scream play-back tests were used to test sow responsiveness to piglet screams, the sows were also quite reactive on Days 1–3 (Hutson et al., 1991, 1992; Herskin et al., 1998; Thodberg et al., 2002). Our data suggest that immobility and maternal responsiveness again increase about 8 h postpartum. As indicated by Figs. 2 and 3 there may also be a slight, however not significant, decline around Hour 14 probably reflecting normal resting behaviour after a period with high mobility. From an evolutionary point of view, it makes sense if a timing of postparturient behaviours has developed, so that the increase in maternal responsiveness coincides with the postpartum increase in activity, which in our study seemed to occur from about 8–10 h postpartum, and perhaps also with the onset of a more synchronised, established nursing pattern characterised by discrete milk ejections. As long as farrowing is still in progress and as long as colostrum is constantly available, the most important factor for piglet survival is secure access to the udder. Therefore, the optimal behaviour for the sow in order to safeguard her offspring would be to remain lying in lateral recumbency. However, when colostrum ejections begin to occur at regular intervals, the piglets should have ingested considerable amounts of colostrum and have good energy reserves. Thus, the sow can begin to move about as long as she remains close to the piglets and nurses them at regular intervals. At this point, one of the most important factors for piglet survival is likely to be that the

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sow is responsive, particularly when she stands/walks in the nest, lies or rolls over and that she actively cares for her piglets. Discrete milk ejections and synchronised suckling begin to occur within the first day postpartum. Some authors report that it happens as soon as between 5 and 11 h postpartum (Lewis and Hurnik, 1985; Castrén et al., 1993b; De Passillé and Rushen, 1989), whereas others report it as happening as late as 20–29 h postpartum (Herskin et al., 1999). The variations are probably due to differences in definitions of cyclic nursing, the shift being very gradual, making it difficult to determine (De Passillé and Rushen, 1989) and finally, due to the fact that the timing can be affected by farrowing environment (Herskin et al., 1999). Non-systematic observations made when sampling colostrum (unpublished data for the larger study of which this experiment was part) indicated that in our experiment, the shift occurred sometime around 8–12 h postpartum. Thus, in our study, maternal responsiveness may very well have been related to the timing of postpartum activity or postpartum synchronised nursing. This is an aspect that would be interesting to investigate further in order to completely understand the timing of maternal responsiveness. The temporal pattern of mean heart rate only reflects the pattern of posture changing, to some extent (see Figs. 3 and 4). Heart rate declines slowly after the birth of the first piglet, whereas responsiveness and posture-changing behaviour falls sharply. This illustrates that the physical process of parturition itself, coupled with the hormonal elevations that have been described at this time (Jarvis et al., 1998), is probably causing heart rate to remain elevated even though the overt physical movement associated with posture-changing has decreased. 4.2. Effects of feed-back from a farrowing nest Feed-back from a farrowing nest affected maternal responsiveness, indicated by a consistently higher index in sows that were not allowed feed-back from a nest than in sows that were allowed to keep their nest. Also the average time piglets within a litter took to suckle the first time was affected, in that piglets born by sows that were not allowed feed-back from a nest took longer to suckle for the first time than piglets born by sows that were allowed to keep the nest. The timing of the changes in maternal responsiveness was not affected. In the treatment sows, the index remained positive throughout the experimental period, but in the control sows the index was positive during the first 2 h interval only and then became and remained negative, which is very similar to the maternal responsiveness index reported by Jarvis et al. (1999) in sows with parturitions of normal length (<4 h). The level of the index in our experiment was somewhat lower in the control sows and somewhat higher in the treatment sows than that reported by Jarvis et al. (1999). This may be explained by the differences in farrowing environment and experimental animals as Jarvis et al. (1999) used a straw bedded pen for all animals and Large White × Landrace multiparous sows. The finding that primiparous sows reacted faster than multiparous sows to piglet screams (Hutson et al., 1992), suggests that age, experience or mobility may affect sow responsiveness. It has previously been shown that environmental factors can also affect sow responsiveness. Herskin et al. (1998) showed that provision of nest materials to loose housed sows increased the response to piglet screams 1–3-day postpartum. Similarly, sows in crates with no nest materials were less responsive to piglet screams 1–3-day postpartum (Cronin et al., 1996; Thodberg et al., 2002) and investigated and vocalised less to piglets on Day 1 (Cronin et al., 1996) than sows in pens with nest materials. Sows respond more to auditory stimuli

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from piglets than to tactile or visual stimuli except when the piglet is near the sow’s head (Hutson et al., 1991) and therefore, maternal responsiveness as measured in our study cannot be directly compared with maternal responsiveness as measured by various auditory tests. Nonetheless, the results of our study clearly show that the farrowing environment affects sow responsiveness also during parturition and the immediate postpartum hours. In accordance with the reversed adaptive relationships during parturition compared to 24 h postpartum these effects were opposite to those previously reported (Cronin et al., 1996; Herskin et al., 1998), i.e. the suboptimal environment leads to higher responsiveness during and immediately after farrowing. The reason for the increased maternal responsiveness in treatment sows in our experiment may be that the lack of feed-back from a nest constituted an acute stressor that interfered with hormonal regulation of the maternal responsiveness. Oxytocin is important in the regulation of maternal interaction and attachment to the offspring in the rat (Pedersen and Prange, 1979; Pedersen et al., 1982; Fahrbach et al., 1985), sheep (Kendrick et al., 1987), humans (Nissen et al., 1998) and probably also in the pig (Jarvis et al., 1999). According to Uvnäs-Moberg et al. (2001), oxytocin induces adaptations consistent with an antistress-like pattern and promotes behaviours characterised by calmness and reduced levels of anxiety. In the pig, opioids are secreted in situations characterised by acute stress (Rushen and Ladewig, 1991; Rushen et al., 1993). During parturition it is part of the normal physiological changes associated with farrowing that plasma concentrations of opioids increase (Jarvis et al., 1998), but the concentrations increase further if the sow is acutely stressed, e.g. being moved in the initial stage of parturition resulted in opioid mediated inhibition of oxytocin (Lawrence et al., 1992). It therefore seems possible that the treatment sows in our experiment had increased opioid secretion due to the lack of feed-back from a nest and that oxytocin secretion was inhibited resulting in behaviour that was less calm and more responsive. On the other hand, Jarvis et al. (1999) showed that administration of naloxone, an opioid antagonist, increased standing, lying ventrally and posture changes and tended to increase maternal responsiveness during parturition and the first few hours after. Thus, in this experiment high maternal responsiveness was associated with low levels of opioids and probably with high levels of oxytocin which is in contrast to what would be expected according to previous descriptions of oxytocin as an antistress hormone promoting behaviours characterised by calmness and reduced levels of anxiety (Uvnäs-Moberg et al., 2001). However, the associations between oxytocin and maternal behaviour are not completely understood and they are very complex. The relationship between maternal responsiveness and oxytocin in the pig has never been studied directly, and needs to be further investigated in order to fully understand the hormonal regulation of maternal behaviour during parturition. In our experiment, treatment did not affect the frequency of postural changes as it did maternal responsiveness. The reason may be that the frequency of postural changes is a coarser measurement, which occurs much more rarely than sow piglet interactions. Standard errors of the estimates for postural changes were somewhat larger than standard error for maternal responsiveness indicating less precise estimates for the former. This may explain why we were not able to demonstrate any differences between treatment in the number of postural changes whereas we were for the maternal responsiveness. As suggested by Jarvis et al. (1999) immobility and low maternal responsiveness during parturition and the immediate postpartum time probably constitute good maternal behaviour

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as it decreases the risk of crushing and trampling and gives the piglets access to the udder and the warmth of being close to the sow. The contention that access to the teats and colostrum can be impaired in sows with high maternal responsiveness during parturition was supported by our data as piglets born by sows that had had their nest removed took almost twice as long to suckle the first time as piglets born by sows that were allowed to keep the nest. With increased time from birth to first suckling the immunoglobulin level of piglets is reduced (Pejsak et al., 1987/1988; Klobasa et al., 1990) and early initiation of suckling seems to be of great importance for piglet health (Tyler et al., 1990; De Passillé and Rushen, 1989) and survival (Bünger, 1985; Tuchscherer et al., 2000). In addition, Ahlström (1997) found that gilts, which were more responsive towards their piglets in the early stages of farrowing were more likely to go on to savage their piglets. Thus, savaging (and perhaps other types of poor periparturient maternal care) may be associated with increased responsiveness to piglets although we could not demonstrate this in our study as savaging is a relatively rare behaviour and it did not occur in our experiment at all. 4.3. Conclusion and perspectives Our hypothesis that farrowing environment could affect parturient and postparturient maternal responsiveness and piglets’ chances of getting early access to colostrum was confirmed as sows which could not achieve feed-back from a nest were more responsive to their piglets, although they were not otherwise more active nor had elevated heart rates, and piglets from these sows took longer time to suckle the first time. This may help to explain the increased piglet mortality found in studies where sows without bedding have been compared to sows with bedding (e.g. Herskin et al., 1998) and the still unsolved problem of piglet mortality in commercial pig production. The findings emphasise the importance of a proper farrowing environment and the opportunity to construct a nest, both in crated sows but in particular in loose housed sows, where the sow is not surrounded by pen features constructed to protect the piglets and their survival and viability depend greatly on the maternal behaviour of the sow.

Acknowledgements We thank Kith Skovgaard and Birthe Houbak, National Institute of Agricultural Sciences, Department of Animal Health and Welfare, and the staff at the intensive animal unit at Research Centre Foulum for participating in data collection and for care of the animals. The study was funded by Cepros, grant no. Cep97-14.

References Ahlström, S., 1997. Assessing maternal behaviour in the domestic pig. M.Sc. Thesis. University of Edinburgh, UK. Arey, D.S., Petchey, A.M., Fowler, V.R., 1991. The periparturient behaviour of sows in enriched pens and the effect of pre-formed nests. Appl. Anim. Behav. Sci. 31, 61–68.

122

L.J. Pedersen et al. / Applied Animal Behaviour Science 83 (2003) 109–124

Blackshaw, J.K., 1983. Prostaglandin-F-2-alpha induced nest building behaviour in the non-pregnant sow, and some welfare considerations. Int. J. Stud. Anim. Prob. 4, 299–304. Bøe, K., 1994. Variation in maternal behaviour and production of sows in integrated loose housing systems in Norway. Appl. Anim. Behav. Sci. 41, 53–62. Boulton, M.I., Wickens, A., Goode, J.A., Gilbert, C.L., 1997a. Prostaglandin F2-alpha-induced nest-building in pseudopregnant pigs. I. Effects of environment on behaviour and cortisol secretion. Physiol. Behav. 62, 1071–1078. Boulton, M.I., Wickens, A., Goode, J.A., Gilbert, C.L., 1997b. Prostaglandin F2-alpha-induced nest-building in pseudopregnant pigs. II. Space restriction stress does not influence secretion of oxytocin, prolactin, oestradiol or progesterone. Physiol. Behav. 62, 1079–1085. Bünger, B., 1985. Ethological method for assessing the vitality of newborn piglets. Monatshefte fur Veterinarmedizin 40 (15), 519–524. Castrén, H., Algers, B., de Passillé, A.-M., Rushen, J., Uvnäs-Moberg, K., 1993a. Periparturient variation in progesterone, prolactin, oxytocin and somatostatin in relation to nest building in sows. Appl. Anim. Behav. Sci. 38, 91–102. Castrén, H.R., Algers, B., de Passillé, A.M., Rushen, J., Uvnäs-Moberg, K., 1993b. Early milk ejection prolonged parturition and periparturient oxytocin release in the pig. Anim. Prod. 57, 465–471. Cronin, G.M., Simpson, G.J., Hemsworth, P.H., 1996. The effects of the gestation and farrowing environment on sow and piglet behaviour and piglet survival and growth in early lactation. Appl. Anim. Behav. Sci. 46, 175–192. Cronin, G.M., Lefébure, B., McClintock, S., 2000. A comparison of piglet production and survival in the Werribee Farrowing Pen and conventional farrowing crates at a commercial farm. Austr. J. Exp. Agric. 40, 17–23. Damm, B.I., Vestergaard, K.S., Schrøder-Petersen, D.L., Ladewig, J., 2000a. The effects of branches on prepartum nest building in gilts with access to straw. Appl. Anim. Behav. Sci. 69, 113–124. Damm, B.I., Pedersen, L.J., Ladewig, J., Jensen, K.H., 2000b. A simplified technique for non-surgical catheterization of the vena cava cranialis in pigs and an evaluation of the method. Lab. Anim. 34, 182–188. Damm, B.I., Friggens, N.C., Nielsen, J., Ingvartsen, K.L., Pedersen, L.J., 2002. Factors affecting the transfer of porcine parvovirus antibodies from sow to piglets, J. Vet. Med. A 49, 487–495. Damm, B.I., Pedersen, L.J., Marchant-Forde, J.N., Gilbert, C.L., 2003. Does feed-back from a nest affect periparturient behaviour, heart rate and circulatory oxytocin, cortisol, oestradiol-17␤ in gilts? Appl. Anim. Behav. Sci., in press. De Passillé, A.M., Rushen, J., 1989. Suckling and teat disputes by neonatal piglets. Appl. Anim. Behav. Sci. 22, 22–38. Dyck, G.W., Swierstra, E.E., 1987. Causes of piglet death from birth to weaning. Can. J. Anim. Sci. 67, 543–547. Edwards, A., Malkin, S.J., Spechter, H.H., 1986. An analysis of piglet mortality with behavioural observations. Anim. Prod. 42, 470. English, P.R., Smith, W.J., 1975. Some causes of death in neonatal piglets. Vet. Ann. 15, 95–104. Fahrbach, S.E., Morrell, J.I., Pfaff, D.W., 1985. Possible role for endogenous oxytocin in estrogen-facilitated maternal behaviour in rats. Neuroendocrinology 40, 526–532. Fraser, D., 1990. Behavioural aspects on piglet survival. J. Reprod. Fert. Suppl. 40, 355–370. Herskin, M.S., Jensen, K.H., Thodberg, K., 1998. Influence of environmental stimuli on maternal behaviour related to bonding, reactivity and crushing of piglets in domestic sows. Appl. Anim. Behav. Sci. 58, 241–254. Herskin, M.S., Jensen, K.H., Thodberg, K., 1999. Influence of environmental stimuli on nursing and suckling behaviour in domestic sows and piglets. Anim. Sci. 68, 27–34. Hutson, G.D., Wilkinson, J.K.L., Luxford, B.G., 1991. The response of lactating sows to tactile, visual and auditory stimuli associated with a model piglet. Appl. Anim. Behav. Sci. 32, 129–137. Hutson, G.D., Argent, M.F., Dickenson, L.G., Luxford, B.G., 1992. Influence of parity and time since parturition on responsiveness of sows to a piglet distress call. Appl. Anim. Behav. Sci. 34, 303–313. Jarvis, S., Lawrence, A.B., McLean, K.A., Chirnside, J., Deans, L.A., Calvert, S.K., 1998. The effect of environment on plasma cortisol and ␤-endorphin in the parturient pig and the involvement of endogenous opioids. Anim. Reprod. Sci. 52, 139–151. Jarvis, S., McLean, K., Calvert, S.K., Deans, L.A., Chirnside, J., Lawrence, A.B., 1999. The responsiveness of sows to their piglets in relation to the length of parturition and the involvement of endogenous opioids. Appl. Anim. Behav. Sci. 63, 195–207.

L.J. Pedersen et al. / Applied Animal Behaviour Science 83 (2003) 109–124

123

Jensen, P., 1986. Observations on the maternal behaviour of free-ranging domestic pigs. Appl. Anim. Behav. Sci. 16, 131–142. Jensen, P., 1993. Nest building in domestic sows: the role of external stimuli. Anim. Behav. 45, 351–358. Jones, J.E.T., 1966. Observations on parturition in the sow: Part II: The parturient and postparturient phases. Br. Vet. J. 122, 471–478. Just, A., 1982. The net energy value of balanced diets for growing pigs. Livest. Prod. Sci. 8, 541–555. Kendrick, K., Keverne, E.B., Baldwin, B.A., 1987. Intracerebroventricular oxytocin stimulates maternal behaviour in sheep. Neuroendocrinology 46, 56–61. Klobasa, F., Habe, F., Werhahn, E., 1990. Untersuchungen über die Absorption der kolostralen Immunglobuline bei neugeborenen Ferkeln. I. Mitteilung: Einfluss der Zeit von der Geburt bis zur ersten Nahrungsaufnahme. Berl. Münch. Tierärtzl. Wschr. 103, 335–340. Lawrence, A.B., Petherick, J.C., McLean, K., Gilbert, C.L., Chapman, C., Russell, J.A., 1992. Naloxone prevents interruption of parturition and increases plasma oxytocin following environmental disturbance in parturient sows. Physiol. Behav. 52, 917–923. Lewis, N.J., Hurnik, J.F., 1985. The development of nursing behaviour in swine. Appl. Anim. Behav. Sci. 14, 225–232. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS System for Mixed Models. SAS Institute Inc., USA, p. 633. Marchant, J.N., Mendl, M.T., Rudd, A.R., Broom, D.M., 1995. The effect of agonistic interactions on heart rate of group-housed sows. Appl. Anim. Behav. Sci. 46, 49–56. Marchant, J.N., Rudd, A.R., Mendl, M.T., Broom, D.M., Meredith, M.J., Corning, S., Simmins, P.H., 2000. The timing and causes of piglet mortality in alternative and conventional farrowing systems. Vet. Rec. 147, 209–214. Marchant, J.N., Broom, D.M., Corning, S., 2001. The influence of sow behaviour on piglet mortality due to crushing in an open farrowing system. Anim. Sci. 72, 19–28. Nissen, E., Gustavsson, P., Widström, A.-M., Uvnäs-Moberg, K., 1998. Oxytocin, prolactin, milk production and their relation with personality traits in women after vaginal delivery and sectio caesarea. J. Psychosom. Obst. Gynecol. 19, 49–58. Pedersen, C.A., Prange, A.J., 1979. Induction of maternal behaviour in virgin rats after i.c.v. administration of oxytocin. Proc. Natl. Acad. Sci. U.S.A. 76, 6661–6665. Pedersen, C.A., Ascher, J.A., Monroe, Y.L., Prange, A.J., 1982. Oxytocin induces maternal behaviour in virgin female rats. Science 216, 648–650. Pedersen, B.K., Jensen, K.H., Nielsen, N.P., 1998. Farrowing systems for the future. In: Proceedings of the 15th IPVS Congress, Birmingham, England, 5–9 July 1998, pp. 273–280. Pejsak, Z., Deptula, W., Tarasiuk, K., 1987/1988: Biochemical parameters and humoral immunity indices in piglets depending on the time of colostrum intake. Bull. Vet. Inst. Pulawy 30–31, vols. 1–4, pp. 59–68. Petersen, V., Récen, B., Vestergaard, K., 1990. Behaviour of sows and piglets during farrowing under free-range conditions. Appl. Anim. Behav. Sci. 26, 169–179. Rushen, J., Ladewig, J., 1991. Stress-induced hypoalgesia and opioid inhibition of pigs’ responses to restraint. Physiol. Behav. 50, 1093–1096. Rushen, J., Schwarze, N., Ladewig, J., Foxcroft, G., 1993. Opioid modulation of the effects of repeated stress on ACTH, cortisol, prolactin, and growth hormone in pigs. Physiol. Behav. 53, 923–928. Schmid, H., 1992. Abferkelbuchten: ein neues Konzept. FAT-berichte Nr. 417, p. 8. Schmid, H., 1993. Ethological design of a practicable farrowing pen. In: Proceedings of the International Congress on Applied Ethology, Berlin, 1993, pp. 238–242. Thodberg, K., Jensen, K.H., Herskin, M.S., Jørgensen, E., 1999. Influence of environmental stimuli on nest building and farrowing behaviour in domestic sows. Appl. Anim. Behav. Sci. 63, 131–144. Thodberg, K., Jensen, K.H., Herskin, M., 2002. Nursing behaviour, post partum activity and reactivity in sows: effects of farrowing environment, previous experience and temperament. Appl. Anim. Behav. Sci. 77, 53–76. Tuchscherer, M., Puppe, B., Tuchscherer, A., Tiemann, U., 2000. Early identification of neonates at risk: traits of newborn piglets with respect to survival. Theriogenology 54 (3), 371–388. Tyler, J.W., Cullor, J.S., Thurmond, M.C., Douglas, V.L., Parker, K.M., 1990. Immunologic factors related to survival and performance in neonatal swine. Am. J. Vet. Res. 51 (1), 1400–1406. Uvnäs-Moberg, K., Johansson, B., Lupoli, B., Svennersten-Sjaunja, K., 2001. Oxytocin facilitates behavioural, metabolic and physiological adaptations during lactation. Appl. Anim. Behav. Sci. 72, 225–234.

124

L.J. Pedersen et al. / Applied Animal Behaviour Science 83 (2003) 109–124

Weary, D.M., Pajor, E.A., Thompson, B.K., Fraser, D., 1996. The relationship between piglet body condition and proximity to the sow: a trade-off between feeding and the risk of mortality by maternal crushing? Anim. Behav. 51, 619–624. Wechsler, B., Hegglin, D., 1997. Individual differences in the behaviour of sows at the nest-site and the crushing of piglets. Appl. Anim. Behav. Sci. 51, 39–49. Widowski, T.M., Curtis, S.E., Dziuk, P.J., Wagner, W.C., Sherwood, O.D., 1990. Behavioural and endocrine responses of sows to prostaglandin F-2-alpha and cloprostenol. Biol. Reprod. 42 (2), 290–297.