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Cross-suckling and nursing synchronisation in group housed lactating sows
Applied Animal Behaviour Science 75 (2001) 17±32
Cross-suckling and nursing synchronisation in group housed lactating sows J. MaletõÂnskaÂ*, M. SÏpinka Ethology Group, Research Institute of Animal Production, Pratelstvi 815, 10400 Prague, UhrÏÂõneÏves, Czech Republic Accepted 20 July 2001
Abstract Group housing systems for lactating sows with piglets enable the animals to behave more naturally than traditional restrictive systems. However, piglets may occasionally suckle from other sows than their mother. The in¯uence of litter size, age of the litter, mother parity, piglet gender and, in particular, nursing synchronisation, on the following: the occurrence of cross-suckling (presence of alien piglets at the udder during milk ejection); cross-suckling strategies; and piglets' success at achieving nursings, was investigated. The observations were carried out on six stable groups of three or four unrelated sows with their piglets between 19 and 32 days postpartum. Crosssuckling was frequent (occurred in 29% of all suckling events). The main determinant of crosssuckling was litter size. Piglets from larger litters missed nursings of their mothers more often (r s 0:72; n 22; P < 0:001) and performed cross-suckling more often than piglets from smaller litters (r s 0:54; n 22; P < 0:05). Piglets, who were observed suckling only alien sows, belonged to larger litters than piglets suckling only their own mother (Wilcoxon signed rank T-test; n 6; P < 0:05). Sows with larger litters were preferred targets for cross-suckling (Wilcoxon signed rank T-test; n 78; P < 0:001). Piglets from older litters cross-suckled more often than piglets from younger litters (r s 0:50; n 22; P < 0:05). Nursing synchronisation (sows nursing within one minute of each other) was high at 82%. Sows nursing immediately after other sows attracted less cross-suckling. The higher the number of sows which had nursed just before a focal sow, the fewer alien piglets were then present at her nursing (r s 0:35; n 14; Cochran± Mantel±Haenszel (CMH) statistic; P < 0:05). Piglets belonging to a speci®c litter were less likely to cross-suckle at an alien sow if her nursing was preceded by a nursing of the mother of that litter (CMH statistic for 28 piglets; P < 0:01). Permanently cross-suckling, occasionally cross-suckling and faithful piglets achieved a similar number of suckling events indicating that these strategies may be equally successful in a stabilised multi-suckling situation. Mother parity and piglets' gender had no effect on cross-suckling. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Pig; Nursing; Cross-suckling; Suckling strategies; Synchronisation *
Corresponding author. Tel.: 420-2-67710713; fax: 420-2-67710779. E-mail address: [email protected] (J. MaletõÂnskaÂ). 0168-1591/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 1 ) 0 0 1 7 8 - 2
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1. Introduction In commercial pig production, lactating sows are often kept in narrow farrowing crates without any bedding. This housing system limits the movement of the sow and prevents her from performing several natural behavioural patterns such as rooting, resting and selfregulation of contact with her piglets. Group housing or multi-suckling systems allow these behaviours to be performed, and hence, can enhance some aspects of sow welfare (Jensen, 1986; Algers et al., 1991; Wechsler et al., 1991). Often, lactating sows in these systems are kept in individual crates for 1±2 weeks after parturition and then 3±15 of them are moved together with their litters, into a common straw-bedded pen. However, such systems have problems of their own, such as cross-suckling. Cross-suckling (where young mammals suckle at dams other than their mother) (also called allo-suckling) has been observed in many wild, feral and domestic animals that live in groups (Riedman, 1982; Packer et al., 1992). Within pigs, cross-suckling has been reported in the wart-hog (Phacochoerus aethiopicus) (FraÈdrich, 1965), the wild boar (Sus scrofa) (Mauget, 1981), and in both free-ranging (Newberry and Wood-Gush, 1985) and indoor housed domestic pigs (WuÈlbers-Mindermann, 1992; Brodmann and Wechsler, 1994; Puppe and Tuchscherer, 1995) at various rates. The cross-suckling in the commercial multi-suckling systems deserves special attention because of its unwanted consequences. Cross-suckling may result in ®ghting among piglets, disruption of previously established teat orders (Andersson and AndreÂasson, 1992; Pedersen et al., 1998; Wattanakul et al., 1997, 1998b), a higher proportion of missed nursings and nursings without milk ejection (Arey and Sancha, 1996; Wattanakul et al., 1998a; Pedersen et al., 1998) and, as a result, reduced milk intake and weight gain (Puppe and Tuchscherer, 1995; WuÈlbers-Mindermann, 1992). Both the cross-suckling piglets and those, which remain faithful to their mothers, may be affected (Puppe and Tuchscherer, 1995; Pedersen et al., 1998). Indeed, it remains unclear whether cross-suckling piglets achieve a lower, equal or higher number of successful sucklings than their faithful siblings. Although it has been documented that cross-suckling brings some disorder into multi-suckling groups, it has not yet been established whether, from an individual piglet's point of view, cross-suckling is a poorer, as good as, or better, strategy for obtaining more milk than remaining faithful. Several factors probably affect the incidence of cross-suckling. First, in groups of between 5 and 11 sows, the occurrence of cross-suckling declines with the decreasing number of sows in group (Fraser and Broom, 1990; WuÈlbers-Mindermann, 1992). This may indicate that cross-suckling might be infrequent in very small groups, e.g. three to four sows. Indeed, incidence below or around 10% was reported in such small groups by GoÈtz et al. (1991), WuÈlbers-Mindermann (1992), Brodmann and Wechsler (1994) and Puppe and Tuchscherer (1995). Second, high levels of cross-suckling were observed in groups, which were composed of litters varying considerably in age (Braun and Jensen, 1988) and/or size (WuÈlbersMindermann, 1992; GoÈtz et al., 1991; Brodmann and Wechsler, 1994). Third, the incidence of cross-suckling may change during ontogeny. High levels of cross-suckling were observed for several days after grouping the sows and their litters into the common pen (Hatet et al., 1994; Wattanakul et al., 1997). A second peak may occur during the fourth week of lactation when the milk production of the sow starts to decline
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(Hartman et al., 1962; Burgerstaller, 1985; Jensen, 1988; WuÈlbers-Mindermann, 1992). Fourth, the incidence of cross-suckling may be in¯uenced by the parity of the dam. Older dams with more maternal experience may be more able to prevent cross-suckling, for instance, by better synchronising with other sows, not starting a nursing when there are alien piglets around, or by interrupting a nursing if there is too much ®ghting for teats. Finally, cross-suckling behaviour of piglets in a group-housing pen can be in¯uenced by the synchronisation of nursing bouts among sows (GoÈtz et al., 1991). This presumption is indirectly supported by the fact that the proportion of successful nursings (nursings with milk ejection) tends to be higher in groups with highly synchronised nursings (Bryant et al., 1983; Wattanakul et al., 1997). The effect of nursing synchronisation on cross-suckling has not yet been investigated in pigs. Cross-suckling piglets differ in whether they opportunistically switch between suckling several sows or focus on suckling a single alien dam, and in whether they still suckle at their own mother. Accordingly, cross-suckling piglets can be classi®ed into different categories, e.g. as habitual (or permanent) versus occasional (or opportunistic) cross-sucklers (Brodmann and Wechsler, 1994; Olsen et al., 1998; WuÈlbers-Mindermann, 1992). When assessing the effects of the various factors on cross-suckling, attention should be paid not only to the total number of cross-suckling piglets or cross-suckling events, but also to how the events are distributed among cross-sucklers using different strategies. The aim of this study was to assess the in¯uence of litter size, age of the litter, mother parity, piglet gender and, in particular, nursing synchronisation on the occurrence of crosssuckling, cross-suckling strategies, and piglets' success at achieving nursings in a commercial multi-suckling system with three to four sows per group. 2. Materials and methods 2.1. Animals and housing The observations were carried out in a commercial piggery in South Bohemia. Pregnant sows were housed in large (up to 30 animals) dynamic groups in straw-bedded pens. One week before parturition, sows were placed in individual farrowing crates. All piglets were ear-tattooed on the day of birth. When piglets were approximately 10 days old (median) (minimum 6; ®rst quartile 9; third quartile 13; maximum 18) groups of three or four lactating sows and their litters were formed. Each group was housed in a pen measuring 9:4 m 4:5 m. The pen included a lying area covered with straw bedding (two®fth of the total area), a small shelter (120 cm 50 cm 50 cm) for piglets, a dunging area without bedding (one-®fth of the total area Ð the lowest part of the pen) and an elevated part for drinking and eating (two-®fth of the total area). The sows were fed a standard diet for lactating sows at 06.00 h and 15.00 h, piglets had free access to a feeder with a standard diet for early weaned piglets, which was located in an elevated part of the pen. Six groups of unrelated lactating sows (two groups of three sows and four groups of four sows) were observed. These groups included two Large White and 20 Landrace sows, ranging between ®rst and eighth (median fourth) lactation and their 207 piglets. Piglets were between 19 and 32 (median 24) days of age during the observations and the intragroup
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difference in age ranged from 0 to 8 days (median 2 days) in individual groups. The average litter size was nine piglets (range: 3±13). 2.2. Observations Each group was observed on two consecutive days between 08.00 and 15.00 h. One hour before observations began all piglets in the group were marked on their backs using differently coloured numbers for each litter. We observed one sow at a time for four successful nursings. We recorded the beginning of nursing, success of nursing (with or without milk ejection) and identity of all suckling piglets. A piglet was considered to suckle at a given sow when it was present at her udder during the time of milk ejection. We also recorded which sows in the group nursed at the same time, immediately before or immediately after the nursing of a focal sow. During the observations, the following behavioural de®nitions were used:
beginning of nursing Ð at least two piglets started massage of teats of the focal sow and this sow started characteristic nursing grunting; end of milk ejection Ð piglets started switching between teats and/or massaging their teats after they have been suckling the teats rhythmically during milk ejection; sows nursing at the same time as the focal sow Ð sows which started to nurse during the interval between beginning of nursing and end of the milk ejection of the focal sow; sows nursing immediately before the focal sow Ð sows which started to nurse not more than 1 min before the focal sow; sows nursing immediately after the focal sow Ð sows which started to nurse at latest 1 min after the end of milk ejection of the focal sow.
2.3. Statistical analysis Two-tailed tests with a level of 0.05 were used, throughout the statistical analysis. 2.3.1. Quantification of cross-suckling Piglets were sorted into four (``suckling strategies'') categories according to their observed suckling/cross-suckling behaviour: those suckling only their own mother (SS_OWN), those suckling both the own mother and one or more alien sows (SS_OWN ALIEN), those suckling solely one alien sow (SS_1_ALIEN), and those suckling more than one alien dam, but not the own mother (SS_MORE_ALIENS). For certain analyses, we pooled the last two categories (SS_1_ALIEN; SS_MORE_ALIENS) into one larger, which included all piglets that had been observed to suckle at one or more alien dams, but not at the own mother (SS_ALIENS). The in¯uence of piglet gender was tested on the suckling/cross-suckling behaviour using a w2-test on a contingency table with sex and suckling strategies as sorting variables. In order to quantify the amount of cross-suckling, the following variables were derived:
number of alien piglets present at a nursing (ALIENPIGS) Ð the number of alien piglets suckling teats of the focal sow during the milk ejection (rhythmical suckling of teats);
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proportion of own piglets absenting in a nursing (%OWNABSENT) Ð the difference between the litter size of the focal sow and the number of her piglets participating in the given nursing during the milk ejection (rhythmical suckling of teats), divided by litter size; average number of cross-suckling acts by the own piglets (CROSSUCKS) Ð the total number of times the piglets from the focal litter were seen cross-suckling (during milk ejection) at other sows of the group, divided by litter size; total number of nursings achieved by a piglet (TOTSUCKS) Ð the total number of times a piglet was observed to suckle (i.e. was present at the udder during milk ejection), independent of whether it was at the own mother or another dam.
For variables relating to own piglets of the focal sows (%OWNABS, CROSSUCKS), we took proportional measures related to the focal sow's litter size because they expressed the tendency of an ``average'' piglet to be absent from the own mother and to suckle at alien sows. For of the variable ALIENPIGS, the absolute (not proportional) measure seemed more appropriate because it was unclear whether the litter size of the foster sow or that of the biological mother should be used for a proportional measure. For the purposes of correlation analyses under Sections 2.3.2 and 2.3.3. variables ALIENPIGS and %OWNABSENT were averaged across the four observed nursings. 2.3.2. Cross-suckling and litter size, piglet age and sow parity The factors affecting incidence of cross-suckling were analysed using correlation. The effect of group identity was removed using the SAS GLM procedure with the group identity as a single random factor. The residual values were used as replicates in the analyses. Hence, within-group associations between the analysed variables were assessed. Since some sets of the data departed from normality, Spearmann non-parametric correlations were applied. The effects of litter size, age of the litter and parity of the mother on the amount crosssuckling were assessed by correlating these three variables with ALIENPIGS, %OWNABSENT and CROSSUCKS, using the within-group residuals as described above. Second, whether litter size, age of the litter and parity of the mother in¯uenced the piglets' probability of becoming a cross-sucker was examined. Within each group, the mean litter size (or mean age, or mean mother's parity, respectively) between the piglets of the SS_OWN category, on one side, and the piglets of the SS_ALIENS and SS_OWN ALIEN categories, on the other was compared. A Wilcoxon signed rank ttest was used, for each of the comparisons, to test whether the resulting six differences (one per group) differed signi®cantly from zero. Third, whether the cross-suckling piglets preferred as their stepmothers sows with larger (or smaller) litters, relatively older (or younger) litters or mothers of higher (or lower) parity was investigated. For each cross-suckling piglet, the litter size of the target sow(s) (weighted average litter size in case of SS_MORE_ALIENS piglets) was subtracted from the average litter size of all sows in the group except for the own mother of the crosssuckling piglet. The Wilcoxon signed rank T-test tested, whether the resulting differences were centred around zero or not. Similar calculations were performed for litter age and parity of the target sow(s).
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2.3.3. Relationship between suckling of own and alien piglets Using the residual values after removing the group identity effect, correlations were performed on the variables ALIENPIGS, %OWNABSENT, and CROSSUCKS, in order to determine whether, within groups, the presence of alien cross-suckling piglets at a certain sow was related to the suckling/cross-suckling behaviour of the own piglets of that sow. 2.3.4. Cross-suckling and nursing synchronisation The role of between-sow nursing synchronisation in cross-suckling was examined in two ways. First, at the sow level, whether nursing in synchrony affected the probability that the focal sow will be a target of cross-suckling and the probability that her own piglets will be missing at the udder was investigated. The Cochran±Mantel±Haenszel (CMH) stratumadjusted correlation statistic of the SAS Proc Freq procedure (SAS Institute, 1999) was used. This statistic calculates the correlation coef®cient between two variables in each stratum of the data and then gives an overall statistic, which indicates whether there is a linear association between the two variables, after controlling for the third (stratifying) variable. In this case, the CMH statistic ®rst calculated, over the four observed nursings of each sow, the Spearmann correlation coef®cient between the number of other sows nursing in synchrony with the focal one in a given nursing and the variables ALIENPIGS and %OWNABSENT in the same nursing. Then overall statistics indicated whether these relationships were signi®cant over the whole sample of 22 sows, after controlling for the confounding effect of sow identity. This analysis was performed separately for the synchrony types ``mother sow nursed immediately before the focal sow'', ``mother sow nursed at the same time as the focal sow'' and ``mother sow nursed immediately after the focal sow''. Second, whether the individual piglets cross-suckled more (or less) often during those nursings in which their mother was synchronised with the other dams was investigated. A particular, piglet was focussed on and all nursings by other sows in the group than its mother (i.e. eight nursings in case of a three-sow group and 12 nursings in case of a foursow group) were sorted into a 2 2 contingency table. The rows in table were the nursing was synchronised between the sow in question and the mother of the focal piglets, or was not; and the columns were the focal piglet attended (as a cross-suckler) the nursing, or did not. This resulted in a strati®ed N 2 2 contingency table, where N is the number of evaluated piglets. The CMH General Association statistic (also called the stratum-adjusted Pearson w2; SAS Institute, 1999) was then applied, to test whether there was any relationship between the mother-focal sow synchrony in a speci®c nursing and the probability that a piglet would cross-suckle in that nursing. This analysis was done separately for the 46 SS_OWN ALIEN piglets and the 32 SS_ALIENS piglets, and also separately for the synchrony types ``mother sow nursed immediately before the focal sow'', ``mother sow nursed at the same time as the focal sow'' and ``mother sow nursed immediately after the focal sow'', resulting in a total of six runs of the analysis. 2.3.5. Cross-suckling and the number of achieved nursings The observed number of nursings achieved by each piglet was compared with expected values. As four successful nursings of each sow were observed, the expected number of achieved nursings under the latter condition (and under the assumption that piglets never
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miss nursings) would be four per piglet. For each of the six groups, the average observed number of nursings per piglet, was calculated, and four was deducted from it. The Wilcoxon signed rank T-test was applied to determine whether the resulting six differences were signi®cantly above or below zero. We were interested in how the total number of nursings in which piglets from a litter participated (TOTSUCKS) was affected by the litter size, age of the litter and parity of the mother; in other words, whether piglets from, for instance, an older litter (relative to other litters in the group) succeeded in getting milk more often. To examine this, the number of achieved nursings per piglet (TOTSUCKS) for each litter was calculated and then subjected to a SAS GLM procedure with group identity as a single random effect. The same SAS GLM procedure was applied to the variables ``litter size'', ``age of the litter'' and ``parity of the dam''. The residual values of TOTSUCKS were then correlated with the residuals of litter size, age of the litter and parity of the mother. Lastly whether there was any difference in the number of achieved nursings between cross-suckling piglets and those, which kept suckling at their mothers, was examined. Because some of the `strategies' had, by de®nition, an upper limit of nursings in which the piglets could have been observed (e.g. the maximum value of SS_OWN piglet was four nursings because each sow was observed during four nursings), only two comparisons were performed: strategy SS_OWN was compared with SS_1_ALIEN, and SS_OWN ALIEN with SS_MORE_ALIENS. For each litter for which it was possible, the difference between mean number of achieved nursings by piglets of the one strategy and the other was calculated. The Wilcoxon signed rank T-test was then used to determine whether there was a tendency for one or the other strategy to achieve more nursing. 3. Results 3.1. Occurrence of cross-suckling and cross-suckling strategies More than one-third of piglets cross-suckled at least once and some of them suckled exclusively alien sow/sows (Fig. 1). Eighteen out of the 22 litters contained at least one cross-suckler and 19 of 22 sows were at least once targets of cross-suckling. Of 798 participations of individual piglets in nursings, 234 (29.3%) occurred at a sow other than the piglet's biological mother (Fig. 2). Suckling behaviour of piglets was not in¯uenced by their gender. Female piglets belonged with 29.0, 11.1, 5.3 and 2.4% to strategies SS_OWN, SS_OWN ALIEN, SS_1_ALIEN and SS_MORE_ALIENS, while in male piglets, the percentages were 30.4, 11.1, 5.3 and 2.4% (w2 1 0:735; P > 0:1). Because of the very close match between female and male piglets, gender was subsequently disregarded in all further analyses. 3.2. Cross-suckling and litter size, piglet age and sow parity The correlations between the three measures of cross-suckling and the litter attributes, are displayed in Table 1. The correlations are based on residual values after removing the effect of group identity, so they re¯ect differences within groups. Piglets from large or older
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Fig. 1. Categorisation of piglets according to their suckling behaviour. SS_OWN piglets which suckled only their own mother; SS_OWN ALIEN piglets which suckled the own mother and one or more alien sows; SS_1_ALIEN piglets which suckled solely one alien sow; SS_MORE_ALIENS piglets which suckled more than one alien dam, but not the own mother; X piglets which were never seen to suckle during the observations.
Fig. 2. Distribution of all achieved sucklings in relation to piglets suckling strategies (n 798 sucklings). Suckling of faithful piglets (SS_OWN) at own mother (A); suckling of occasional cross-sucklers (SS_OWN ALIEN) at own mother (B); suckling of occasional cross-sucklers (SS_OWN ALIEN) at alien sows (C); sucklings of permanent cross-sucklers (SS_ALIENS) at alien sows (D).
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Table 1 Correlations (N 22) between litter size, litter age and sow's parity, on one side, and three measures of crosssuckling on the othera rs (ALIENPIGS) Litter size Litter age Sows' parity
0.31 0.33 0.36
rs (%OWNABS) ***
0.72 0.10 0.40
rs (CROSSUCK) 0.54** 0.50* 0.32
a
Spearmann correlation coefficients based on residual values after removing the effect of the group. P < 0:05. ** P < 0:01. *** P < 0:001. *
litters (relative to other litters in the group) missed nursings of their mother and performed cross-suckling more often. Next, the data were analysed from the point of view of the piglets' strategies looking at whether cross-suckling piglets originated from larger or older litters or from mothers of higher parity. Piglets which were observed to suckle only alien sows (SS_ALIENS) belonged to larger litters than piglets suckling only their own mother (SS_OWN; Wilcoxon signed rank T-test; n 6; P < 0:05). No other signi®cant differences were found between SS_OWN piglets, on one side, and SS_ALIENS or SS_OWN ALIEN piglets, on the other, in the size of their litters, their age or in the parity of their mother. Cross-suckling piglets preferred among the potential target sows those with larger litter size (Wilcoxon signed rank T-test; P < 0:001), and also those of higher parity (Wilcoxon signed rank T-test; P < 0:05). The age of the ``host'' litter had no in¯uence on the choice of target sows by the piglets (Wilcoxon signed rank T-test; P > 0:05). 3.3. Relationship between suckling of own and alien piglets There were signi®cant correlations between variables ALIENPIGS and %OWNABSENT (r s 0:46; n 22; P < 0:05) indicating that if a mother was a target of crosssuckling, her own piglets often absented from her nursings. Variables %OWNABSENT and CROSSUCKS were also correlated (r s 0:65; n 22; P < 0:01) showing that litters with high proportion of piglets missing at the mother's udder participated actively in the crosssuckling. However, no direct link was found between the number of alien piglets at a sow and the tendency of her own piglet to cross-suckle elsewhere Ð ALIENPIGS were not correlated with CROSSUCKS (r s 0:03; n 22; P > 0:1). 3.4. Cross-suckling and nursing synchronisation The mean rate of synchronisation was 0.818, i.e. when the focal sow was nursing, each other sow in the group had, on average, the probability of 82% that she will be nursing immediately before (26%), during the same time (35%), or immediately after (21%) the nursing of the focal sow.
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Table 2 Mean correlation coefficients (rs) between measures of nursing synchronisation and measures of cross-suckling, calculated as average values of Spearmann correlation coefficients obtained for each sow over her four observed nursingsa Type of synchronisation
ALIENPIGS
%OWNABS
Number of other sows nursing immediately before focal sow Number of other sows nursing at the same time as focal sow Number of other sows nursing immediately after focal sow
Mean rs: 0.35; n 14; CMH: 4.73* Mean rs: 0.21; n 16; CMH: 1.29 Mean rs: 0.01; n 13; CMH: 0.003
Mean rs: 0.43; n 14; CMH: 8.51** Mean rs: 0.17; n 18; CMH: 2.28 Mean rs: 0.07; n 15; CMH: 0.39
a
Significance based on CMH statistic. P < 0:05. ** P < 0:01. *
Table 2 shows the averages of correlation coef®cients between measures of nursing synchronisation and measures of cross-suckling (across the four observed nursings within each focal sow). The number of sows on which the CMH test was based varied, as the correlation coef®cient could not be calculated for some sows, e.g. because they had no own piglets missing in any of the four nursings. There were two signi®cant relationships. First, the higher the number of sows which nursed just before the focal sow, the less alien piglets were then present at the nursing of the focal sow (average Spearmann correlation coef®cient in 14 sows was 0.35, CMH statistics; P < 0:05). Second, the higher the number of sows, which nursed before the focal sow, the higher, was the proportion of own piglets, which were missing (average of the correlation coef®cients in 14 sows was 0.43, CMH statistics; P < 0:01). Using strati®ed 2 2 contingency tables, the tendency to cross-suckle less when the own mother and the potential ``stepmother'' nursed in synchrony among the 46 SS_OWN ALIEN piglets and among the 32 SS_ALIENS piglets was assessed. In some of the contingency tables, a row or a column was empty, and hence, N varies between tests. For SS_OWN ALIEN piglets, there was no association between the variables ``mother sow was nursing at the same time as the focal sow'' and ``the piglet was cross-suckling at the focal sow'' (CMH General Association statistics for 30 piglets; P > 0:1). Similarly, cases of ``mother sow nursed immediately after the focal sow'' and ``the piglet was crosssuckling at the focal sow'' occurred at the expected frequency (CMH General Association statistics for 30 piglets; P > 0:1). However, cases of ``mother sow nursed immediately before the focal sow'' and ``the piglet was cross-suckling at the focal sow'' were less frequent than expected (CMH General Association statistics for 28 piglets; P < 0:01). The odds ratio for this association was 0.39, indicating that when the mother sow nursed just before a focal sow, the probability that an SS_OWN ALIEN piglet will cross-suckle at that sow was only 39% compared to the probability when there was no synchrony. For SS_ALIENS piglets, observed frequencies of cross-suckling when the mother sow was nursing either just before, at the same time, or just after the focal sow did not differ from those expected by chance (CMH General Association statistics for 13, 17 and 12 piglets, respectively; all P > 0:05).
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3.5. Cross-suckling and the number of achieved nursings The mean number of nursings in which the piglets participated (irrespective of whether it was at the own mother or at another dam) was 3.86 (ranging from 3.64 to 5.00 in the six groups). This was not different from four nursings, which would be theoretically expected under the assumptions of no cross-suckling and full participation of piglets in all nursings (Wilcoxon signed rank T-test; n 6; P > 0:05). Within the groups, the number of achieved nursings (TOTSUCKS) per piglet was not correlated with litter size (r s 0:02; n 22; P > 0:05) or dams parity (r s 0:11; n 22; P > 0:05), but was correlated with litter age (r s 0:44; n 22; P < 0:05) indicating that belonging to an older litter within a group may have an advantage in terms of a more frequent participation in nursings. The SS_OWN piglets achieved, on the average, 3.64 nursings, while SS_1_ALIEN piglets achieved 3.45 nursings. The difference was not signi®cant, as indicated by the paired comparison in 10 litters in which there was at least one piglet using the SS_OWN strategy and at least one using the SS_1_ALIEN strategy (Wilcoxon signed rank T-test; P > 0:05). Similarly, the SS_OWN ALIEN piglets did not differ from the SS_MORE_ALIENS ones in the number of achieved nursings (4.86 versus 5.00, Wilcoxon signed rank T-test; n 7; P > 0:05). 4. Discussion According to previous studies of cross-suckling, the incidence of this behaviour should decline with decreasing number of sows in a group (Fraser and Broom, 1990; WuÈlbersMindermann, 1992). Low incidence of cross-suckling in small groups (four sows) was reported by GoÈtz et al. (1991) Ð 4%; WuÈlbers-Mindermann (1992) Ð 5% and Brodmann and Wechsler (1994) Ð 8%. Nevertheless, this study had found a substantial amount of cross-suckling (29% of all sucklings) even in small groups of three to four sows. The high occurrence of cross-suckling in this study may be connected to the fact that the observations were made at 19±32 days postpartum. This is the lactation phase when the milk production gradually declines and piglets start to search for additional sources of milk (Burgerstaller, 1985). Consequently, the incidence of cross-suckling might be expected to rise as found by other authors (e.g. Burgerstaller, 1985; Jensen, 1988; WuÈlbers-Mindermann, 1992). In this study, there was a signi®cant within group correlation between litter age and the amount of cross-suckling. This might be interpreted as an evidence that between late third and early ®fth week postpartum, the cross-suckling increases in frequency. Alternatively, it might have been that the correlation was caused by the relative litter age differences within the groups, rather than by the absolute increase of crosssuckling with age. Among our piglets, there were 22% ``occasional'' cross-sucklers (the SS_OWN ALIEN category). This agrees roughly with previous reports by Andersson and AndreÂasson (1992) who observed 16% of occasional cross-sucklers, Olsen et al. (1998) who observed 29% of piglets using this strategy and Brodmann and Wechsler (1994) who observed it in 13% of piglets. Quite a high proportion (16%) of piglets, which shifted entirely to one or
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more adoptive sows (the SS_1_ALIEN and SS_MORE_ALIENS categories) was recorded in this study. Most researchers described lower rates of permanent cross-sucklers, e.g. Algers et al. (1991) Ð 3%; GoÈtz et al. (1991) Ð 4%; Brodmann and Wechsler (1994) Ð 11% and Olsen et al. (1998) Ð 5%, although Andersson and AndreÂasson (1992) reported 31% permanent cross-sucklers. In this study, the permanent cross-sucklers mostly switched completely from the own mother to one alien sow (11%) while only a few of them (5%) oscillated among more sows. Brodmann and Wechsler (1994), Puppe and Tuchscherer (1995) and Olsen et al. (1998) also found that a majority of permanent cross-sucklers suckled at one ``adoptive'' sow only. It, therefore, appears that even in a multi-suckling situation, piglets attempt to secure a stable source of milk: either the own mother (which some of them occasionally leave for opportunistic cross-suckling) or a single ``stepmother''. According to the present study, litter size appears to be an important determinant of cross-suckling. Piglets from large litters cross-suckled more often and missed nursings of their mothers more often than piglets from smaller litters in the same group. Andersson and AndreÂasson (1992) reported a similar trend. This effect might be due to differences in milk intake. Piglets from large litters have to share milk with more littermates; hence, individuals grow slower and have more to gain by trying alternative sources of milk. This explanation is indirectly supported by the results of Olsen et al. (1998). In their study, litter size was large and its variability low and consequently, no effect of litter size on crosssuckling was found. However, the milk production of a sow before mixing (measured by daily piglet weight gain) was a strong predictor for how much cross-suckling her piglets displayed. In the present study, the effect of litter size on cross-suckling was limited to permanent cross-sucklers because within groups, SS_ALIENS piglets originated from larger litters than the faithful (SS_OWN) piglets, but SS_OWN ALIEN did not. This may indicate that the risky decision of switching completely to another source of milk is undertaken more often by piglets who have more to gain, whereas any piglet may undertake the opportunistic cross-suckling. Another question related to litter size is whether the litter size of the potential target sows plays a role in how attractive they are for cross-suckling. Several authors state that cross-suckling piglets sucked usually in smaller litters than was their own (WuÈlbers-Mindermann, 1992; GoÈtz et al., 1991; Brodmann and Wechsler, 1994). In a post-hoc calculation, it was found that this was also the case in this study (Wilcoxon paired T-test; P < 0:01). However, this, in itself, is not proof that piglets are attracted to small litters for cross-suckling. Rather, it may be just a side effect of the fact that crosssuckling piglets come from large litters and hence, the potential target litters are, by de®nition, smaller than the average. The more appropriate question is whether the cross-sucklers preferred, among the potential target sows (i.e. sows in the group excluding their mother), sows with small or large litters. Contrary to expectation, it was found that they preferred sows with larger litters. This ®nding was supported by the correlation between litter size of a sow and the number of alien piglets participating in her nursing, which was positive (although not signi®cant), rather than negative. There are two possible reasons why cross-suckling piglets avoided sows with small litters. First, although sows with smaller litters have more unoccupied teats, most of these probably were not functional by the time when the litters
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were mixed as the milk glands cease producing milk after the teat is not emptied during the ®rst week of lactation (Kim et al., 2000). Hence, number of unoccupied teats may be less important than the number of free functional teats. Our data indicate that sows with relatively large litters may offer more opportunities for ®nding a free functional teat, as the litter size correlated strongly with the proportion of own piglets absent at nursings. Moreover, this proportion of missing own piglets correlated signi®cantly with the number of alien piglets participating in nursings, which suggests that alien piglets do indeed often use teats vacated by missing ``native'' piglets. Another reason why sows with small litters were less often targeted by cross-suckling may be that they were better able to repel the cross-suckling attempts through attacking selectively the alien piglets. In groups of six sows, piglets that were seen cross-suckling at least once received more aggression from non-maternal sows even though sows performed less nose contacts with foster sows compared to their own piglets (Olsen et al., 1998). The effect of piglet age on cross-suckling was less pronounced than the effect of litter size in this study. Nevertheless, some interesting relationships were evident: within groups, older piglets performed active cross-suckling more often than younger ones. At the same time, older piglets were not more frequently absent from nursings of their mothers. Taken together, this might indicate that older litters have, on the average, a better ability to utilise nursings of alien sows while not missing nursings at the own mother. Indeed, the average number of nursings in which a piglet from a certain litter participated was signi®cantly correlated with age of the litter. We did not ®nd other age effects such as higher incidence of alien piglets in nursings of sows with younger litters (WuÈlbers-Mindermann, 1992). Admittedly, the ability of this study to detect age/ontogeny effects was limited because we did not follow the same piglets repeatedly and differences in litter ages within the groups were relatively small. Despite the wide range of parities within groups of observed sows, no effect of parity number on the presence of alien piglets or absence of own piglets and piglets' frequency of active cross-suckling was found. WuÈlbers-Mindermann (1992) and Olsen et al. (1998) observed higher incidence of cross-suckling among progeny of high-parity sows. Puppe and Tuchscherer (1995), to the contrary, recorded higher cross-suckling activity among piglets born to primiparous sows. The effect of parity, thus, remains unclear, but is probably less important than that of litter size and litter age. The sows in this study displayed an 82% nursing synchronisation. If the sows would nurse completely independently of each other, the estimated degree of synchronisation would amount to only 10%. Other authors also reported pronounced nursing synchronisation in multi-suckling systems (Bryant et al., 1983; Wechsler and Brodmann, 1996; Newberry and Wood-Gush, 1985). The nursing synchronisation among group-housed sows may have a considerable effect on piglets (cross)suckling behaviour (Bryant et al., 1983; GoÈtz et al., 1991; WuÈlbersMindermann, 1992; Wechsler and Brodmann, 1996; Wattanakul et al., 1997). It is important to differentiate how exactly the nursing bouts are synchronised because an even small temporal shift between two nursings can change the distribution of crosssuckling. The results indicate that if sows nurse quickly one after another, then the ®rst one to nurse attracts more piglets. Three indications that this is the case were found. First and second, the more sows that nursed just before a focal sow, the fewer alien piglets
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that participated in her nursing and the lower was the attendance of her own piglets in the nursing. Third, when the own mother of an occasional cross-suckler (a SS_OWN ALIEN piglet) nursed just before a potential stepmother, then the probability that this piglet would cross-suckle at the stepmother during her current nursing was reduced by 61%. However, this last relationship was not present in permanent cross-sucklers (SS_ALIENS piglets), which indicates that once a piglet ceases to suckle at its own mother, it is no longer in¯uenced by her behaviour. These results are in accordance with ®ndings of WuÈlbers-Mindermann (1992) that the opportunistic cross-sucklers (those which crosssuckled <35% of nursings) mostly cross-suckled in nursings when their own mother was not synchronised. These results appear to indicate that an ef®cient strategy for a sow to avoid cross-suckling attempts by alien piglets is to wait until another sow or sows begin nursing and then to start nursing herself. A high degree of synchronisation may a result if all sows follow this strategy so that when one of them starts a nursing, the others follow in a chain reaction. The number of nursings in which a piglet participated during the observation period was used as an indirect measure of success of the various (cross)suckling strategies. Because of the design of the experiment and de®nition of the cross-suckling categories, only two unbiased comparisons could be made. Piglets which chose one alien sow in place of their own mother (SS_1_ALIEN) attended a similar number of nursings as faithful piglets (SS_OWN) and permanent cross-sucklers at more than one sows (SS_MORE_ALIENS) achieved a similar number of sucklings as piglets with the opportunistic suckling strategy (SS_OWN ALIEN). Hence, according to this criterion, the three main categories of piglets (the faithful ones, the opportunistic and the permanent cross-sucklers) were equally successful at getting access to nursings. This suggests that in a multi-suckling system, the frequency of various suckling strategies eventually develop into a balance when all of them are equally pro®table. Overall, piglets in this study achieved the same number of sucklings as would be expected in a no-cross-suckling situation. This study, thus, suggests that, although crosssuckling may be frequent in stabilised multi-suckling group, this need not have an adverse effect on the overall milk intake of the piglets. Arey and Sancha (1996) found out that in the ``family group housing system'' (multi-suckling system) a high percentage of piglets was present at each suckling bout (96%), which is in accordance with our calculations for the average proportion of achievable nursings (96.5%). 5. Conclusions 1. Frequent cross-suckling (29% of all suckling events) was observed in a commercial multi-suckling system with small groups of sows at the fourth week of lactation. 2. Large litter size was the main determinant of cross-suckling, especially for permanent cross-sucklers. 3. Sows nursing immediately after other sows attracted less cross-suckling. High degrees of nursing synchrony observed in multi-suckling systems may result from attempts of sows to avoid cross-suckling through starting their nursing immediately after the other sows.
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4. Permanently cross-suckling, occasionally cross-suckling and faithful piglets achieved the same number of suckling, indicating that these strategies may be equally successful in a stabilised multi-suckling situation. Acknowledgements We thank the staff at the pig farm in OparÏany for their excellent technical assistance. We are grateful to Hayley Randle and Suzanne Held for improving English of earlier version of the manuscript. This work was supported by a grant from the Ministry of Agriculture of the Czech Republic (MZe M02-99-03) and GA 523/99/0985 from Grant Agency of the Czech Republic. References Algers, B., Madej, A., Rojanasthien, S., UvnaÈs-Moberg, K., 1991. Quantitative relationships between suckinginduced teat stimulation and the release of prolactin, gastrin, somatostatin, insulin, glucagon and vasoactive intestinal polypeptide in sows. Vet. Res. Commun. 15, 395±407. Andersson, C., AndreÂasson, E., 1992. Digivande suggor i smaÈ grupper. Dygnsrytm, sociala interaktioner och digivnings-beteende. Examensarbete 41. Swedish University of Agricultural Sciences. Uppsala, p. 56 (in Swedish). Arey, D.S., Sancha, E.S., 1996. Behavior and productivity of sows and piglets in a family system and in farrowing crates. Appl. Anim. Behav. Sci. 50, 135±145. Braun, S., Jensen, P., 1988. Cross-sucking in piglets in loose-housed sow groups, or what makes a piglet become a cuckoo. In: Proceedings of the International Congress on Applied Ethology in Farm Animals, Skara, Sweden, pp. 170±173. Brodmann, N., Wechsler, B., 1994. Strategien von fremdsaugenden Ferkeln bei der Gruppenhaltung von ferkelfuhrenden Sauen. In: Aktuelle Arbeiten zur artgemaÈûen Tierhaltung 370, 237±246 (in German). Bryant, M.J., Rowlinson, P., Van der Steen, H.A.M., 1983. A comparison of the nursing and suckling behavior of group-housed and individually-housed sows and their litters. Anim. Prod. 36, 445±451. Burgerstaller, G., 1985. Praktische SchweinefuÈtterung. Eugen Ulmer, Stuttgart (in German). Fraser, A.F., Broom, D.M., 1990. Feeding. In: Farm Animal Behavior and Welfare. Bailliere Tindall, London, pp. 79±98. FraÈdrich, H., 1965. Zur Biologie des Warzenschweines (Phacochoerus aethiopicus) unter BeruÈcksichtigung des Verhaltens den Suiden. Z. Tierpsychol. 22, 328±393 (in German). GoÈtz, M., Weiss, E., Rist, M., 1991. Cross-suckling und Saugordnung im Gruppenabferkeln. In: Aktuelle Arbeiten zur argemaÈûen Tierhaltung. 344, 70±79 (in German). Hartman, D.A., Ludwick, T.M., Wilson, R.F., 1962. Certain aspects of lactation performance in sows. J. Anim. Sci. 21, 883±886. Hatet, G., Edwards, S.A., Gall, K., Arey, D.S., 1994. Effect of three lactation housing systems on sow and piglet performance and behavior. Anim. Prod. 58, 475. Jensen, P., 1986. Observations on the maternal behavior of free-ranging domestic pigs. Appl. Anim. Behav. Sci. 16, 131±142. Jensen, P., 1988. Maternal behavior and mother-young interactions during lactation in free-ranging domestic pigs. Appl. Anim. Behav. Sci. 20, 297±308. Kim, S.W., Easter, A., Hurley, W.L., 2000. Regression of non-suckled mammary glands in lactating sows. In: Proceedings of the 5th Joint EAAP/ASAS Workshop on the Biology of Lactation in Farm Animals, Hague, The Netherlands, p. 31. Mauget, R., 1981. Behavioral and reproductive strategies in wild forms of Sus scrofa (European wild boar and feral pigs). In: Sybesma, W. (Ed.), The Welfare of Pigs. Nijhoff, The Hague, pp. 3±13.
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Newberry, R.C., Wood-Gush, G.M., 1985. The suckling behavior of domestic pigs in a semi-natural environment. Behaviour 95, 11±25. Olsen, A.N.W., Dybkjaer, L., Vestergaard, K.S., 1998. Cross-sucking and associated behavior in piglets and sows. Appl. Anim. Behav. Sci. 61, 13±24. Packer, C., Lewis, S., Pusey, A., 1992. A comparative analysis of non-offspring nursing. Anim. Behav. 43, 265± 281. Pedersen, L.J., Studnitz, M., Jensen, K.H., Giersing, A.M., 1998. Suckling behavior of piglets in relation to accessibility to the sow and the presence of foreign litters. Appl. Anim. Behav. Sci. 58, 267±279. Puppe, B., Tuchscherer, M., 1995. Zum Saugverhalten und zur Entwicklung biochemischer Parameter bei Ferkeln unter den Bedingungen einer Gruppenhaltung saÈugender Sauen: Erste Ergebnisse. Berliner und Munchener Tierarztliche Wochenschrift 108, 161±166 (in German). Riedman, M.L., 1982. The evolution of alloparental care and adoption in mammals and birds. Q. Rev. Biol. 57, 405±435. SAS Institute, 1999. SAS Version 8, Online Document on CD-ROM. Wattanakul, W., Stewart, A.H., Edwards, S.A., English, P.R., 1997. Effects of grouping piglets and changing sow location on suckling behavior and performance. Appl. Anim. Behav. Sci. 55, 21±35. Wattanakul, W., Edwards, S.A., Stewart, A.H., English, P.R., 1998a. Effect of familiarity the environment on the behavior and performance response of sows and piglets to grouping with during lactation. Appl. Anim. Behav. Sci. 61, 25±39. Wattanakul, W., Stewart, A.H., Edwards, S.A., English, P.R., 1998b. The effect of cross-suckling and presence of additional piglets on sucking behavior and performance of individually housed litters. Anim. Sci. 66, 449± 455. Wechsler, B., Schmid, H., Moser, H., 1991. Der Stolba-Familienstall fuÈr Hausschweine: ein tiergerechtes Haltungsystem fuÈr Zucht- und Mastschweine. Birkhaeuser, Basel (in German). Wechsler, B., Brodmann, N., 1996. The synchronisation of nursing bouts in group-housed sows. Appl. Anim. Behav. Sci. 47, 191±199. WuÈlbers-Mindermann, M., 1992. Characteristics of cross-suckling piglets reared in a group housing system. Department of Animal Hygiene, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Skara, Sweden. Specialarbete 13, 77.
Cross-suckling and nursing synchronisation in group housed lactating sows J. MaletõÂnskaÂ*, M. SÏpinka Ethology Group, Research Institute of Animal Production, Pratelstvi 815, 10400 Prague, UhrÏÂõneÏves, Czech Republic Accepted 20 July 2001
Abstract Group housing systems for lactating sows with piglets enable the animals to behave more naturally than traditional restrictive systems. However, piglets may occasionally suckle from other sows than their mother. The in¯uence of litter size, age of the litter, mother parity, piglet gender and, in particular, nursing synchronisation, on the following: the occurrence of cross-suckling (presence of alien piglets at the udder during milk ejection); cross-suckling strategies; and piglets' success at achieving nursings, was investigated. The observations were carried out on six stable groups of three or four unrelated sows with their piglets between 19 and 32 days postpartum. Crosssuckling was frequent (occurred in 29% of all suckling events). The main determinant of crosssuckling was litter size. Piglets from larger litters missed nursings of their mothers more often (r s 0:72; n 22; P < 0:001) and performed cross-suckling more often than piglets from smaller litters (r s 0:54; n 22; P < 0:05). Piglets, who were observed suckling only alien sows, belonged to larger litters than piglets suckling only their own mother (Wilcoxon signed rank T-test; n 6; P < 0:05). Sows with larger litters were preferred targets for cross-suckling (Wilcoxon signed rank T-test; n 78; P < 0:001). Piglets from older litters cross-suckled more often than piglets from younger litters (r s 0:50; n 22; P < 0:05). Nursing synchronisation (sows nursing within one minute of each other) was high at 82%. Sows nursing immediately after other sows attracted less cross-suckling. The higher the number of sows which had nursed just before a focal sow, the fewer alien piglets were then present at her nursing (r s 0:35; n 14; Cochran± Mantel±Haenszel (CMH) statistic; P < 0:05). Piglets belonging to a speci®c litter were less likely to cross-suckle at an alien sow if her nursing was preceded by a nursing of the mother of that litter (CMH statistic for 28 piglets; P < 0:01). Permanently cross-suckling, occasionally cross-suckling and faithful piglets achieved a similar number of suckling events indicating that these strategies may be equally successful in a stabilised multi-suckling situation. Mother parity and piglets' gender had no effect on cross-suckling. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Pig; Nursing; Cross-suckling; Suckling strategies; Synchronisation *
Corresponding author. Tel.: 420-2-67710713; fax: 420-2-67710779. E-mail address: [email protected] (J. MaletõÂnskaÂ). 0168-1591/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 1 ) 0 0 1 7 8 - 2
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1. Introduction In commercial pig production, lactating sows are often kept in narrow farrowing crates without any bedding. This housing system limits the movement of the sow and prevents her from performing several natural behavioural patterns such as rooting, resting and selfregulation of contact with her piglets. Group housing or multi-suckling systems allow these behaviours to be performed, and hence, can enhance some aspects of sow welfare (Jensen, 1986; Algers et al., 1991; Wechsler et al., 1991). Often, lactating sows in these systems are kept in individual crates for 1±2 weeks after parturition and then 3±15 of them are moved together with their litters, into a common straw-bedded pen. However, such systems have problems of their own, such as cross-suckling. Cross-suckling (where young mammals suckle at dams other than their mother) (also called allo-suckling) has been observed in many wild, feral and domestic animals that live in groups (Riedman, 1982; Packer et al., 1992). Within pigs, cross-suckling has been reported in the wart-hog (Phacochoerus aethiopicus) (FraÈdrich, 1965), the wild boar (Sus scrofa) (Mauget, 1981), and in both free-ranging (Newberry and Wood-Gush, 1985) and indoor housed domestic pigs (WuÈlbers-Mindermann, 1992; Brodmann and Wechsler, 1994; Puppe and Tuchscherer, 1995) at various rates. The cross-suckling in the commercial multi-suckling systems deserves special attention because of its unwanted consequences. Cross-suckling may result in ®ghting among piglets, disruption of previously established teat orders (Andersson and AndreÂasson, 1992; Pedersen et al., 1998; Wattanakul et al., 1997, 1998b), a higher proportion of missed nursings and nursings without milk ejection (Arey and Sancha, 1996; Wattanakul et al., 1998a; Pedersen et al., 1998) and, as a result, reduced milk intake and weight gain (Puppe and Tuchscherer, 1995; WuÈlbers-Mindermann, 1992). Both the cross-suckling piglets and those, which remain faithful to their mothers, may be affected (Puppe and Tuchscherer, 1995; Pedersen et al., 1998). Indeed, it remains unclear whether cross-suckling piglets achieve a lower, equal or higher number of successful sucklings than their faithful siblings. Although it has been documented that cross-suckling brings some disorder into multi-suckling groups, it has not yet been established whether, from an individual piglet's point of view, cross-suckling is a poorer, as good as, or better, strategy for obtaining more milk than remaining faithful. Several factors probably affect the incidence of cross-suckling. First, in groups of between 5 and 11 sows, the occurrence of cross-suckling declines with the decreasing number of sows in group (Fraser and Broom, 1990; WuÈlbers-Mindermann, 1992). This may indicate that cross-suckling might be infrequent in very small groups, e.g. three to four sows. Indeed, incidence below or around 10% was reported in such small groups by GoÈtz et al. (1991), WuÈlbers-Mindermann (1992), Brodmann and Wechsler (1994) and Puppe and Tuchscherer (1995). Second, high levels of cross-suckling were observed in groups, which were composed of litters varying considerably in age (Braun and Jensen, 1988) and/or size (WuÈlbersMindermann, 1992; GoÈtz et al., 1991; Brodmann and Wechsler, 1994). Third, the incidence of cross-suckling may change during ontogeny. High levels of cross-suckling were observed for several days after grouping the sows and their litters into the common pen (Hatet et al., 1994; Wattanakul et al., 1997). A second peak may occur during the fourth week of lactation when the milk production of the sow starts to decline
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(Hartman et al., 1962; Burgerstaller, 1985; Jensen, 1988; WuÈlbers-Mindermann, 1992). Fourth, the incidence of cross-suckling may be in¯uenced by the parity of the dam. Older dams with more maternal experience may be more able to prevent cross-suckling, for instance, by better synchronising with other sows, not starting a nursing when there are alien piglets around, or by interrupting a nursing if there is too much ®ghting for teats. Finally, cross-suckling behaviour of piglets in a group-housing pen can be in¯uenced by the synchronisation of nursing bouts among sows (GoÈtz et al., 1991). This presumption is indirectly supported by the fact that the proportion of successful nursings (nursings with milk ejection) tends to be higher in groups with highly synchronised nursings (Bryant et al., 1983; Wattanakul et al., 1997). The effect of nursing synchronisation on cross-suckling has not yet been investigated in pigs. Cross-suckling piglets differ in whether they opportunistically switch between suckling several sows or focus on suckling a single alien dam, and in whether they still suckle at their own mother. Accordingly, cross-suckling piglets can be classi®ed into different categories, e.g. as habitual (or permanent) versus occasional (or opportunistic) cross-sucklers (Brodmann and Wechsler, 1994; Olsen et al., 1998; WuÈlbers-Mindermann, 1992). When assessing the effects of the various factors on cross-suckling, attention should be paid not only to the total number of cross-suckling piglets or cross-suckling events, but also to how the events are distributed among cross-sucklers using different strategies. The aim of this study was to assess the in¯uence of litter size, age of the litter, mother parity, piglet gender and, in particular, nursing synchronisation on the occurrence of crosssuckling, cross-suckling strategies, and piglets' success at achieving nursings in a commercial multi-suckling system with three to four sows per group. 2. Materials and methods 2.1. Animals and housing The observations were carried out in a commercial piggery in South Bohemia. Pregnant sows were housed in large (up to 30 animals) dynamic groups in straw-bedded pens. One week before parturition, sows were placed in individual farrowing crates. All piglets were ear-tattooed on the day of birth. When piglets were approximately 10 days old (median) (minimum 6; ®rst quartile 9; third quartile 13; maximum 18) groups of three or four lactating sows and their litters were formed. Each group was housed in a pen measuring 9:4 m 4:5 m. The pen included a lying area covered with straw bedding (two®fth of the total area), a small shelter (120 cm 50 cm 50 cm) for piglets, a dunging area without bedding (one-®fth of the total area Ð the lowest part of the pen) and an elevated part for drinking and eating (two-®fth of the total area). The sows were fed a standard diet for lactating sows at 06.00 h and 15.00 h, piglets had free access to a feeder with a standard diet for early weaned piglets, which was located in an elevated part of the pen. Six groups of unrelated lactating sows (two groups of three sows and four groups of four sows) were observed. These groups included two Large White and 20 Landrace sows, ranging between ®rst and eighth (median fourth) lactation and their 207 piglets. Piglets were between 19 and 32 (median 24) days of age during the observations and the intragroup
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difference in age ranged from 0 to 8 days (median 2 days) in individual groups. The average litter size was nine piglets (range: 3±13). 2.2. Observations Each group was observed on two consecutive days between 08.00 and 15.00 h. One hour before observations began all piglets in the group were marked on their backs using differently coloured numbers for each litter. We observed one sow at a time for four successful nursings. We recorded the beginning of nursing, success of nursing (with or without milk ejection) and identity of all suckling piglets. A piglet was considered to suckle at a given sow when it was present at her udder during the time of milk ejection. We also recorded which sows in the group nursed at the same time, immediately before or immediately after the nursing of a focal sow. During the observations, the following behavioural de®nitions were used:
beginning of nursing Ð at least two piglets started massage of teats of the focal sow and this sow started characteristic nursing grunting; end of milk ejection Ð piglets started switching between teats and/or massaging their teats after they have been suckling the teats rhythmically during milk ejection; sows nursing at the same time as the focal sow Ð sows which started to nurse during the interval between beginning of nursing and end of the milk ejection of the focal sow; sows nursing immediately before the focal sow Ð sows which started to nurse not more than 1 min before the focal sow; sows nursing immediately after the focal sow Ð sows which started to nurse at latest 1 min after the end of milk ejection of the focal sow.
2.3. Statistical analysis Two-tailed tests with a level of 0.05 were used, throughout the statistical analysis. 2.3.1. Quantification of cross-suckling Piglets were sorted into four (``suckling strategies'') categories according to their observed suckling/cross-suckling behaviour: those suckling only their own mother (SS_OWN), those suckling both the own mother and one or more alien sows (SS_OWN ALIEN), those suckling solely one alien sow (SS_1_ALIEN), and those suckling more than one alien dam, but not the own mother (SS_MORE_ALIENS). For certain analyses, we pooled the last two categories (SS_1_ALIEN; SS_MORE_ALIENS) into one larger, which included all piglets that had been observed to suckle at one or more alien dams, but not at the own mother (SS_ALIENS). The in¯uence of piglet gender was tested on the suckling/cross-suckling behaviour using a w2-test on a contingency table with sex and suckling strategies as sorting variables. In order to quantify the amount of cross-suckling, the following variables were derived:
number of alien piglets present at a nursing (ALIENPIGS) Ð the number of alien piglets suckling teats of the focal sow during the milk ejection (rhythmical suckling of teats);
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proportion of own piglets absenting in a nursing (%OWNABSENT) Ð the difference between the litter size of the focal sow and the number of her piglets participating in the given nursing during the milk ejection (rhythmical suckling of teats), divided by litter size; average number of cross-suckling acts by the own piglets (CROSSUCKS) Ð the total number of times the piglets from the focal litter were seen cross-suckling (during milk ejection) at other sows of the group, divided by litter size; total number of nursings achieved by a piglet (TOTSUCKS) Ð the total number of times a piglet was observed to suckle (i.e. was present at the udder during milk ejection), independent of whether it was at the own mother or another dam.
For variables relating to own piglets of the focal sows (%OWNABS, CROSSUCKS), we took proportional measures related to the focal sow's litter size because they expressed the tendency of an ``average'' piglet to be absent from the own mother and to suckle at alien sows. For of the variable ALIENPIGS, the absolute (not proportional) measure seemed more appropriate because it was unclear whether the litter size of the foster sow or that of the biological mother should be used for a proportional measure. For the purposes of correlation analyses under Sections 2.3.2 and 2.3.3. variables ALIENPIGS and %OWNABSENT were averaged across the four observed nursings. 2.3.2. Cross-suckling and litter size, piglet age and sow parity The factors affecting incidence of cross-suckling were analysed using correlation. The effect of group identity was removed using the SAS GLM procedure with the group identity as a single random factor. The residual values were used as replicates in the analyses. Hence, within-group associations between the analysed variables were assessed. Since some sets of the data departed from normality, Spearmann non-parametric correlations were applied. The effects of litter size, age of the litter and parity of the mother on the amount crosssuckling were assessed by correlating these three variables with ALIENPIGS, %OWNABSENT and CROSSUCKS, using the within-group residuals as described above. Second, whether litter size, age of the litter and parity of the mother in¯uenced the piglets' probability of becoming a cross-sucker was examined. Within each group, the mean litter size (or mean age, or mean mother's parity, respectively) between the piglets of the SS_OWN category, on one side, and the piglets of the SS_ALIENS and SS_OWN ALIEN categories, on the other was compared. A Wilcoxon signed rank ttest was used, for each of the comparisons, to test whether the resulting six differences (one per group) differed signi®cantly from zero. Third, whether the cross-suckling piglets preferred as their stepmothers sows with larger (or smaller) litters, relatively older (or younger) litters or mothers of higher (or lower) parity was investigated. For each cross-suckling piglet, the litter size of the target sow(s) (weighted average litter size in case of SS_MORE_ALIENS piglets) was subtracted from the average litter size of all sows in the group except for the own mother of the crosssuckling piglet. The Wilcoxon signed rank T-test tested, whether the resulting differences were centred around zero or not. Similar calculations were performed for litter age and parity of the target sow(s).
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2.3.3. Relationship between suckling of own and alien piglets Using the residual values after removing the group identity effect, correlations were performed on the variables ALIENPIGS, %OWNABSENT, and CROSSUCKS, in order to determine whether, within groups, the presence of alien cross-suckling piglets at a certain sow was related to the suckling/cross-suckling behaviour of the own piglets of that sow. 2.3.4. Cross-suckling and nursing synchronisation The role of between-sow nursing synchronisation in cross-suckling was examined in two ways. First, at the sow level, whether nursing in synchrony affected the probability that the focal sow will be a target of cross-suckling and the probability that her own piglets will be missing at the udder was investigated. The Cochran±Mantel±Haenszel (CMH) stratumadjusted correlation statistic of the SAS Proc Freq procedure (SAS Institute, 1999) was used. This statistic calculates the correlation coef®cient between two variables in each stratum of the data and then gives an overall statistic, which indicates whether there is a linear association between the two variables, after controlling for the third (stratifying) variable. In this case, the CMH statistic ®rst calculated, over the four observed nursings of each sow, the Spearmann correlation coef®cient between the number of other sows nursing in synchrony with the focal one in a given nursing and the variables ALIENPIGS and %OWNABSENT in the same nursing. Then overall statistics indicated whether these relationships were signi®cant over the whole sample of 22 sows, after controlling for the confounding effect of sow identity. This analysis was performed separately for the synchrony types ``mother sow nursed immediately before the focal sow'', ``mother sow nursed at the same time as the focal sow'' and ``mother sow nursed immediately after the focal sow''. Second, whether the individual piglets cross-suckled more (or less) often during those nursings in which their mother was synchronised with the other dams was investigated. A particular, piglet was focussed on and all nursings by other sows in the group than its mother (i.e. eight nursings in case of a three-sow group and 12 nursings in case of a foursow group) were sorted into a 2 2 contingency table. The rows in table were the nursing was synchronised between the sow in question and the mother of the focal piglets, or was not; and the columns were the focal piglet attended (as a cross-suckler) the nursing, or did not. This resulted in a strati®ed N 2 2 contingency table, where N is the number of evaluated piglets. The CMH General Association statistic (also called the stratum-adjusted Pearson w2; SAS Institute, 1999) was then applied, to test whether there was any relationship between the mother-focal sow synchrony in a speci®c nursing and the probability that a piglet would cross-suckle in that nursing. This analysis was done separately for the 46 SS_OWN ALIEN piglets and the 32 SS_ALIENS piglets, and also separately for the synchrony types ``mother sow nursed immediately before the focal sow'', ``mother sow nursed at the same time as the focal sow'' and ``mother sow nursed immediately after the focal sow'', resulting in a total of six runs of the analysis. 2.3.5. Cross-suckling and the number of achieved nursings The observed number of nursings achieved by each piglet was compared with expected values. As four successful nursings of each sow were observed, the expected number of achieved nursings under the latter condition (and under the assumption that piglets never
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miss nursings) would be four per piglet. For each of the six groups, the average observed number of nursings per piglet, was calculated, and four was deducted from it. The Wilcoxon signed rank T-test was applied to determine whether the resulting six differences were signi®cantly above or below zero. We were interested in how the total number of nursings in which piglets from a litter participated (TOTSUCKS) was affected by the litter size, age of the litter and parity of the mother; in other words, whether piglets from, for instance, an older litter (relative to other litters in the group) succeeded in getting milk more often. To examine this, the number of achieved nursings per piglet (TOTSUCKS) for each litter was calculated and then subjected to a SAS GLM procedure with group identity as a single random effect. The same SAS GLM procedure was applied to the variables ``litter size'', ``age of the litter'' and ``parity of the dam''. The residual values of TOTSUCKS were then correlated with the residuals of litter size, age of the litter and parity of the mother. Lastly whether there was any difference in the number of achieved nursings between cross-suckling piglets and those, which kept suckling at their mothers, was examined. Because some of the `strategies' had, by de®nition, an upper limit of nursings in which the piglets could have been observed (e.g. the maximum value of SS_OWN piglet was four nursings because each sow was observed during four nursings), only two comparisons were performed: strategy SS_OWN was compared with SS_1_ALIEN, and SS_OWN ALIEN with SS_MORE_ALIENS. For each litter for which it was possible, the difference between mean number of achieved nursings by piglets of the one strategy and the other was calculated. The Wilcoxon signed rank T-test was then used to determine whether there was a tendency for one or the other strategy to achieve more nursing. 3. Results 3.1. Occurrence of cross-suckling and cross-suckling strategies More than one-third of piglets cross-suckled at least once and some of them suckled exclusively alien sow/sows (Fig. 1). Eighteen out of the 22 litters contained at least one cross-suckler and 19 of 22 sows were at least once targets of cross-suckling. Of 798 participations of individual piglets in nursings, 234 (29.3%) occurred at a sow other than the piglet's biological mother (Fig. 2). Suckling behaviour of piglets was not in¯uenced by their gender. Female piglets belonged with 29.0, 11.1, 5.3 and 2.4% to strategies SS_OWN, SS_OWN ALIEN, SS_1_ALIEN and SS_MORE_ALIENS, while in male piglets, the percentages were 30.4, 11.1, 5.3 and 2.4% (w2 1 0:735; P > 0:1). Because of the very close match between female and male piglets, gender was subsequently disregarded in all further analyses. 3.2. Cross-suckling and litter size, piglet age and sow parity The correlations between the three measures of cross-suckling and the litter attributes, are displayed in Table 1. The correlations are based on residual values after removing the effect of group identity, so they re¯ect differences within groups. Piglets from large or older
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Fig. 1. Categorisation of piglets according to their suckling behaviour. SS_OWN piglets which suckled only their own mother; SS_OWN ALIEN piglets which suckled the own mother and one or more alien sows; SS_1_ALIEN piglets which suckled solely one alien sow; SS_MORE_ALIENS piglets which suckled more than one alien dam, but not the own mother; X piglets which were never seen to suckle during the observations.
Fig. 2. Distribution of all achieved sucklings in relation to piglets suckling strategies (n 798 sucklings). Suckling of faithful piglets (SS_OWN) at own mother (A); suckling of occasional cross-sucklers (SS_OWN ALIEN) at own mother (B); suckling of occasional cross-sucklers (SS_OWN ALIEN) at alien sows (C); sucklings of permanent cross-sucklers (SS_ALIENS) at alien sows (D).
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Table 1 Correlations (N 22) between litter size, litter age and sow's parity, on one side, and three measures of crosssuckling on the othera rs (ALIENPIGS) Litter size Litter age Sows' parity
0.31 0.33 0.36
rs (%OWNABS) ***
0.72 0.10 0.40
rs (CROSSUCK) 0.54** 0.50* 0.32
a
Spearmann correlation coefficients based on residual values after removing the effect of the group. P < 0:05. ** P < 0:01. *** P < 0:001. *
litters (relative to other litters in the group) missed nursings of their mother and performed cross-suckling more often. Next, the data were analysed from the point of view of the piglets' strategies looking at whether cross-suckling piglets originated from larger or older litters or from mothers of higher parity. Piglets which were observed to suckle only alien sows (SS_ALIENS) belonged to larger litters than piglets suckling only their own mother (SS_OWN; Wilcoxon signed rank T-test; n 6; P < 0:05). No other signi®cant differences were found between SS_OWN piglets, on one side, and SS_ALIENS or SS_OWN ALIEN piglets, on the other, in the size of their litters, their age or in the parity of their mother. Cross-suckling piglets preferred among the potential target sows those with larger litter size (Wilcoxon signed rank T-test; P < 0:001), and also those of higher parity (Wilcoxon signed rank T-test; P < 0:05). The age of the ``host'' litter had no in¯uence on the choice of target sows by the piglets (Wilcoxon signed rank T-test; P > 0:05). 3.3. Relationship between suckling of own and alien piglets There were signi®cant correlations between variables ALIENPIGS and %OWNABSENT (r s 0:46; n 22; P < 0:05) indicating that if a mother was a target of crosssuckling, her own piglets often absented from her nursings. Variables %OWNABSENT and CROSSUCKS were also correlated (r s 0:65; n 22; P < 0:01) showing that litters with high proportion of piglets missing at the mother's udder participated actively in the crosssuckling. However, no direct link was found between the number of alien piglets at a sow and the tendency of her own piglet to cross-suckle elsewhere Ð ALIENPIGS were not correlated with CROSSUCKS (r s 0:03; n 22; P > 0:1). 3.4. Cross-suckling and nursing synchronisation The mean rate of synchronisation was 0.818, i.e. when the focal sow was nursing, each other sow in the group had, on average, the probability of 82% that she will be nursing immediately before (26%), during the same time (35%), or immediately after (21%) the nursing of the focal sow.
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Table 2 Mean correlation coefficients (rs) between measures of nursing synchronisation and measures of cross-suckling, calculated as average values of Spearmann correlation coefficients obtained for each sow over her four observed nursingsa Type of synchronisation
ALIENPIGS
%OWNABS
Number of other sows nursing immediately before focal sow Number of other sows nursing at the same time as focal sow Number of other sows nursing immediately after focal sow
Mean rs: 0.35; n 14; CMH: 4.73* Mean rs: 0.21; n 16; CMH: 1.29 Mean rs: 0.01; n 13; CMH: 0.003
Mean rs: 0.43; n 14; CMH: 8.51** Mean rs: 0.17; n 18; CMH: 2.28 Mean rs: 0.07; n 15; CMH: 0.39
a
Significance based on CMH statistic. P < 0:05. ** P < 0:01. *
Table 2 shows the averages of correlation coef®cients between measures of nursing synchronisation and measures of cross-suckling (across the four observed nursings within each focal sow). The number of sows on which the CMH test was based varied, as the correlation coef®cient could not be calculated for some sows, e.g. because they had no own piglets missing in any of the four nursings. There were two signi®cant relationships. First, the higher the number of sows which nursed just before the focal sow, the less alien piglets were then present at the nursing of the focal sow (average Spearmann correlation coef®cient in 14 sows was 0.35, CMH statistics; P < 0:05). Second, the higher the number of sows, which nursed before the focal sow, the higher, was the proportion of own piglets, which were missing (average of the correlation coef®cients in 14 sows was 0.43, CMH statistics; P < 0:01). Using strati®ed 2 2 contingency tables, the tendency to cross-suckle less when the own mother and the potential ``stepmother'' nursed in synchrony among the 46 SS_OWN ALIEN piglets and among the 32 SS_ALIENS piglets was assessed. In some of the contingency tables, a row or a column was empty, and hence, N varies between tests. For SS_OWN ALIEN piglets, there was no association between the variables ``mother sow was nursing at the same time as the focal sow'' and ``the piglet was cross-suckling at the focal sow'' (CMH General Association statistics for 30 piglets; P > 0:1). Similarly, cases of ``mother sow nursed immediately after the focal sow'' and ``the piglet was crosssuckling at the focal sow'' occurred at the expected frequency (CMH General Association statistics for 30 piglets; P > 0:1). However, cases of ``mother sow nursed immediately before the focal sow'' and ``the piglet was cross-suckling at the focal sow'' were less frequent than expected (CMH General Association statistics for 28 piglets; P < 0:01). The odds ratio for this association was 0.39, indicating that when the mother sow nursed just before a focal sow, the probability that an SS_OWN ALIEN piglet will cross-suckle at that sow was only 39% compared to the probability when there was no synchrony. For SS_ALIENS piglets, observed frequencies of cross-suckling when the mother sow was nursing either just before, at the same time, or just after the focal sow did not differ from those expected by chance (CMH General Association statistics for 13, 17 and 12 piglets, respectively; all P > 0:05).
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3.5. Cross-suckling and the number of achieved nursings The mean number of nursings in which the piglets participated (irrespective of whether it was at the own mother or at another dam) was 3.86 (ranging from 3.64 to 5.00 in the six groups). This was not different from four nursings, which would be theoretically expected under the assumptions of no cross-suckling and full participation of piglets in all nursings (Wilcoxon signed rank T-test; n 6; P > 0:05). Within the groups, the number of achieved nursings (TOTSUCKS) per piglet was not correlated with litter size (r s 0:02; n 22; P > 0:05) or dams parity (r s 0:11; n 22; P > 0:05), but was correlated with litter age (r s 0:44; n 22; P < 0:05) indicating that belonging to an older litter within a group may have an advantage in terms of a more frequent participation in nursings. The SS_OWN piglets achieved, on the average, 3.64 nursings, while SS_1_ALIEN piglets achieved 3.45 nursings. The difference was not signi®cant, as indicated by the paired comparison in 10 litters in which there was at least one piglet using the SS_OWN strategy and at least one using the SS_1_ALIEN strategy (Wilcoxon signed rank T-test; P > 0:05). Similarly, the SS_OWN ALIEN piglets did not differ from the SS_MORE_ALIENS ones in the number of achieved nursings (4.86 versus 5.00, Wilcoxon signed rank T-test; n 7; P > 0:05). 4. Discussion According to previous studies of cross-suckling, the incidence of this behaviour should decline with decreasing number of sows in a group (Fraser and Broom, 1990; WuÈlbersMindermann, 1992). Low incidence of cross-suckling in small groups (four sows) was reported by GoÈtz et al. (1991) Ð 4%; WuÈlbers-Mindermann (1992) Ð 5% and Brodmann and Wechsler (1994) Ð 8%. Nevertheless, this study had found a substantial amount of cross-suckling (29% of all sucklings) even in small groups of three to four sows. The high occurrence of cross-suckling in this study may be connected to the fact that the observations were made at 19±32 days postpartum. This is the lactation phase when the milk production gradually declines and piglets start to search for additional sources of milk (Burgerstaller, 1985). Consequently, the incidence of cross-suckling might be expected to rise as found by other authors (e.g. Burgerstaller, 1985; Jensen, 1988; WuÈlbers-Mindermann, 1992). In this study, there was a signi®cant within group correlation between litter age and the amount of cross-suckling. This might be interpreted as an evidence that between late third and early ®fth week postpartum, the cross-suckling increases in frequency. Alternatively, it might have been that the correlation was caused by the relative litter age differences within the groups, rather than by the absolute increase of crosssuckling with age. Among our piglets, there were 22% ``occasional'' cross-sucklers (the SS_OWN ALIEN category). This agrees roughly with previous reports by Andersson and AndreÂasson (1992) who observed 16% of occasional cross-sucklers, Olsen et al. (1998) who observed 29% of piglets using this strategy and Brodmann and Wechsler (1994) who observed it in 13% of piglets. Quite a high proportion (16%) of piglets, which shifted entirely to one or
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more adoptive sows (the SS_1_ALIEN and SS_MORE_ALIENS categories) was recorded in this study. Most researchers described lower rates of permanent cross-sucklers, e.g. Algers et al. (1991) Ð 3%; GoÈtz et al. (1991) Ð 4%; Brodmann and Wechsler (1994) Ð 11% and Olsen et al. (1998) Ð 5%, although Andersson and AndreÂasson (1992) reported 31% permanent cross-sucklers. In this study, the permanent cross-sucklers mostly switched completely from the own mother to one alien sow (11%) while only a few of them (5%) oscillated among more sows. Brodmann and Wechsler (1994), Puppe and Tuchscherer (1995) and Olsen et al. (1998) also found that a majority of permanent cross-sucklers suckled at one ``adoptive'' sow only. It, therefore, appears that even in a multi-suckling situation, piglets attempt to secure a stable source of milk: either the own mother (which some of them occasionally leave for opportunistic cross-suckling) or a single ``stepmother''. According to the present study, litter size appears to be an important determinant of cross-suckling. Piglets from large litters cross-suckled more often and missed nursings of their mothers more often than piglets from smaller litters in the same group. Andersson and AndreÂasson (1992) reported a similar trend. This effect might be due to differences in milk intake. Piglets from large litters have to share milk with more littermates; hence, individuals grow slower and have more to gain by trying alternative sources of milk. This explanation is indirectly supported by the results of Olsen et al. (1998). In their study, litter size was large and its variability low and consequently, no effect of litter size on crosssuckling was found. However, the milk production of a sow before mixing (measured by daily piglet weight gain) was a strong predictor for how much cross-suckling her piglets displayed. In the present study, the effect of litter size on cross-suckling was limited to permanent cross-sucklers because within groups, SS_ALIENS piglets originated from larger litters than the faithful (SS_OWN) piglets, but SS_OWN ALIEN did not. This may indicate that the risky decision of switching completely to another source of milk is undertaken more often by piglets who have more to gain, whereas any piglet may undertake the opportunistic cross-suckling. Another question related to litter size is whether the litter size of the potential target sows plays a role in how attractive they are for cross-suckling. Several authors state that cross-suckling piglets sucked usually in smaller litters than was their own (WuÈlbers-Mindermann, 1992; GoÈtz et al., 1991; Brodmann and Wechsler, 1994). In a post-hoc calculation, it was found that this was also the case in this study (Wilcoxon paired T-test; P < 0:01). However, this, in itself, is not proof that piglets are attracted to small litters for cross-suckling. Rather, it may be just a side effect of the fact that crosssuckling piglets come from large litters and hence, the potential target litters are, by de®nition, smaller than the average. The more appropriate question is whether the cross-sucklers preferred, among the potential target sows (i.e. sows in the group excluding their mother), sows with small or large litters. Contrary to expectation, it was found that they preferred sows with larger litters. This ®nding was supported by the correlation between litter size of a sow and the number of alien piglets participating in her nursing, which was positive (although not signi®cant), rather than negative. There are two possible reasons why cross-suckling piglets avoided sows with small litters. First, although sows with smaller litters have more unoccupied teats, most of these probably were not functional by the time when the litters
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were mixed as the milk glands cease producing milk after the teat is not emptied during the ®rst week of lactation (Kim et al., 2000). Hence, number of unoccupied teats may be less important than the number of free functional teats. Our data indicate that sows with relatively large litters may offer more opportunities for ®nding a free functional teat, as the litter size correlated strongly with the proportion of own piglets absent at nursings. Moreover, this proportion of missing own piglets correlated signi®cantly with the number of alien piglets participating in nursings, which suggests that alien piglets do indeed often use teats vacated by missing ``native'' piglets. Another reason why sows with small litters were less often targeted by cross-suckling may be that they were better able to repel the cross-suckling attempts through attacking selectively the alien piglets. In groups of six sows, piglets that were seen cross-suckling at least once received more aggression from non-maternal sows even though sows performed less nose contacts with foster sows compared to their own piglets (Olsen et al., 1998). The effect of piglet age on cross-suckling was less pronounced than the effect of litter size in this study. Nevertheless, some interesting relationships were evident: within groups, older piglets performed active cross-suckling more often than younger ones. At the same time, older piglets were not more frequently absent from nursings of their mothers. Taken together, this might indicate that older litters have, on the average, a better ability to utilise nursings of alien sows while not missing nursings at the own mother. Indeed, the average number of nursings in which a piglet from a certain litter participated was signi®cantly correlated with age of the litter. We did not ®nd other age effects such as higher incidence of alien piglets in nursings of sows with younger litters (WuÈlbers-Mindermann, 1992). Admittedly, the ability of this study to detect age/ontogeny effects was limited because we did not follow the same piglets repeatedly and differences in litter ages within the groups were relatively small. Despite the wide range of parities within groups of observed sows, no effect of parity number on the presence of alien piglets or absence of own piglets and piglets' frequency of active cross-suckling was found. WuÈlbers-Mindermann (1992) and Olsen et al. (1998) observed higher incidence of cross-suckling among progeny of high-parity sows. Puppe and Tuchscherer (1995), to the contrary, recorded higher cross-suckling activity among piglets born to primiparous sows. The effect of parity, thus, remains unclear, but is probably less important than that of litter size and litter age. The sows in this study displayed an 82% nursing synchronisation. If the sows would nurse completely independently of each other, the estimated degree of synchronisation would amount to only 10%. Other authors also reported pronounced nursing synchronisation in multi-suckling systems (Bryant et al., 1983; Wechsler and Brodmann, 1996; Newberry and Wood-Gush, 1985). The nursing synchronisation among group-housed sows may have a considerable effect on piglets (cross)suckling behaviour (Bryant et al., 1983; GoÈtz et al., 1991; WuÈlbersMindermann, 1992; Wechsler and Brodmann, 1996; Wattanakul et al., 1997). It is important to differentiate how exactly the nursing bouts are synchronised because an even small temporal shift between two nursings can change the distribution of crosssuckling. The results indicate that if sows nurse quickly one after another, then the ®rst one to nurse attracts more piglets. Three indications that this is the case were found. First and second, the more sows that nursed just before a focal sow, the fewer alien piglets
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that participated in her nursing and the lower was the attendance of her own piglets in the nursing. Third, when the own mother of an occasional cross-suckler (a SS_OWN ALIEN piglet) nursed just before a potential stepmother, then the probability that this piglet would cross-suckle at the stepmother during her current nursing was reduced by 61%. However, this last relationship was not present in permanent cross-sucklers (SS_ALIENS piglets), which indicates that once a piglet ceases to suckle at its own mother, it is no longer in¯uenced by her behaviour. These results are in accordance with ®ndings of WuÈlbers-Mindermann (1992) that the opportunistic cross-sucklers (those which crosssuckled <35% of nursings) mostly cross-suckled in nursings when their own mother was not synchronised. These results appear to indicate that an ef®cient strategy for a sow to avoid cross-suckling attempts by alien piglets is to wait until another sow or sows begin nursing and then to start nursing herself. A high degree of synchronisation may a result if all sows follow this strategy so that when one of them starts a nursing, the others follow in a chain reaction. The number of nursings in which a piglet participated during the observation period was used as an indirect measure of success of the various (cross)suckling strategies. Because of the design of the experiment and de®nition of the cross-suckling categories, only two unbiased comparisons could be made. Piglets which chose one alien sow in place of their own mother (SS_1_ALIEN) attended a similar number of nursings as faithful piglets (SS_OWN) and permanent cross-sucklers at more than one sows (SS_MORE_ALIENS) achieved a similar number of sucklings as piglets with the opportunistic suckling strategy (SS_OWN ALIEN). Hence, according to this criterion, the three main categories of piglets (the faithful ones, the opportunistic and the permanent cross-sucklers) were equally successful at getting access to nursings. This suggests that in a multi-suckling system, the frequency of various suckling strategies eventually develop into a balance when all of them are equally pro®table. Overall, piglets in this study achieved the same number of sucklings as would be expected in a no-cross-suckling situation. This study, thus, suggests that, although crosssuckling may be frequent in stabilised multi-suckling group, this need not have an adverse effect on the overall milk intake of the piglets. Arey and Sancha (1996) found out that in the ``family group housing system'' (multi-suckling system) a high percentage of piglets was present at each suckling bout (96%), which is in accordance with our calculations for the average proportion of achievable nursings (96.5%). 5. Conclusions 1. Frequent cross-suckling (29% of all suckling events) was observed in a commercial multi-suckling system with small groups of sows at the fourth week of lactation. 2. Large litter size was the main determinant of cross-suckling, especially for permanent cross-sucklers. 3. Sows nursing immediately after other sows attracted less cross-suckling. High degrees of nursing synchrony observed in multi-suckling systems may result from attempts of sows to avoid cross-suckling through starting their nursing immediately after the other sows.
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