Influence of housing and social changes on growth, behaviour and cortisol in piglets at weaning.

The present experiment aimed at evaluating the relative effects of environmental and social changes on behaviour, growth and salivary cortisol of piglets at weaning. On Day 0, 26-day old piglets were weaned and allocated to one of four treatments: neither environmental nor social change (C), environmental change (E), social change (S), and both changes (SE). Overall, 6 replicates of 10-12 animals/pen/treatment were analysed. Piglets were video recorded during the first three days after weaning to observe social behaviour and general activity. Saliva was collected between 07:00 and 09:00 on Day 0 just before weaning (D0H7), on Day 1 (D1H7) and Day 2 (D2H7 and D2H16) to measure cortisol. Saliva cortisol did not change after weaning in C piglets but increased significantly at D1H7 in S and SE piglets, at D2H7 and D2H16 in E and SE piglets. Compared to C piglets, numerous behaviours were altered in SE piglets: more total lying (P<0.08), less lying on the belly, less environmental exploration, less playing, more fighting regardless the day, more lying awake inactive on Day 0 (P<0.05). Compared to C piglets, E piglets displayed more total lying but less environmental exploration whereas S piglets showed less lying on the belly but more fighting (P<0.05). Present results show that moving piglets to a new environment as well as mixing them with unfamiliar conspecifics at weaning have stressful effects which are additive.

Neuroendocrine consequences of very early weaning in swine.

An experiment was conducted to investigate the consequences of very early weaning of piglets on neuroendocrine variables and growth. Sixty piglets from eight litters were either weaned on Postnatal Day 6 (early weaning, or EW piglets) or left with their dam until normal weaning at Day 28 (control piglets, or C). At Days 5, 7, 11, 14, and 19, urine was collected between 7:00 and 8:00 a.m. for the measurement of catecholamines, glucocorticoids, and creatinine. Compared with C, EW piglets displayed a transient increase in urinary cortisol on the day following separation from their dam (Day 7) (P<.05). Urinary norepinephrine (NE) was three times lower in EW compared to C piglets from Day 7 until Day 14 (P<.01) but there was no difference between the two groups on Day 19. Urinary epinephrine (EPI) did not differ between C and EW piglets on the day after weaning. Thereafter, EW piglets displayed a three times drop in urinary EPI as compared to C piglets until the end of the period (P<.01). Weaning induced an immediate reduction in food intake and growth rate and at Day 28, the body weight of EW piglets was 1.60 kg lower than that of C piglets (P<.0001). In conclusion, weaning of 6-day-old piglets results in a marked and prolonged suppression of the release of catecholamines. This result likely reflects physiological responses to insufficient energy intake after weaning, as reflected also by changes in thermoregulatory behavior. The transient increase in cortisol excretion in weanlings may be caused by both emotional distress and acute food deprivation.

Behavioural, growth and immune consequences of early weaning in one-week-old large-white piglets.

Genetic improvement in sows' prolificity is limited by their milk capacities, which do not allow all piglets to survive or grow normally. This experiment compared the behaviour, growth and immune responses of piglets that were weaned early at 6 days of age (EW) vs. control Large White piglets' (C) suckled by their mothers. Behaviour of 9 litters of 5 to 8 piglets in each group were observed from d5 to d20. All piglets were weighed from birth to d74. Three piglets from each group were slaughtered on d36 for immunological analysis. Until they began to eat dry food, EW piglets walked and vocalised more than C piglets. After that time, when resting, they were less often lying down and more frequently in contact with littermates under the heater. Aggressive behaviour and belly-nosing were more frequent. They displayed a more marked growth check after weaning than did C piglets until 28 days of age. In EW piglets, at 36 days of age, there was a higher density of T- and B-lymphocytes in the gut epithelium and lamina propria, fespectively, in relation to the size of lymphoid follicles of Peyer's patches. The results indicate great behavioural adaptation capacities of very early-weaned piglets, together with earlier maturation of their gut immune system.

Role of mother-young interactions in the survival of offspring in domestic mammals.

The defining characteristic of mammals is that females nurse and care for their young; without this, the neonate has no chance to survive. Studies on wild and domestic species show that the neonatal period is the most critical step in the lifetime of a mammal. This review compares three well-studied species (the rabbit, pig and sheep) that differ in their parental strategies and in the problems that neonates have to overcome. As a general trend, mother-young interactions vary according to the maturity of the newborn, and the size of the litter. Neonatal survival relies to a great extent on an environment that is ecologically appropriate for the developmental stage of the neonate, and on optimum interactions with the mother. Adaptive maternal care supposes that the mother provides the basic needs of the neonate: warmth (in pigs and rabbits) or shelter, food, water and immunological protection (via colostrum) and, in some instances, protection from predators and other conspecifics. A major risk facing all neonates, other than the birth process itself, is inadequate colostrum intake owing to delayed suckling or competition with siblings, which leads to starvation, hypothermia or even crushing, as has been observed in pigs.

Learning of olfactory cues is not necessary for early lamb recognition by the mother.

Ewes identify their young through the use of different sensory modalities. Olfactory recognition, which mediates selective acceptance at the udder, is established at 4 h postpartum (pp). Visual and auditory cues are involved in recognition at a distance, which is evident at 12 h pp. This study investigates whether anosmic ewes are able (a) to develop visual and auditory recognition and (b) to restore selective acceptance of their lamb at the udder. Visual and auditory recognition was assessed in anosmic and intact ewes at 12 h and 24 h pp by a test of two choices: their own and an alien lamb. Selectivity at allowing suckling was tested by presenting successively an alien and the familiar lamb at 4 h, 3 days, and 1 month pp. In the two-choice recognition test, at both 12 h and 24 h pp, anosmic as well as intact ewes showed a preference for their familiar lamb. Although anosmic ewes showed no difference in their acceptance of alien and familiar lambs for suckling at 4 h and 3 days pp, they nursed the alien lamb less at 1 month pp and showed more rejection behaviors toward it. Thus, visual, auditory, or both those types of recognition can be rapidly established, independent of olfactory recognition. Moreover, differential behavior of anosmic ewes toward their own versus an alien lamb at the udder at 1 month suggests that vision and audition may compensate to some extent for the loss of olfaction.

Immediate postnatal sucking in the rabbit: its influence on pup survival and growth.

This study was aimed at characterising the impact of immediate postnatal sucking on pup survival and development. The interactive effects of postnatal success with the day 0 weight of pups, the nest-access regimen (controlled or free) or parity of females was investigated. Pups (n = 900) were categorised according to their initial ingestion of colostrum. In primiparous does: (1) pup mortality between d0-d10 was higher for unsuccessful than for successful early suckers; (2) lighter d0-weight reduced survival for unsuccessful but not for successful pups; (3) free nest-access of females annihilated the survival advantage fostered by the initial sucking success. In secondiparous does, these impacts waned. Finally, whatever the does' parity, only d0-weight influenced pup weight-gain between d0-21. Thus, pup survival seemed to depend (at least in primiparae) on their ability to suck right after birth, and to display a pattern of energy saving without being disturbed by the females' nest entries.

Psychobiological consequences of two different weaning methods in sheep.

Weaning is associated with a break in the mother-infant contact. In sheep, under natural conditions, the rupture of the social bond is progressive. In contrast, weaning imposed by breeders may result in psychobiological disturbances. The aim of this experiment was to measure the behavioural, hormonal and immune consequences of two types of sudden weaning: total separation (TS) and partial separation (PS), in 42 Ile-de-France ewes and their 60 lambs. TS animals (lambs and ewes) vocalized less frequently and for a shorter period of time than did the PS animals. Neither the plasmatic cortisol level in lambs nor the humoral response of dams and young were modified by the two weaning methods. In contrast, the excretion of coccidial oocysts increased significantly after weaning in TS lambs only and the growth rate of TS females was lower than that of the other lambs. These results suggest that these methods of rupture of mother-young social contact have only limited negative consequences on both partners in sheep, contrary to primates and rodents.

Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues?

Two studies were carried out to test the ability of Préalpes du Sud x Lacaune (Study 1) and Rambouillet ewes (Study 2) to recognize their lambs during the first 24 h postpartum. Ewes were given the choice between their own and an alien lamb of approximately the same age, in a triangular pen of 10 m×10 m×10 m. A lamb was placed in each of the two corners while the mother was released from the third corner. Direct access to the lambs was prevented by an open barrier located at 1 m from the pens in which the lambs were kept. Ewes were studied at 8 h (n=10, 12), 12 h (n=20, 10) and 24 h postpartum (n=29, 9; Study 1 and Study 2 respectively). Tests lasted 3 and 5 min in Study 1 and 2, respectively. Although the first choice of the ewes did not differ from random, in both studies mothers spent significantly more time near their own lamb than near the alien. In both breeds a significant preference for the own lamb was already present at 8 h (P<0.05). We conclude that ewes are very likely to recognize their lamb without the aid of olfactory cues as early as 8 h postpartum, which is much sooner than thought from previous studies.

Cholecystokinin receptors mediate the development of a preference for the mother by newly born lambs.

The aim of this study was to investigate the effect of selective cholecystokinin (CCK) antagonists on the development of a preference for the mother by newly born lambs. At birth lambs received an injection of the CCK-A antagonist devazepide (0.01 or 0.1 mg/kg), the CCK-B antagonist PD135158 (0.01 or 0.1 mg/kg), or saline for the controls (1 ml/kg). No major side effects were observed in the first 4 postnatal hours except that lambs receiving PD135158 displayed more exploratory behavior towards the maternal body than lambs from the other groups. When tested in a 2-choice test situation at 24 hr of age, lambs treated with PD135158 or saline spent significantly more time near their dams than near the alien ewes, whereas lambs treated with devazepide did not show any discrimination. The effect of devazepide persisted at 48 hr of age. The use of a CCK-A antagonist, but not a CCK-B antagonist, was concluded to prevent the formation of a preferential relationship between the lamb and its mother, most probably by impairing neonatal learning.

Plasma cholecystokinin concentrations in 3-day-old lambs: effect of the duration of fasting preceding a sucking bout.

Cholecystokinin (CCK) is a regulatory peptide released into the circulation after the ingestion of food. Our knowledge concerning the factors affecting its pattern of secretion in the mammalian neonate is scanty. Therefore, in this work we studied plasma concentrations of CCK in 3-day-old lambs after a sucking bout that followed either a short (2 h) or a long fasting period (9 h). Plasma concentrations of CCK were measured by radioimmunoassay in blood samples collected from jugular veins 10 min before, immediately after a sucking bout, and then at 10-min intervals during the following hour. In the first experiment a period of fasting of 2 h before allowing the lambs to suck did not lower the levels of CCK. On the other hand, a significant decrease was recorded 10 min after feeding ended. Between 20 and 50 min after the end of sucking, the mean CCK concentration rose back to the pre-feeding level before decreasing again at 60 min. In the second experiment a period of fasting of 9 h, on the other hand, significantly lowered the levels of CCK. Plasma levels also tended to decrease immediately after sucking was ended. This was followed by a substantial rise and levels remained high during the rest of the sampling period. It was concluded that the decrease recorded immediately after a sucking bout could be due to an inhibitory effect of the oral phase while the following rise reflected the stimulatory effect of milk nutrients on intestinal CCK-producing cells.

Gas chromatographic-mass spectrometric method to characterise the transfer of dietary odorous compounds into plasma and milk.

The flavours contained in a mammalian mother's milk can exert a marked influence on her offspring's proximate suckling behaviour and later preferences. The aim of this study was to establish a reliable analytical procedure to characterise the mammary transfer of selected volatile constituents of maternal food from non-pregnant and recently parturient ewes. Six known volatile compounds, most representative of cumin aroma (alpha-pinene, gamma-terpinene, cuminaldehyde, p-cymene, limonene and cineole), were traced in the blood and milk of ewes fed with cumin seeds, using liquid-liquid extraction combined with gas chromatography-specific ion monitoring mass spectrometry. Among the six cumin odour markers, only one, p-cymene, was transferred in quantifiable amounts into the venous plasma. The other cumin markers could only be detected as traces corresponding to amounts lower that the limit of quantification. In milk, four of the cumin markers could be detected, and two of these were quantified.

Sexual play behavior in lambs androgenized in utero.

In lambs, play behavior, mainly including male-like sexual behavior patterns, is observed during weeks 4-8 following birth. The higher frequency of this behavior in male lambs has no obvious relationships with secretions of testosterone during infancy. In our experiment, pregnant ewes received subcutaneous implants of testosterone on gestation day 50. The frequency of male-like sexual patterns did not differ reliably between female lambs born to treated ewes and male lambs born to treated or control ewes. However, the frequency was lower for female control lambs. These results suggest that sexually dimorphic social play in lambs is dependent on prenatal exposure, which seems to have a masculinized effect.

Olfaction mediates the establishment of selective bonding in goats.

Nine pregnant goats of the Creole breed were rendered anosmic 3 weeks before parturition by irrigating their olfactory mucosa with zinc sulfate, and nine additional pregnant goats were left intact. At parturition, interactions between all females and their young were observed for 1 h. No differences were found in mother-young relationships between intact and anosmic mothers during this time, except that kids from anosmic females were slower to suck than controls. After 4 h of uninterrupted mother-young, mothers underwent three successive 5-min tests in a predetermined order to study selective bonding: with their own kid, an alien kid of similar coat color and pattern, and an alien kid of dissimilar coat color and pattern. Intact goats readily discriminated between kids, and rejected the two aliens while accepting their own. By contrast, anosmic mothers showed no signs of discrimination and accepted the three types of kids. It is concluded that during the first postpartum hours of contact, mother goats memorize individual olfactory characteristics of their kid that serve as a basis for selective suckling and exclusive bonding. Furthermore, at this early stage, visual characteristics of the young do not appear able to compensate for the loss of olfactory cues.

Establishment of maternal bonding and its mediation by vaginocervical stimulation in goats.

To investigate the establishment of offspring recognition in mother goats, 11 females were subjected to two successive 5-min tests with their own kid and an alien, 2 h 30 min postpartum. All mothers accepted their own kid, while nine rejected the alien. This suggests that in goats, 2.5 h are sufficient for the development of an exclusive bond with the kid. We also studied the role of physiological factors mediating maternal bonding in this species. Eight of the nine goats that rejected alien kids were, therefore, submitted to 5 min of vaginocervical stimulation (VCS) immediately following the selectivity tests. Of these eight goats, five changed their behavior after VCS and accepted the alien kid (0/8 before VCS vs. 5/8 after VCS, p = 0.031). Thus, VCS appears to reduce rejection behavior towards alien kids while resulting in a significant increase in their rate of acceptance. Underlying physiological mechanisms by which VCS may act are discussed.

Olfaction in utero: can the rodent model be generalized?

In this article we discuss five requirements that theoretically must be fulfilled for transnatal chemosensory learning to occur in three placental species, the rat, the sheep, and the human, viz. (1) minimum or partial maturity of nasal chemoreceptor systems, (2) efficient odorivector compounds in the fetal environment, (3) the ability to memorize chemosensory information across birth, (4) perinatal continuity in chemical signals, (5) neonatal ability to detect air-borne odorants previously experienced in the aquatic environment. A substantial body of data is reviewed for the rat, in which fetal chemosensation is now firmly established. The less studied ovine perinate also shows preliminary evidence of nasal chemoreception and of postnatal retention of prenatally experienced odorants. Concerning the human species, we discuss extensive anatomical data supporting nasochemoreception in utero, but as yet no direct or indirect functional demonstration is provided. Furthermore, the strongest evidence of odorivector compounds in amniotic fluid is from human data. The results presented allow generalization of chemosensory functioning in utero in the species considered.

[Nasal chemoreception in utero: preliminary experiences in fetal sheep]. / Chimioréception nasale in utero: expériences préliminaires chez le foetus ovin.

Intranasal injections of a fragrant solution of 2-methyl-2-thiazoline elicited significant heart rate decelerations in late pregnancy fetal sheep, while the injection of a control fluid (isotonic saline) had no effect. This result indicates that the ovine fetuses are able to detect nasally administered odorants, as previously demonstrated in the fetuses of murine rodents.

Female effect in sheep. II. Role of volatile substances from the sexually receptive female; implication of the sense of smell.

The importance of olfactory cues in inducing luteinizing hormone and testosterone secretion as a response to stimulation by sexually receptive ewes has been tested. In sexually experienced rams, olfactory stimulation with urine, wool and vaginal secretions from sexually receptive females placed in a mask did not induce an endocrine response. The female-induced secretion of LH and testosterone was similar in anosmic, sham-operated and in control rams. These results show that olfactory cues are not necessary in the mediation of interindividual stimulation of endocrine response in the sexually experienced ram.

Female effect in sheep. I. The effects of sexual receptivity of females and the sexual experience of rams.

When in contact with receptive or non-receptive ewes, the presence of females increased LH peak frequency both in experienced and inexperienced rams (P less than 0.05). The highest response was found in experienced rams stimulated by sexually receptive ewes. In this group only, the mean testosterone levels increased during stimulation (P less than 0.05). Sexual behavior did not differ between experienced and inexperienced males. The sexual receptivity of the females and the sexual experience of rams appear to interact and thus facilitate the rams' LH and testosterone responses to the presence of ewes.

Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs.

Within a 4-hr period after parturition, the ewe learns the odor of her lamb that will allow later recognition of her offspring from alien lamb. This study investigated the importance of the activation of olfactory bulb (OB) beta-noradrenergic receptors in establishing this olfactory memory. Pregnant ewes (n = 24) were cannulated bilaterally in the OB. Two days before parturition, OB were perfused continuously (10 microliters/hr) with either a solution containing the selective beta-noradrenergic antagonist propranolol (10(-3) M) or vehicle. The results showed that, although 8 of 9 control ewes were still able to bond selectively to their lambs, only 7 of 15 propranolol-treated animals were able to bond (p = .04). These results suggest that activation of beta-noradrenergic receptors in the OB during the period surrounding parturition is required to establish olfactory recognition of the lamb.

Sexual differentiation of reproductive behavior in pigs: defeminizing effects of prepubertal estradiol.

The present study sought to determine (1) whether estrogen by itself can defeminize the behavior of pigs during the late juvenile-early pubertal period, and (2) whether the progressive late defeminization reported for pigs is a true organizational effect, as opposed to an artifact of the time between castration and testing. Male pigs were castrated at 19-22 days or left intact and females were ovariectomized at 3 months. Additional males castrated at 19-22 days and females ovariectomized at 3 months were implanted with estradiol benzoate (EB) from 3 to 5.5 months. After castration of the previously intact males at the age of 5.5 months, all subjects were tested beginning at 6.5 months for proceptivity (choice of a male versus a female in a T-maze) and receptivity (immobilization to a mounting male) following an injection of EB. EB administered during development significantly defeminized proceptivity and receptivity in both sexes. The decrease in proceptivity was more pronounced in males than in females and was more pronounced than the decrease in receptivity, as if differentiation ends earlier for proceptivity than for receptivity; the decrease in receptivity was more pronounced in females. To see whether the capacity to display female-typical behavior is a function of time since castration, we castrated additional males at 4 months and tested for receptivity 9 days later following an injection of EB, then tested again with the other subjects at 6.5 months. The proceptivity and receptivity scores for males castrated at 4 months fell between those for intact males and males castrated at 3 weeks, and thus these animals were not completely defeminized. They were more receptive at 6.5 months than at 4 months, but the difference was not significant. These results indicate that in pigs estradiol defeminizes both receptive and proceptive behavior and that this defeminization can occur relatively late in development.