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Sensory and physiological determinants of maternal behavior in the goat (Capra hircus)
Hormones and Behavior 52 (2007) 99 – 105 www.elsevier.com/locate/yhbeh
Sensory and physiological determinants of maternal behavior in the goat (Capra hircus) Pascal Poindron a,b,c,d,f,h,⁎, Angélica Terrazas e , María de la Luz Navarro Montes de Oca e , Norma Serafín f , Horacio Hernández g a
g
INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France b CNRS, UMR6175, F-37380 Nouzilly, France c Université de Tours, F-37041 Tours, France d Haras Nationaux, F-37380 Nouzilly, France e Facultad de Estudios Superiores Cuautitlán, UNAM, Km 2.5 Carretera Cuautitlán-Teoloyucan, Cuautitlán Izcalli, 54714 E. MEX, Mexico f Instituto de Neurobiología, Campus UNAM-UAQ Juriquilla Km. 15 Carretera Querétaro-San Luis Potosi, Querétaro 76230, QRO, Mexico Centro de Investigación en Reproducción Caprina, Departamento de Ciencias Médico Veterinarias, Universidad Autónoma Agraria Antonio Narro, Carretera a Santa Fe y Periférico A.P. 940, Torreón, Coahuila, Mexico h CIRA, CINVESTAV-UAT, AP 62, Tlaxcala TLAX 90000, Mexico Received 28 March 2007; revised 28 March 2007; accepted 29 March 2007 Available online 4 April 2007
Abstract Maternal behavior in the goat appears at the time of parturition, partly under the activating influence of vaginocervical stimulation. Mothers actively lick their neonate and rapidly establish a selective bond with their kid through olfactory recognition. They also develop visual and acoustic recognition of the kid within 4 h following birth. Acoustic recognition is present at 48 h. The establishment of maternal recognition can be impaired by underfeeding during the second half of pregnancy. There is no indication that the mechanisms controlling the onset of maternal behavior and bonding are different from those reported in sheep, despite the fact that lambs start to follow their mother within a few hours after birth and kids hide for about a week. During lactation, the cues provided by the kid are necessary for the maintenance of maternal responsiveness, but suckling itself does not appear of primary importance. The presence of the kid also modulates the hormonal response to udder stimulation and influences recovery of postpartum sexual activity when kidding (i.e. birthing) takes place in autumn. Finally, the rapid establishment of mutual attachment between mother goats (does) and their kids offers the possibility to investigate an aspect of mother–young affiliation that is not present in many laboratory species. © 2007 Elsevier Inc. All rights reserved. Keywords: Mother–young recognition; Olfaction; Hearing; Vaginal stimulation; Nursing; Undernutrition; Hider; Prolactin; Oxytocin; Sensitive period; Bonding; Attachment
Introduction Mother–young relationships in domestic ungulates are mainly characterized by the fact that mothers give birth to precocious neonates capable of a high degree of independent activity from birth, which differentiate them from most altricial laboratory species, whose young are relatively immobile and helpless at birth (e.g. rat, house mouse, rabbit; González-Mariscal and Poindron, ⁎ Corresponding author. UMR 6175, PRC, INRA, 37380 Nouzilly, France. E-mail address: [email protected] (P. Poindron). 0018-506X/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2007.03.023
2002; Nowak et al., 2000; Poindron et al., 2007). Also, two major types of mother–young relationships can be distinguished in ungulates. On the one hand, sows give birth to a large litter which is confined to a nest for several days, and fostering of alien young is relatively easy (Nowak et al., 2000). On the other hand cattle, sheep and goats give birth to one or few young; mothers do not build a nest and bond selectively to their own neonate (Nowak et al., 2000; Numan et al., 2006; Poindron et al., 2007). This bonding process in the mother has been regarded as an example of maternal attachment somewhat similar to that of filial imprinting in young birds and has been well studied in these species, but
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more particularly in the goat and even more so in the sheep (Herscher et al., 1963; Poindron et al., 2007). In this latter species, the establishment of maternal recognition and exclusive care of the neonate, as well as their physiological and neurobiological determinants has been the object of extensive research (Kendrick et al., 1997; Kendrick, 2000; Lévy et al., 1996; Nowak et al., 2007). Whether the characteristics and determinants of maternal care and bonding in the goat are similar to those found in sheep is a relevant question, given the differences of mother–young relationships existing between the two species once the mother leaves the birth site. Indeed, after the first postpartum hours of intense mother–young care at the birth site, the doe leaves her kids for several hours, while the young hide and wait for her to come back for nursing (Lent, 1974; Lickliter, 1984; O'Brien, 1984, 1988; Rudge, 1970). Lambs, in contrast, move along with their dam and remain close to her as soon as she leaves the birth site to join the rest of the flock and graze (Lent, 1974; Lynch et al., 1992; Nowak et al., 2000). It has been hypothesized that the different spatial mother–young relationships found in hiders and followers during the first days postpartum may be associated with differences in early abilities and underlying mechanisms of mother–young recognition in the two species (Gubernick, 1980, 1981; Lickliter and Heron, 1984). If this is the case, the physiological control of maternal care and bonding could also be different between species since bonding to the lamb depends on the facilitation of learning by physiological changes occurring at parturition (Kendrick et al., 1997; Kendrick, 2000; Lévy et al., 1996). While no direct comparisons between the two species have been carried out to examine this question, the data available in goats provide us with sufficient information to approach this question. After briefly describing the main behavioral characteristics of maternal behavior in the goat, we will review the physiological determinants of maternal behavior in this species, how the mother recognizes and bonds to her kid and how the presence of the young may influence maternal endocrinology during lactation. Main characteristics of goat maternal behavior Maternal behavior at parturition Prepartum isolation Preparturient females are typically wary and seek remote or concealed birth sites prior to parturition. Under free range conditions, goats tend to isolate themselves to give birth (O'Brien, 1983, 1984; Rudge, 1970). This is also the case under intensive farm management where females show increased restlessness, frequent vocalizations and increased intolerance of conspecifics (Das and Tomer, 1997; Lickliter, 1985; Sambraus and Wittmann, 1989). This tendency to isolation is associated with a clear decrease in gregariousness at parturition as goats show a marked reduction of their behavioral response to social isolation (i.e. agitation index) between 24 h and about 1 h prepartum (Fig. 1). Proper prepartum isolation without causing agitation is likely to help in the display of proper maternal care and bonding.
Fig. 1. Change of behavioral response to social separation in preparturient goats. The response to social separation is expressed as a median agitation index and interquartile range (vertical bars), obtained by subtracting the agitation score obtained before from that obtained after withdrawal of the rest of the group from the pen where the animals lived. Agitation scores were obtained by summing numbers of squares crossed, vocalizations, jumps, attempts to jump, mictions and defecations over a 5 min period (see Poindron et al., 1997 for details of procedure). All groups were independent. Test at parturition was performed after rupture of the waterbag or sight of the fetus' hooves, whichever occurred first. Also, goats in this group gave birth either on day 150 or day 151 of pregnancy, i.e. less than 24 h after the corresponding test for the group at day 150. ⁎: Response of parturition group significantly lower than in any other group (Mann–Whitney, P b 0.025), the other pregnant groups not differing one from another or from the non-pregnant controls. This decrease in the agitation score was not due only to a reduction in motor activity, but also to a significant reduction of high-pitched bleats (two- to three-fold decrease), another key indicator of agitation. It is also important to mention that the overall weight of vocal activity in the index is higher than that of motor activity and that, even in the middle of the parturition process, goats are perfectly able to walk.
Immediate maternal care to the neonate In the goat, most births occur during day time (over 80% between 06:00 and 20:00; Allan et al., 1991; Das and Tomer, 1997; Lickliter, 1985). During parturition does usually lie down, and in some instances they lick the udder and teats. A few minutes after expulsion of the fetus the mother rises and starts to lick her kid vigorously, generally beginning with its head and neck (Collias, 1956; Lickliter, 1985). Licking is accompanied by numerous low and high pitched bleats and occasionally by flehmen behavior, especially when consuming urine from the neonate (Sambraus and Wittmann, 1989). There is little information concerning differential care of male and female neonates in sheep and goats, but preliminary results suggest that does may preferentially lick males more than females and that this difference relies on olfactory information since it is abolished in anosmic mothers (Serafin et al., 2003). The neonate tries to stand up within 5–10 min after birth and usually succeeds in doing so by 20 to 30 min. In less than 1 h after birth, the neonate finds the mother's udder by trial and error exploration and begins to feed (Allan et al., 1991; Collias, 1956). Establishment of neonate recognition and selective bonding Olfactory recognition of the kid and selective bonding Goats, like sheep, rapidly develop an exclusive maternal bond with their neonate(s). Immediately after parturition,
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mothers groom and nurse any kid, but then rapidly learn to discriminate and nurse only their own young (Collias, 1956; Herscher et al., 1963). In some conditions, 5 to 10 min of contact with the neonate are sufficient for does to become selective (Gubernick, 1981) and most mothers reject alien kids at 2 to 4 h postpartum, regardless of their age or the similarity of their coat to that of their own young (Romeyer and Poindron, 1992; Romeyer et al., 1994a). This selective nursing depends primarily on the main olfactory system since prepartum peripherally induced anosmia, which affects only the main olfactory system, prevents the establishment of selective nursing (Lévy et al., 2004; Poindron et al., 2007). There is some evidence suggesting that selectivity may result from olfactory labeling of the kid by the mother through licking and nursing (Gubernick, 1981), at variation with sheep in which the recognition of the lamb depends on its individual olfactory signature (Lévy et al., 2004). Nonetheless, in undisturbed conditions (i.e. without postpartum separation before testing), selective acceptance and nursing of the own young by its postparturient dam clearly depends on the learning by the doe of some individual olfactory signature of the kid during the first hours of mother–young interaction. Even twins have different olfactory signatures (Romeyer et al., 1993, 1994a). This olfactory learning process is modulated by vaginocervical stimulation and involves the main olfactory system, even though some role of the vomeronasal organ and accessory system cannot be excluded (Poindron et al., 2007; Romeyer et al., 1994a). Non-olfactory recognition of the kid. Some authors have suggested that mothers are not able to recognize their kids by sight or hearing before 2 to 5 days postpartum (Addae et al., 2000; Awotwi et al., 2000; Lenhardt, 1977). Nonetheless, there is growing evidence that does can already discriminate between their own kid and an unfamiliar one at 4 h postpartum without the help of olfactory cues (Poindron et al., 2003). In addition, they can make such a discrimination on the basis of only acoustic cues at 48 h, possibly due to the existence of an individual acoustic signature in the kids' bleats at that age (Terrazas et al., 2003). However, this non-olfactory recognition of the kid does not appear to be essential for the establishment and maintenance of selective nursing in the postparturient doe. Anosmic goats will accept unfamiliar kids as rapidly as intact mothers despite the fact that they are able to identify their own young with the help of visual and acoustic cues (Poindron et al., 2003). Recent results suggest that the establishment of the visual and/or acoustic recognition of the kid may be influenced by the level of maternal nutrition in late pregnancy (Terrazas et al., 2004 and unpublished results). The relevance of early visual and acoustic recognition of the young for the survival of the kid remains to be investigated in goats. In sheep, acoustic communication appears important for the early survival of the lamb (Nowak, 1990), which makes adaptive sense since ewes and lambs ambulate soon after birth and have to maintain close contact. Kids, on the other hand, do not walk much during the first days of their life due to their hiding behavior (see below). However, as olfactory recognition works only at very short distances (b1 m; Poindron et al., 2003), acoustic and visual
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recognition may still be important to locate the hiding or “lyingout” site of the kid. Strategy around the birth site: the hiding behavior of kids Parturition and lying-out sites are usually located in areas heavily used by the herd and close to the traditional night camp (O'Brien, 1983). Also, lying-out sites tend to be under cover, with relatively low wind velocity and light intensity, close to or adjacent to vertical objects. Mothers visit and nurse their kids only a few times per day (O'Brien, 1984). In the wild, the timing and extent of the hiding phase appear to vary among studies. Field studies of wild and feral goat populations indicate that newborn goats spend their first 3–4 days lying alone at a considerable distance from their mothers (McDougall, 1975; Rudge, 1970). In other instances, however, kids were found to remain with their mother for a few days before displaying hiding behavior, which continues up to about 6 weeks of age (McDougall, 1975). Also, some dams maintain a considerable distance from their young (leavers), while others remain in the vicinity of the site where the young hides after nursing (stayers; O'Brien, 1984). This plasticity in postpartum behavior may have strong selective advantages in feral goats, which occupy a range of habitats or are exposed to varying predation pressures (O'Brien, 1984). The hiding behavior of kids can also be observed in domesticated goats and under intensive farm management conditions, showing that hiding behavior has not been lost due to domestication. Newborn kids move away from their mother and birth site 15–26 h after parturition and spend most of their time secluded from congeners for 4 to 7 days. Physical mother– young contact at the time of reunion is generally initiated by the kids (Lickliter, 1984). Nonetheless, in intensive management conditions, frequencies of nursing appear higher than those reported in feral goats (Delgadillo et al., 1997), possibly as a result of confinement and reduced opportunity for the mother to move far away from her kid(s). Activation of maternal behavior at parturition Physiological factors If immediately separated from their neonate, parturient goats display maternal behavior spontaneously only for a short time after giving birth, although the duration of this period of initial responsiveness towards the neonate is longer in multiparous mothers (Lickliter, 1982). This indicates the existence of a sensitive period for the establishment of the relationship between the newborn kid and its mother (Herscher et al., 1963; Poindron et al., 2007) and suggests that it is controlled by some physiological factors associated with parturition. However, attempts to identify these factors have met with little success so far. The changes of concentration in estrogen and progesterone in the goat during late pregnancy and parturition are very similar to those found in sheep, in which these hormones play an important role in the display of maternal behavior (Poindron et al., 2007). However, an exogenous treatment of estradiol and progesterone that induces lactation and
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Fig. 2. Impairment of maternal behavior by peridural anesthesia in the parturient goat and its recovery following vaginocervical stimulation (VCS). A: Display of maternal behavior in goats receiving a peridural anesthesia just before expulsion of the fetus (Late Peridural, control group n = 12; see text for details), or when peridural was applied at the first signs of labor (Early Peridural, n = 9). Licking latencies in the first 3 h following parturition. Bleating activity for the first 30 min postpartum. B: Facilitation of maternal behavior by 5 min of artificial vaginocervical stimulation applied after the 7 non-responding mothers in part A (see text) had recovered from the peridural anesthesia, as evidenced by recovery of hind legs motor activity. Mothers were observed for 30 min before and 30 min after VCS. A: Mann–Whitney tests; B: Wilcoxon tests, with unidirectional hypotheses of a negative effect of peridural anesthesia and of a positive effect of VCS. Values are medians (histograms) and interquartiles ranges (vertical bars). P: one-tail probabilities. Fq/30 min: frequency of behavior per 30 min.
facilitates maternal behavior in non-pregnant ewes is ineffective in the goat (Rosenblatt and Siegel, 1981). The alternative of inducing maternal behavior with treatments mimicking more closely the hormonal changes occurring at parturition has not been investigated. The possibility that vaginocervical stimulation (VCS) resulting from delivery of the fetus may be involved in activating maternal behavior was explored by blocking the corresponding sensory inputs with peridural anesthesia in primiparous/inexperienced and in multiparous/experienced mothers (Poindron et al., 1998). The experimental design and methods were similar to those of Krehbiel et al. (1987) and Lévy et al. (1992) in sheep. In contrast to sheep, the effects of blocking VCS did not differ between primiparous and multiparous mothers. Peridural anesthesia applied at the first signs of labor (Early Peridural EP, on average 1 h 30 min prepartum) impaired the display of maternal behavior at parturition more strongly than when it was applied 15 min before fetus expulsion (Late Peridural, LP; Fig. 2). In this latter group, which served as control, most mothers behaved as parturient goats normally do, with short latencies to initiate licking, intense grooming and emission of numerous low-pitched bleats. Nonetheless, even in the LP group some females failed to display maternal behavior (EP: 4/9; LP: 3/12), resulting in non significant differences between groups (Fig. 2). The facilitating action of VCS is also supported by the effects of VCS applied after recovery from the peridural anesthesia in the seven mothers that did not show maternal behavior at parturition. While none of these 7 mothers
had shown maternal behavior during the first 30 min after recovering their motor ability, they all displayed some licking and/ or low pitched bleats during the following 30 min after artificial VCS (Fig. 2). This was particularly obvious in one mother, in which aggressive behavior disappeared immediately after VCS while licking of the neonate was triggered (Fig. 3). Further evidence for a role of VCS in the control of maternal behavior in the goat comes from its effects on maternal selectivity. Goats, like ewes, bond rapidly to their neonate(s). Two hours after parturition, most mothers actively reject kids they have not interacted with (Romeyer et al., 1994b). However, 5 min of artificial VCS applied at 2 h postpartum allows the acceptance of an unfamiliar kid in more than half of the mothers that were rejecting it just before VCS (Romeyer et al., 1994b). Therefore, VCS inhibits the display of maternal selectivity in the goat as it does in sheep and facilitates the establishment of a new bond. These results are similar to those reported in the ewe. It seems therefore reasonable to hypothesize that the establishment of maternal selectivity in the goat also depends on the learning of individual phenotypic cues from the kid, under the facilitation of physiological factors, as already shown in the ewe (Lévy and Fleming, 2006). Sensory cues Maternal olfaction plays an important role in the control of maternal behavior in the immediate postpartum period in two complementary ways. First, it is important that the mother has access to the olfactory cues provided by licking of the neonate. About half of does prevented from licking their kid during the first 4 h postpartum fail to show adequate maternal care when reunited with their young (Bordi et al., 1994; Romeyer et al., 1993). Second, this full access to olfactory cues through licking facilitates the establishment of maternal selectivity. Of the mothers that remain maternal despite 4 h of licking deprivation, half fail to be selective and still accept alien kids, in contrast to mothers that have fully interacted with their neonate during the same period. As a whole, these results may suggest an involvement of the
Fig. 3. Individual example of the recovery of maternal behavior by vaginocervical stimulation (VCS) in a goat having received a peridural anesthesia 15 min before the expulsion of the fetus (Late Peridural Anesthesia, LPA). VCS was applied about 2 h 30 min postpartum, more than 30 min after motor recovery from PA. For more details see text and Krehbiel et al. (1987). Li: licking time (s/30 min); LB: lowpitched bleats (frequency/30 min): AB: aggressive behavior (frequency/30 min); Nu: nursing time (s/30 min).
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vomeronasal system in the control of maternal behavior and selectivity at parturition in the goat (Poindron et al., 2007). Regulation of maternal behavior and physiology during lactation Influence of the kid on the maintenance of maternal behavior Once the hiding phase has ended, kids suckle about twice per hour, with a progressive decrease as they get older (Delgadillo et al., 1997). While nursing rhythms decrease over time, synchrony between the activities of the mother and her young may increase (Lickliter, 1987), which is characteristic of hider species. In addition, kids may gather in peer groups or crèches (Lickliter, 1987) that may be important for the acquisition of food preferences, together with transmission of food choice by the mother (Biquand and Biquand-Guyot, 1992). There is little information concerning the relationship between does and their kids during late lactation and weaning, which appears to take place in the wild between 3 and 6 months of age (Collias, 1956; Herscher et al., 1963). In any case, the presence of the young is critical for the maintenance of maternal behavior during lactation. Thus, in a recent study (see Fig. 4), we found that 2 weeks of total separation from the kid at 3 months postpartum (groups 3 and 4) led to a significant decrease in the time that dams nurse their kid or the proportion of dams doing so, in comparison to mothers in which some contact was maintained (groups 1 and 2). The actual stimulation of suckling was not necessary to maintain maternal responsiveness since nursing time and the proportion of goats accepting their kid were in fact highest in mothers that could see, hear and smell their kids, but could not nurse them (group 2, Fig. 4). These results indicate also that the state of lactation itself is not sufficient to maintain maternal responsiveness since acceptance was lowest in mothers totally separated from their kid, despite the maintenance of lactation by milking (group 4, Fig. 4). Finally, among the nine mothers (out of 33) that kept accepting their own kid after 15 days of total separation, none accepted an alien kid, indicating that recognition was still present at that time in these mothers.
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Limiting the duration of daily mother–young interactions can also influence maternal endocrinology and milk production. Mothers that are allowed only 5 h of contact per day with their kid display higher basal and post-suckling concentrations of PRL and growth hormone (GH) than mothers in permanent contact with their kids, or mothers that are totally separated from them and milked (Hernandez et al., in press). Such a restriction of mother– young contact, when associated with one daily milking, allows extra collection of milk without severe impact on kid growth, illustrating the great flexibility of the nursing rhythms of mothers and their kids. Recovery of maternal ovarian activity is another parameter that can also be influenced by the presence of the young. As in several other ruminants (e.g. sheep), goats display a period of postpartum sexual rest, also called postpartum anestrus. Under temperate and subtropical latitudes, this period normally coincides with the seasonal inhibition of reproduction in spring. Therefore, postpartum anestrus per se can only be studied in females that give birth in autumn. In this case, the presence of the kid and/or suckling can delay the recovery of sexual activity (Delgadillo et al., 1997, 1998). The selective bond between the doe and her kid(s) does not seem critical in the control of postpartum anestrus. Preventing the
Influence of the kid on maternal postpartum physiology As in other mammals, presence of the kid and nursing have a number of consequences on maternal physiology. Some mothers can respond with an increase in peripheral OT levels following exposure to olfactory, acoustic or visual cues from their kids (McNeilly, 1972). In addition, maternal selectivity modulates the release of OT during nursing, while PRL release does not appear to depend on this aspect of maternal behavior (Hernández et al., 2002). Indeed, in this study, intact/selective mothers showed a peripheral increase of OT only in response to suckling by their own kid but not by an alien. In contrast, in anosmic/non-selective mothers OT levels increased in response to suckling by either their own or an alien kid. PRL release, on the other hand, was present in intact mothers regardless of the identity of the kid that suckled. This PRL release also occurred in anosmic dams, although the response was lower than in intact mothers.
Fig. 4. Maintenance of maternal behavior in mixed breed goats undergoing 2 weeks of various degrees of separation from their kids at 3 months of lactation. From left to right: Controls (group 1), no mother–young separation; No suckling allowed (group 2), mothers and kids were separated by an openwork fence preventing nursing, but mothers could see, hear and smell their young, and the udder was emptied every third day by cannulation; Total Separation from kids (group 3), udder emptied every third day by cannulation; Total separation from kids and one daily machine milking (group 4). The mothers' acceptance of their own kid and of an alien kid (not shown —see text) was tested individually in a 5 min behavior test at the end of the 15 days of treatment. Mann–Whitney and Fisher exact probabilities. For a given variable, bars with different letters indicate a significant difference between the corresponding groups. All probabilities are two-tailed. Note the general effect of the presence of the young (groups 1 + 2 vs groups 3 + 4 ). x⁎: P = 0.084.
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establishment of maternal selectivity through peripheral anosmia before kidding did not result in reducing its duration (Hernández et al., 2004), contrary to what has been reported in cattle (Griffith and Williams, 1996).
the two referees and Prof. D. Krehbiel for their comments and help in correcting the manuscript.
Conclusions
Addae, P.C., Awotwi, E.K., Oppong-Anane, K., Oddoye, E.O.K., 2000. Behavioural interactions between West African dwarf nanny goats and their single-born kids during the first 48 hours post-partum. Appl. Anim. Behav. Sci. 67, 77–88. Allan, C.J., Holst, P.J., Hinch, G.N., 1991. Behaviour of parturient Australian bush goats. I. Doe behaviour and kid vigour. Appl. Anim. Behav. Sci. 32, 55–64. Awotwi, E.K., Oppong-Anane, K., Addae, P.C., Oddoye, E.O.K., 2000. Behavioural interactions between West African dwarf nanny goats and their twin-born kids during the first 48 h post-partum. Appl. Anim. Behav. Sci. 68, 281–291. Biquand, S., Biquand-Guyot, V., 1992. The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus). Appl. Anim. Behav. Sci. 34, 231–245. Bordi, A., De Rosa, G., Napolitano, F., Litterio, M., Marino, V., Rubino, R., 1994. Postpartum development of the mother–young relationship in goats. Appl. Anim. Behav. Sci. 42, 145–152. Collias, N.E., 1956. The analysis of socialization in sheep and goats. Ecology 37, 228–239. Das, N., Tomer, O.S., 1997. Time pattern on parturition sequences in Beetal goats and crosses: comparison between primiparous and multiparous does. Small Rumin. Res. 26, 157–161. Delgadillo, J.A., Poindron, P., Krehbiel, D., Duarte, G., Rosales, E., 1997. Nursing, suckling and postpartum anoestrus of creole goats kidding in January in subtropical Mexico. Appl. Anim. Behav. Sci. 55, 91–101. Delgadillo, J.A., Flores, J.A., Villarreal, O., Flores, M.J., Hoyos, G., Chemineau, P., Malpaux, B., 1998. Length of postpartum anestrus in goats in subtropical Mexico: effect of season of parturition and duration of nursing. Theriogenology 49, 1209–1218. González-Mariscal, G., Poindron, P., 2002. Parental care in mammals: immediate internal and sensory factors of control. In: Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrfbach, S.E., Rubin, R.T. (Eds.), Hormones, Brain and Behavior, vol. 1. Academic Press, New York, pp. 215–298. Griffith, M.K., Williams, G.L., 1996. Roles of maternal vision and olfaction in suckling-mediated inhibition of luteinizing hormone secretion, expression of maternal selectivity, and lactational performance of beef cows. Biol. Reprod. 54, 761–768. Gubernick, D.J., 1980. Maternal “imprinting” or maternal “labelling” in goats. Anim. Behav. 28, 124–129. Gubernick, D.J., 1981. Parent and Infant attachment in mammals. In: Gubernick, D.J., Klopfer, P.H. (Eds.), Parental Care in Mammals. Plenum Press, New-York, pp. 243–305. Hernández, H., Serafín, N., Terrazas, A., Marnet, P.G., Kann, G., Delgadillo, J.A., Poindron, P., 2002. Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats. Horm. Behav. 42, 232–244. Hernández, H., Delgadillo, J.A., Serafin, N., Rodriguez, A.D., Poindron, P., 2004. Prepartum peripherally-induced hyposmia does not reduce postpartum anoestrus duration in nursing goats. Reprod. Nutr. Dev. 44, 251–259. Hernandez, H., Delgadillo, J.A., Flores J.A, Rodríguez, A.D., Serafín, N., Kann, G., Marnet, P.G., Poindron, P., in press. Effects of restricted nursing on milk production and collection, kid growth and plasma prolactin and growth hormone concentrations in dairy goats. Animal. Herscher, L., Richmond, J.B., Moore, A.U., 1963. Maternal behavior in sheep and goats. In: Rheingold, H.L. (Ed.), Maternal Behavior in Mammals. John Wiley and Sons Inc., New-York, pp. 203–232. Kendrick, K.M., 2000. Oxytocin, motherhood and bonding. Exp. Physiol. 85, 111–124. Kendrick, K.M., Da Costa, A.P., Broad, K.D., Ohkura, S., Guevara, R., Lévy, F., Keverne, E.B., 1997. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44, 383–395. Krehbiel, D., Poindron, P., Lévy, F., Prud'Homme, M.J., 1987. Peridural anesthesia disturbs maternal behavior in primiparous and multiparous parturient ewes. Physiol. Behav. 40, 463–472.
As a whole, our understanding of the mechanisms that control the activation of maternal responsiveness in the goat remains somewhat fragmentary. Nonetheless, in light of the results concerning the effects of VCS on the onset of maternal behavior, these mechanisms do not appear fundamentally different from those existing in sheep (see Nowak et al., this issue), even though the endocrine factors involved remain to be identified. Similarly, the establishment of recognition of the neonate, the control of maternal selectivity and the sensory cues involved do not seem to differ between the two species. Therefore, the difference of mother–young spatial relationships developed during the early postpartum period in goats, which give birth to hider neonates and in sheep, which give birth to followers, does not seem to be associated with different proximate factors controlling maternal responsiveness and bonding. It is possible that the selection pressure resulted from the combination of two main factors common to the two species, a very mobile neonate and a strong gregarious tendency in the mother. Alternatively, it cannot be excluded that the lack of differences between the two species may result from domestication, which imposed similar environmental constraints on both of them, resulting in the fading of differences existing in their wild ancestors. However, this second possibility is less likely, given that domestication has not suppressed hiding behavior in kids or following in lambs. Further studies on wild hider and follower ungulates with varying degrees of gregariousness would help to clarify the possible weight of these factors on the evolution of maternal behavior and bonding mechanisms. Finally, comparative studies of the development of filial and maternal attachment in sheep and goats certainly represent an excellent opportunity to investigate the mechanisms controlling the affective aspect of bonding. In these two species, the mother and the neonate develop an affective individual bond, but the time course of its establishment is quite different. Ewes and lambs respond to separation from each other within hours and independently of the nursing pattern due to the follower nature of the relationships. Goats and kids, on the other hand, probably take longer to develop a distress response to mother–young separation because of the hiding tendency of the kid and also because the response to separation is inhibited by nursing (Addae et al., 2000). Therefore, a comparative investigation of the establishment of the distress response to separation and of its neurobiological control would certainly provide valuable information for the understanding of affective behavior in general. Acknowledgments Most of the unpublished results presented in this review were obtained at the Instituto de Neurobiologia de la UNAM, Campus Juriquilla, Queretaro with support of PAPIIT IN217205 and IFS grant B/3872-1. The authors are grateful to
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P. Poindron et al. / Hormones and Behavior 52 (2007) 99–105 Lenhardt, M.L., 1977. Vocal contour cues in maternal recognition of goat kids. Appl. Anim. Ethol. 3, 211–220. Lent, P.C., 1974. Mother–infant relationship in ungulates. In: Geist, V., Walther, F. (Eds.), The Behaviour of Ungulates and Its Relation to Management. U.I.C.N., Morgues, Switzerland, pp. 14–55. Lévy, F., Fleming, A.S., 2006. The neurobiology of maternal behavior in mammals. In: Marshall, P.J., Fox, N.A. (Eds.), The Development of Social Engagement. Neurobiological Perspectives. Oxford University Press, New York, pp. 197–246. Lévy, F., Kendrick, K.M., Keverne, E.B., Piketty, V., Poindron, P., 1992. Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behav. Neurosci. 106, 427–432. Lévy, F., Kendrick, K., Keverne, E.B., Porter, R.H., Romeyer, A., 1996. Physiological, sensory and experiential factors of parental care in sheep. Adv. Study Behav. 25, 385–473. Lévy, F., Keller, M., Poindron, P., 2004. Olfactory regulation of maternal behavior in mammals. Horm. Behav. 46, 284–302. Lickliter, R.E., 1982. Effects of a post-partum separation on maternal responsiveness in primiparous and multiparous domestic goats. Appl. Anim. Ethol. 8, 537–542. Lickliter, R.E., 1984. Mother–infant spatial relationships in domestic goats. Appl. Anim. Behav. Sci. 13, 93–100. Lickliter, R.E., 1985. Behavior associated with parturition in the domestic goat. Appl. Anim. Behav. Sci. 13, 335–345. Lickliter, R.E., 1987. Activity patterns and companion preferences of domestic goat kids. Appl. Anim. Behav. Sci. 19, 137–145. Lickliter, R.E., Heron, J.R., 1984. Recognition of mother by newborn goats. Appl. Anim. Behav. Sci. 12, 187–192. Lynch, J.J., Hinch, G.N., Adams, D.B., 1992. The Behaviour of Sheep. Biological Principles and Implications for Production. C.A.B. International, Oxon, U.K. McDougall, P., 1975. The feral goats of Kielderhead Moor. J. Zool. London 126, 215–246. McNeilly, A.S., 1972. The blood levels of oxytocin during suckling and handmilking in the goat with some observations on the pattern of hormone release. J. Endocrinol. 52, 177–188. Nowak, R., 1990. Lamb's bleats: important for the establishment of the mother– young bond? Behaviour 115, 14–29. Nowak, R., Porter, R.H., Levy, F., Orgeur, P., Schaal, B., 2000. Role of mother–young interactions in the survival of offspring in domestic mammals. Rev. Reprod. 5, 153–163. Nowak, R., Keller, M., Val-Laillet, D., Lévy, F., 2007. Perinatal visceral events and brain mechanisms involved in the development of mother young bonding in sheep. Horm. Behav. 52, 92–98, doi:10.1016/j. yhbeh.2007.03.021. Numan, M., Fleming, A.S., Levy, F., 2006. Maternal behavior, In: Neill, J.D. (Ed.), Third edition. The Physiology of Reproduction, vol. 2. Elsevier, New York, pp. 1921–1993.
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O'Brien, P.H., 1983. Feral goat parturition and lying-out sites: spatial, physical and meteorological characteristics. Appl. Anim. Ethol. 10, 325–339. O'Brien, P.H., 1984. Leavers and stayers: maternal post-partum strategies in feral goats. Appl. Anim. Behav. Sci. 12, 233–243. O'Brien, P.H., 1988. Feral goat social organization: a review and comparative analysis. Appl. Anim. Behav. Sci. 21, 209–221. Poindron, P., Soto, R., Romeyer, A., 1997. Decrease of response to social separation in preparturient ewes. Behav. Processes 40, 45–51. Poindron, P., Hernandez, H., Navarro, M.L., Gonzalez, F., Delgadillo, J.A., Garcia, S., 1998. Relaciones madre-cria en cabras. Proceedings of the XIII Reunion Nacional Sobre Caprinocultura, San Luis Potosi. University of San Luis Potosi, Mexico, pp. 48–66. Poindron, P., Gilling, G., Hernandez, H., Serafin, N., Terrazas, A., 2003. Early recognition of newborn goat kids by their mother: I. Nonolfactory discrimination. Dev. Psychobiol. 43, 82–89. Poindron, P., Keller, M., Lévy, F., 2007. Maternal responsiveness and maternal selectivity in domestic sheep and goats: the two facets of maternal attachment. Dev. Psychobiol. 49, 54–70. Romeyer, A., Poindron, P., 1992. Early maternal discrimination of alien kids by post-parturient goats. Behav. Processes 26, 103–112. Romeyer, A., Porter, R.H., Lévy, F., Nowak, R., Orgeur, P., Poindron, P., 1993. Maternal labelling is not necessary for the establishment of discrimination between kids by recently parturient goats. Anim. Behav. 46, 705–712. Romeyer, A., Poindron, P., Orgeur, P., 1994a. Olfaction mediates the establishment of selective bonding in goats. Physiol. Behav. 56, 693–700. Romeyer, A., Poindron, P., Porter, R.H., Lévy, F., Orgeur, P., 1994b. Establishment of maternal bonding and its mediation by vaginocervical stimulation in goats. Physiol. Behav. 55, 395–400. Rosenblatt, J.S., Siegel, H.I., 1981. Factors governing the onset and maintenance of maternal behavior among nonprimate mammals. In: Gubernick, D.J., Klopfer, P.H. (Eds.), Parental Care in Mammals. Plenum Press, New-York, pp. 13–76. Rudge, M.R., 1970. Mother and kid behaviour in feral goats (Capra hircus L.). Z. Tierpsychol. 27, 687–692. Sambraus, H.H., Wittmann, M., 1989. Observations of the birth and suckling behavior of goats. Tierarztl. Prax. 17, 359–365. Serafin, N., Terrazas, A., Hernandez, H., Paredes, A., Poindron, P., 2003. Maternal behavior of intact and anosmic parturient goats. Poster presented at the International Ethological Conference, Florianapolis, Brasil. Terrazas, A., Serafin, N., Hernandez, H., Nowak, R., Poindron, P., 2003. Early recognition of newborn goat kids by their mother: II. Auditory recognition and evidence of an individual acoustic signature in the neonate. Dev. Psychobiol. 43, 311–320. Terrazas, A., Robledo, V., Serafin, N., Poindron, P., 2004. Goat–Kid Mutual Recognition in the First Day after Birth are Affected by Maternal Undernutrition in Pregnancy. Paper Presented at the Congress of the International Society of Applied Ethology. Helsinski, Finland.
Sensory and physiological determinants of maternal behavior in the goat (Capra hircus) Pascal Poindron a,b,c,d,f,h,⁎, Angélica Terrazas e , María de la Luz Navarro Montes de Oca e , Norma Serafín f , Horacio Hernández g a
g
INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France b CNRS, UMR6175, F-37380 Nouzilly, France c Université de Tours, F-37041 Tours, France d Haras Nationaux, F-37380 Nouzilly, France e Facultad de Estudios Superiores Cuautitlán, UNAM, Km 2.5 Carretera Cuautitlán-Teoloyucan, Cuautitlán Izcalli, 54714 E. MEX, Mexico f Instituto de Neurobiología, Campus UNAM-UAQ Juriquilla Km. 15 Carretera Querétaro-San Luis Potosi, Querétaro 76230, QRO, Mexico Centro de Investigación en Reproducción Caprina, Departamento de Ciencias Médico Veterinarias, Universidad Autónoma Agraria Antonio Narro, Carretera a Santa Fe y Periférico A.P. 940, Torreón, Coahuila, Mexico h CIRA, CINVESTAV-UAT, AP 62, Tlaxcala TLAX 90000, Mexico Received 28 March 2007; revised 28 March 2007; accepted 29 March 2007 Available online 4 April 2007
Abstract Maternal behavior in the goat appears at the time of parturition, partly under the activating influence of vaginocervical stimulation. Mothers actively lick their neonate and rapidly establish a selective bond with their kid through olfactory recognition. They also develop visual and acoustic recognition of the kid within 4 h following birth. Acoustic recognition is present at 48 h. The establishment of maternal recognition can be impaired by underfeeding during the second half of pregnancy. There is no indication that the mechanisms controlling the onset of maternal behavior and bonding are different from those reported in sheep, despite the fact that lambs start to follow their mother within a few hours after birth and kids hide for about a week. During lactation, the cues provided by the kid are necessary for the maintenance of maternal responsiveness, but suckling itself does not appear of primary importance. The presence of the kid also modulates the hormonal response to udder stimulation and influences recovery of postpartum sexual activity when kidding (i.e. birthing) takes place in autumn. Finally, the rapid establishment of mutual attachment between mother goats (does) and their kids offers the possibility to investigate an aspect of mother–young affiliation that is not present in many laboratory species. © 2007 Elsevier Inc. All rights reserved. Keywords: Mother–young recognition; Olfaction; Hearing; Vaginal stimulation; Nursing; Undernutrition; Hider; Prolactin; Oxytocin; Sensitive period; Bonding; Attachment
Introduction Mother–young relationships in domestic ungulates are mainly characterized by the fact that mothers give birth to precocious neonates capable of a high degree of independent activity from birth, which differentiate them from most altricial laboratory species, whose young are relatively immobile and helpless at birth (e.g. rat, house mouse, rabbit; González-Mariscal and Poindron, ⁎ Corresponding author. UMR 6175, PRC, INRA, 37380 Nouzilly, France. E-mail address: [email protected] (P. Poindron). 0018-506X/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2007.03.023
2002; Nowak et al., 2000; Poindron et al., 2007). Also, two major types of mother–young relationships can be distinguished in ungulates. On the one hand, sows give birth to a large litter which is confined to a nest for several days, and fostering of alien young is relatively easy (Nowak et al., 2000). On the other hand cattle, sheep and goats give birth to one or few young; mothers do not build a nest and bond selectively to their own neonate (Nowak et al., 2000; Numan et al., 2006; Poindron et al., 2007). This bonding process in the mother has been regarded as an example of maternal attachment somewhat similar to that of filial imprinting in young birds and has been well studied in these species, but
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more particularly in the goat and even more so in the sheep (Herscher et al., 1963; Poindron et al., 2007). In this latter species, the establishment of maternal recognition and exclusive care of the neonate, as well as their physiological and neurobiological determinants has been the object of extensive research (Kendrick et al., 1997; Kendrick, 2000; Lévy et al., 1996; Nowak et al., 2007). Whether the characteristics and determinants of maternal care and bonding in the goat are similar to those found in sheep is a relevant question, given the differences of mother–young relationships existing between the two species once the mother leaves the birth site. Indeed, after the first postpartum hours of intense mother–young care at the birth site, the doe leaves her kids for several hours, while the young hide and wait for her to come back for nursing (Lent, 1974; Lickliter, 1984; O'Brien, 1984, 1988; Rudge, 1970). Lambs, in contrast, move along with their dam and remain close to her as soon as she leaves the birth site to join the rest of the flock and graze (Lent, 1974; Lynch et al., 1992; Nowak et al., 2000). It has been hypothesized that the different spatial mother–young relationships found in hiders and followers during the first days postpartum may be associated with differences in early abilities and underlying mechanisms of mother–young recognition in the two species (Gubernick, 1980, 1981; Lickliter and Heron, 1984). If this is the case, the physiological control of maternal care and bonding could also be different between species since bonding to the lamb depends on the facilitation of learning by physiological changes occurring at parturition (Kendrick et al., 1997; Kendrick, 2000; Lévy et al., 1996). While no direct comparisons between the two species have been carried out to examine this question, the data available in goats provide us with sufficient information to approach this question. After briefly describing the main behavioral characteristics of maternal behavior in the goat, we will review the physiological determinants of maternal behavior in this species, how the mother recognizes and bonds to her kid and how the presence of the young may influence maternal endocrinology during lactation. Main characteristics of goat maternal behavior Maternal behavior at parturition Prepartum isolation Preparturient females are typically wary and seek remote or concealed birth sites prior to parturition. Under free range conditions, goats tend to isolate themselves to give birth (O'Brien, 1983, 1984; Rudge, 1970). This is also the case under intensive farm management where females show increased restlessness, frequent vocalizations and increased intolerance of conspecifics (Das and Tomer, 1997; Lickliter, 1985; Sambraus and Wittmann, 1989). This tendency to isolation is associated with a clear decrease in gregariousness at parturition as goats show a marked reduction of their behavioral response to social isolation (i.e. agitation index) between 24 h and about 1 h prepartum (Fig. 1). Proper prepartum isolation without causing agitation is likely to help in the display of proper maternal care and bonding.
Fig. 1. Change of behavioral response to social separation in preparturient goats. The response to social separation is expressed as a median agitation index and interquartile range (vertical bars), obtained by subtracting the agitation score obtained before from that obtained after withdrawal of the rest of the group from the pen where the animals lived. Agitation scores were obtained by summing numbers of squares crossed, vocalizations, jumps, attempts to jump, mictions and defecations over a 5 min period (see Poindron et al., 1997 for details of procedure). All groups were independent. Test at parturition was performed after rupture of the waterbag or sight of the fetus' hooves, whichever occurred first. Also, goats in this group gave birth either on day 150 or day 151 of pregnancy, i.e. less than 24 h after the corresponding test for the group at day 150. ⁎: Response of parturition group significantly lower than in any other group (Mann–Whitney, P b 0.025), the other pregnant groups not differing one from another or from the non-pregnant controls. This decrease in the agitation score was not due only to a reduction in motor activity, but also to a significant reduction of high-pitched bleats (two- to three-fold decrease), another key indicator of agitation. It is also important to mention that the overall weight of vocal activity in the index is higher than that of motor activity and that, even in the middle of the parturition process, goats are perfectly able to walk.
Immediate maternal care to the neonate In the goat, most births occur during day time (over 80% between 06:00 and 20:00; Allan et al., 1991; Das and Tomer, 1997; Lickliter, 1985). During parturition does usually lie down, and in some instances they lick the udder and teats. A few minutes after expulsion of the fetus the mother rises and starts to lick her kid vigorously, generally beginning with its head and neck (Collias, 1956; Lickliter, 1985). Licking is accompanied by numerous low and high pitched bleats and occasionally by flehmen behavior, especially when consuming urine from the neonate (Sambraus and Wittmann, 1989). There is little information concerning differential care of male and female neonates in sheep and goats, but preliminary results suggest that does may preferentially lick males more than females and that this difference relies on olfactory information since it is abolished in anosmic mothers (Serafin et al., 2003). The neonate tries to stand up within 5–10 min after birth and usually succeeds in doing so by 20 to 30 min. In less than 1 h after birth, the neonate finds the mother's udder by trial and error exploration and begins to feed (Allan et al., 1991; Collias, 1956). Establishment of neonate recognition and selective bonding Olfactory recognition of the kid and selective bonding Goats, like sheep, rapidly develop an exclusive maternal bond with their neonate(s). Immediately after parturition,
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mothers groom and nurse any kid, but then rapidly learn to discriminate and nurse only their own young (Collias, 1956; Herscher et al., 1963). In some conditions, 5 to 10 min of contact with the neonate are sufficient for does to become selective (Gubernick, 1981) and most mothers reject alien kids at 2 to 4 h postpartum, regardless of their age or the similarity of their coat to that of their own young (Romeyer and Poindron, 1992; Romeyer et al., 1994a). This selective nursing depends primarily on the main olfactory system since prepartum peripherally induced anosmia, which affects only the main olfactory system, prevents the establishment of selective nursing (Lévy et al., 2004; Poindron et al., 2007). There is some evidence suggesting that selectivity may result from olfactory labeling of the kid by the mother through licking and nursing (Gubernick, 1981), at variation with sheep in which the recognition of the lamb depends on its individual olfactory signature (Lévy et al., 2004). Nonetheless, in undisturbed conditions (i.e. without postpartum separation before testing), selective acceptance and nursing of the own young by its postparturient dam clearly depends on the learning by the doe of some individual olfactory signature of the kid during the first hours of mother–young interaction. Even twins have different olfactory signatures (Romeyer et al., 1993, 1994a). This olfactory learning process is modulated by vaginocervical stimulation and involves the main olfactory system, even though some role of the vomeronasal organ and accessory system cannot be excluded (Poindron et al., 2007; Romeyer et al., 1994a). Non-olfactory recognition of the kid. Some authors have suggested that mothers are not able to recognize their kids by sight or hearing before 2 to 5 days postpartum (Addae et al., 2000; Awotwi et al., 2000; Lenhardt, 1977). Nonetheless, there is growing evidence that does can already discriminate between their own kid and an unfamiliar one at 4 h postpartum without the help of olfactory cues (Poindron et al., 2003). In addition, they can make such a discrimination on the basis of only acoustic cues at 48 h, possibly due to the existence of an individual acoustic signature in the kids' bleats at that age (Terrazas et al., 2003). However, this non-olfactory recognition of the kid does not appear to be essential for the establishment and maintenance of selective nursing in the postparturient doe. Anosmic goats will accept unfamiliar kids as rapidly as intact mothers despite the fact that they are able to identify their own young with the help of visual and acoustic cues (Poindron et al., 2003). Recent results suggest that the establishment of the visual and/or acoustic recognition of the kid may be influenced by the level of maternal nutrition in late pregnancy (Terrazas et al., 2004 and unpublished results). The relevance of early visual and acoustic recognition of the young for the survival of the kid remains to be investigated in goats. In sheep, acoustic communication appears important for the early survival of the lamb (Nowak, 1990), which makes adaptive sense since ewes and lambs ambulate soon after birth and have to maintain close contact. Kids, on the other hand, do not walk much during the first days of their life due to their hiding behavior (see below). However, as olfactory recognition works only at very short distances (b1 m; Poindron et al., 2003), acoustic and visual
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recognition may still be important to locate the hiding or “lyingout” site of the kid. Strategy around the birth site: the hiding behavior of kids Parturition and lying-out sites are usually located in areas heavily used by the herd and close to the traditional night camp (O'Brien, 1983). Also, lying-out sites tend to be under cover, with relatively low wind velocity and light intensity, close to or adjacent to vertical objects. Mothers visit and nurse their kids only a few times per day (O'Brien, 1984). In the wild, the timing and extent of the hiding phase appear to vary among studies. Field studies of wild and feral goat populations indicate that newborn goats spend their first 3–4 days lying alone at a considerable distance from their mothers (McDougall, 1975; Rudge, 1970). In other instances, however, kids were found to remain with their mother for a few days before displaying hiding behavior, which continues up to about 6 weeks of age (McDougall, 1975). Also, some dams maintain a considerable distance from their young (leavers), while others remain in the vicinity of the site where the young hides after nursing (stayers; O'Brien, 1984). This plasticity in postpartum behavior may have strong selective advantages in feral goats, which occupy a range of habitats or are exposed to varying predation pressures (O'Brien, 1984). The hiding behavior of kids can also be observed in domesticated goats and under intensive farm management conditions, showing that hiding behavior has not been lost due to domestication. Newborn kids move away from their mother and birth site 15–26 h after parturition and spend most of their time secluded from congeners for 4 to 7 days. Physical mother– young contact at the time of reunion is generally initiated by the kids (Lickliter, 1984). Nonetheless, in intensive management conditions, frequencies of nursing appear higher than those reported in feral goats (Delgadillo et al., 1997), possibly as a result of confinement and reduced opportunity for the mother to move far away from her kid(s). Activation of maternal behavior at parturition Physiological factors If immediately separated from their neonate, parturient goats display maternal behavior spontaneously only for a short time after giving birth, although the duration of this period of initial responsiveness towards the neonate is longer in multiparous mothers (Lickliter, 1982). This indicates the existence of a sensitive period for the establishment of the relationship between the newborn kid and its mother (Herscher et al., 1963; Poindron et al., 2007) and suggests that it is controlled by some physiological factors associated with parturition. However, attempts to identify these factors have met with little success so far. The changes of concentration in estrogen and progesterone in the goat during late pregnancy and parturition are very similar to those found in sheep, in which these hormones play an important role in the display of maternal behavior (Poindron et al., 2007). However, an exogenous treatment of estradiol and progesterone that induces lactation and
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Fig. 2. Impairment of maternal behavior by peridural anesthesia in the parturient goat and its recovery following vaginocervical stimulation (VCS). A: Display of maternal behavior in goats receiving a peridural anesthesia just before expulsion of the fetus (Late Peridural, control group n = 12; see text for details), or when peridural was applied at the first signs of labor (Early Peridural, n = 9). Licking latencies in the first 3 h following parturition. Bleating activity for the first 30 min postpartum. B: Facilitation of maternal behavior by 5 min of artificial vaginocervical stimulation applied after the 7 non-responding mothers in part A (see text) had recovered from the peridural anesthesia, as evidenced by recovery of hind legs motor activity. Mothers were observed for 30 min before and 30 min after VCS. A: Mann–Whitney tests; B: Wilcoxon tests, with unidirectional hypotheses of a negative effect of peridural anesthesia and of a positive effect of VCS. Values are medians (histograms) and interquartiles ranges (vertical bars). P: one-tail probabilities. Fq/30 min: frequency of behavior per 30 min.
facilitates maternal behavior in non-pregnant ewes is ineffective in the goat (Rosenblatt and Siegel, 1981). The alternative of inducing maternal behavior with treatments mimicking more closely the hormonal changes occurring at parturition has not been investigated. The possibility that vaginocervical stimulation (VCS) resulting from delivery of the fetus may be involved in activating maternal behavior was explored by blocking the corresponding sensory inputs with peridural anesthesia in primiparous/inexperienced and in multiparous/experienced mothers (Poindron et al., 1998). The experimental design and methods were similar to those of Krehbiel et al. (1987) and Lévy et al. (1992) in sheep. In contrast to sheep, the effects of blocking VCS did not differ between primiparous and multiparous mothers. Peridural anesthesia applied at the first signs of labor (Early Peridural EP, on average 1 h 30 min prepartum) impaired the display of maternal behavior at parturition more strongly than when it was applied 15 min before fetus expulsion (Late Peridural, LP; Fig. 2). In this latter group, which served as control, most mothers behaved as parturient goats normally do, with short latencies to initiate licking, intense grooming and emission of numerous low-pitched bleats. Nonetheless, even in the LP group some females failed to display maternal behavior (EP: 4/9; LP: 3/12), resulting in non significant differences between groups (Fig. 2). The facilitating action of VCS is also supported by the effects of VCS applied after recovery from the peridural anesthesia in the seven mothers that did not show maternal behavior at parturition. While none of these 7 mothers
had shown maternal behavior during the first 30 min after recovering their motor ability, they all displayed some licking and/ or low pitched bleats during the following 30 min after artificial VCS (Fig. 2). This was particularly obvious in one mother, in which aggressive behavior disappeared immediately after VCS while licking of the neonate was triggered (Fig. 3). Further evidence for a role of VCS in the control of maternal behavior in the goat comes from its effects on maternal selectivity. Goats, like ewes, bond rapidly to their neonate(s). Two hours after parturition, most mothers actively reject kids they have not interacted with (Romeyer et al., 1994b). However, 5 min of artificial VCS applied at 2 h postpartum allows the acceptance of an unfamiliar kid in more than half of the mothers that were rejecting it just before VCS (Romeyer et al., 1994b). Therefore, VCS inhibits the display of maternal selectivity in the goat as it does in sheep and facilitates the establishment of a new bond. These results are similar to those reported in the ewe. It seems therefore reasonable to hypothesize that the establishment of maternal selectivity in the goat also depends on the learning of individual phenotypic cues from the kid, under the facilitation of physiological factors, as already shown in the ewe (Lévy and Fleming, 2006). Sensory cues Maternal olfaction plays an important role in the control of maternal behavior in the immediate postpartum period in two complementary ways. First, it is important that the mother has access to the olfactory cues provided by licking of the neonate. About half of does prevented from licking their kid during the first 4 h postpartum fail to show adequate maternal care when reunited with their young (Bordi et al., 1994; Romeyer et al., 1993). Second, this full access to olfactory cues through licking facilitates the establishment of maternal selectivity. Of the mothers that remain maternal despite 4 h of licking deprivation, half fail to be selective and still accept alien kids, in contrast to mothers that have fully interacted with their neonate during the same period. As a whole, these results may suggest an involvement of the
Fig. 3. Individual example of the recovery of maternal behavior by vaginocervical stimulation (VCS) in a goat having received a peridural anesthesia 15 min before the expulsion of the fetus (Late Peridural Anesthesia, LPA). VCS was applied about 2 h 30 min postpartum, more than 30 min after motor recovery from PA. For more details see text and Krehbiel et al. (1987). Li: licking time (s/30 min); LB: lowpitched bleats (frequency/30 min): AB: aggressive behavior (frequency/30 min); Nu: nursing time (s/30 min).
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vomeronasal system in the control of maternal behavior and selectivity at parturition in the goat (Poindron et al., 2007). Regulation of maternal behavior and physiology during lactation Influence of the kid on the maintenance of maternal behavior Once the hiding phase has ended, kids suckle about twice per hour, with a progressive decrease as they get older (Delgadillo et al., 1997). While nursing rhythms decrease over time, synchrony between the activities of the mother and her young may increase (Lickliter, 1987), which is characteristic of hider species. In addition, kids may gather in peer groups or crèches (Lickliter, 1987) that may be important for the acquisition of food preferences, together with transmission of food choice by the mother (Biquand and Biquand-Guyot, 1992). There is little information concerning the relationship between does and their kids during late lactation and weaning, which appears to take place in the wild between 3 and 6 months of age (Collias, 1956; Herscher et al., 1963). In any case, the presence of the young is critical for the maintenance of maternal behavior during lactation. Thus, in a recent study (see Fig. 4), we found that 2 weeks of total separation from the kid at 3 months postpartum (groups 3 and 4) led to a significant decrease in the time that dams nurse their kid or the proportion of dams doing so, in comparison to mothers in which some contact was maintained (groups 1 and 2). The actual stimulation of suckling was not necessary to maintain maternal responsiveness since nursing time and the proportion of goats accepting their kid were in fact highest in mothers that could see, hear and smell their kids, but could not nurse them (group 2, Fig. 4). These results indicate also that the state of lactation itself is not sufficient to maintain maternal responsiveness since acceptance was lowest in mothers totally separated from their kid, despite the maintenance of lactation by milking (group 4, Fig. 4). Finally, among the nine mothers (out of 33) that kept accepting their own kid after 15 days of total separation, none accepted an alien kid, indicating that recognition was still present at that time in these mothers.
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Limiting the duration of daily mother–young interactions can also influence maternal endocrinology and milk production. Mothers that are allowed only 5 h of contact per day with their kid display higher basal and post-suckling concentrations of PRL and growth hormone (GH) than mothers in permanent contact with their kids, or mothers that are totally separated from them and milked (Hernandez et al., in press). Such a restriction of mother– young contact, when associated with one daily milking, allows extra collection of milk without severe impact on kid growth, illustrating the great flexibility of the nursing rhythms of mothers and their kids. Recovery of maternal ovarian activity is another parameter that can also be influenced by the presence of the young. As in several other ruminants (e.g. sheep), goats display a period of postpartum sexual rest, also called postpartum anestrus. Under temperate and subtropical latitudes, this period normally coincides with the seasonal inhibition of reproduction in spring. Therefore, postpartum anestrus per se can only be studied in females that give birth in autumn. In this case, the presence of the kid and/or suckling can delay the recovery of sexual activity (Delgadillo et al., 1997, 1998). The selective bond between the doe and her kid(s) does not seem critical in the control of postpartum anestrus. Preventing the
Influence of the kid on maternal postpartum physiology As in other mammals, presence of the kid and nursing have a number of consequences on maternal physiology. Some mothers can respond with an increase in peripheral OT levels following exposure to olfactory, acoustic or visual cues from their kids (McNeilly, 1972). In addition, maternal selectivity modulates the release of OT during nursing, while PRL release does not appear to depend on this aspect of maternal behavior (Hernández et al., 2002). Indeed, in this study, intact/selective mothers showed a peripheral increase of OT only in response to suckling by their own kid but not by an alien. In contrast, in anosmic/non-selective mothers OT levels increased in response to suckling by either their own or an alien kid. PRL release, on the other hand, was present in intact mothers regardless of the identity of the kid that suckled. This PRL release also occurred in anosmic dams, although the response was lower than in intact mothers.
Fig. 4. Maintenance of maternal behavior in mixed breed goats undergoing 2 weeks of various degrees of separation from their kids at 3 months of lactation. From left to right: Controls (group 1), no mother–young separation; No suckling allowed (group 2), mothers and kids were separated by an openwork fence preventing nursing, but mothers could see, hear and smell their young, and the udder was emptied every third day by cannulation; Total Separation from kids (group 3), udder emptied every third day by cannulation; Total separation from kids and one daily machine milking (group 4). The mothers' acceptance of their own kid and of an alien kid (not shown —see text) was tested individually in a 5 min behavior test at the end of the 15 days of treatment. Mann–Whitney and Fisher exact probabilities. For a given variable, bars with different letters indicate a significant difference between the corresponding groups. All probabilities are two-tailed. Note the general effect of the presence of the young (groups 1 + 2 vs groups 3 + 4 ). x⁎: P = 0.084.
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establishment of maternal selectivity through peripheral anosmia before kidding did not result in reducing its duration (Hernández et al., 2004), contrary to what has been reported in cattle (Griffith and Williams, 1996).
the two referees and Prof. D. Krehbiel for their comments and help in correcting the manuscript.
Conclusions
Addae, P.C., Awotwi, E.K., Oppong-Anane, K., Oddoye, E.O.K., 2000. Behavioural interactions between West African dwarf nanny goats and their single-born kids during the first 48 hours post-partum. Appl. Anim. Behav. Sci. 67, 77–88. Allan, C.J., Holst, P.J., Hinch, G.N., 1991. Behaviour of parturient Australian bush goats. I. Doe behaviour and kid vigour. Appl. Anim. Behav. Sci. 32, 55–64. Awotwi, E.K., Oppong-Anane, K., Addae, P.C., Oddoye, E.O.K., 2000. Behavioural interactions between West African dwarf nanny goats and their twin-born kids during the first 48 h post-partum. Appl. Anim. Behav. Sci. 68, 281–291. Biquand, S., Biquand-Guyot, V., 1992. The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus). Appl. Anim. Behav. Sci. 34, 231–245. Bordi, A., De Rosa, G., Napolitano, F., Litterio, M., Marino, V., Rubino, R., 1994. Postpartum development of the mother–young relationship in goats. Appl. Anim. Behav. Sci. 42, 145–152. Collias, N.E., 1956. The analysis of socialization in sheep and goats. Ecology 37, 228–239. Das, N., Tomer, O.S., 1997. Time pattern on parturition sequences in Beetal goats and crosses: comparison between primiparous and multiparous does. Small Rumin. Res. 26, 157–161. Delgadillo, J.A., Poindron, P., Krehbiel, D., Duarte, G., Rosales, E., 1997. Nursing, suckling and postpartum anoestrus of creole goats kidding in January in subtropical Mexico. Appl. Anim. Behav. Sci. 55, 91–101. Delgadillo, J.A., Flores, J.A., Villarreal, O., Flores, M.J., Hoyos, G., Chemineau, P., Malpaux, B., 1998. Length of postpartum anestrus in goats in subtropical Mexico: effect of season of parturition and duration of nursing. Theriogenology 49, 1209–1218. González-Mariscal, G., Poindron, P., 2002. Parental care in mammals: immediate internal and sensory factors of control. In: Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrfbach, S.E., Rubin, R.T. (Eds.), Hormones, Brain and Behavior, vol. 1. Academic Press, New York, pp. 215–298. Griffith, M.K., Williams, G.L., 1996. Roles of maternal vision and olfaction in suckling-mediated inhibition of luteinizing hormone secretion, expression of maternal selectivity, and lactational performance of beef cows. Biol. Reprod. 54, 761–768. Gubernick, D.J., 1980. Maternal “imprinting” or maternal “labelling” in goats. Anim. Behav. 28, 124–129. Gubernick, D.J., 1981. Parent and Infant attachment in mammals. In: Gubernick, D.J., Klopfer, P.H. (Eds.), Parental Care in Mammals. Plenum Press, New-York, pp. 243–305. Hernández, H., Serafín, N., Terrazas, A., Marnet, P.G., Kann, G., Delgadillo, J.A., Poindron, P., 2002. Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats. Horm. Behav. 42, 232–244. Hernández, H., Delgadillo, J.A., Serafin, N., Rodriguez, A.D., Poindron, P., 2004. Prepartum peripherally-induced hyposmia does not reduce postpartum anoestrus duration in nursing goats. Reprod. Nutr. Dev. 44, 251–259. Hernandez, H., Delgadillo, J.A., Flores J.A, Rodríguez, A.D., Serafín, N., Kann, G., Marnet, P.G., Poindron, P., in press. Effects of restricted nursing on milk production and collection, kid growth and plasma prolactin and growth hormone concentrations in dairy goats. Animal. Herscher, L., Richmond, J.B., Moore, A.U., 1963. Maternal behavior in sheep and goats. In: Rheingold, H.L. (Ed.), Maternal Behavior in Mammals. John Wiley and Sons Inc., New-York, pp. 203–232. Kendrick, K.M., 2000. Oxytocin, motherhood and bonding. Exp. Physiol. 85, 111–124. Kendrick, K.M., Da Costa, A.P., Broad, K.D., Ohkura, S., Guevara, R., Lévy, F., Keverne, E.B., 1997. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44, 383–395. Krehbiel, D., Poindron, P., Lévy, F., Prud'Homme, M.J., 1987. Peridural anesthesia disturbs maternal behavior in primiparous and multiparous parturient ewes. Physiol. Behav. 40, 463–472.
As a whole, our understanding of the mechanisms that control the activation of maternal responsiveness in the goat remains somewhat fragmentary. Nonetheless, in light of the results concerning the effects of VCS on the onset of maternal behavior, these mechanisms do not appear fundamentally different from those existing in sheep (see Nowak et al., this issue), even though the endocrine factors involved remain to be identified. Similarly, the establishment of recognition of the neonate, the control of maternal selectivity and the sensory cues involved do not seem to differ between the two species. Therefore, the difference of mother–young spatial relationships developed during the early postpartum period in goats, which give birth to hider neonates and in sheep, which give birth to followers, does not seem to be associated with different proximate factors controlling maternal responsiveness and bonding. It is possible that the selection pressure resulted from the combination of two main factors common to the two species, a very mobile neonate and a strong gregarious tendency in the mother. Alternatively, it cannot be excluded that the lack of differences between the two species may result from domestication, which imposed similar environmental constraints on both of them, resulting in the fading of differences existing in their wild ancestors. However, this second possibility is less likely, given that domestication has not suppressed hiding behavior in kids or following in lambs. Further studies on wild hider and follower ungulates with varying degrees of gregariousness would help to clarify the possible weight of these factors on the evolution of maternal behavior and bonding mechanisms. Finally, comparative studies of the development of filial and maternal attachment in sheep and goats certainly represent an excellent opportunity to investigate the mechanisms controlling the affective aspect of bonding. In these two species, the mother and the neonate develop an affective individual bond, but the time course of its establishment is quite different. Ewes and lambs respond to separation from each other within hours and independently of the nursing pattern due to the follower nature of the relationships. Goats and kids, on the other hand, probably take longer to develop a distress response to mother–young separation because of the hiding tendency of the kid and also because the response to separation is inhibited by nursing (Addae et al., 2000). Therefore, a comparative investigation of the establishment of the distress response to separation and of its neurobiological control would certainly provide valuable information for the understanding of affective behavior in general. Acknowledgments Most of the unpublished results presented in this review were obtained at the Instituto de Neurobiologia de la UNAM, Campus Juriquilla, Queretaro with support of PAPIIT IN217205 and IFS grant B/3872-1. The authors are grateful to
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