| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
SHEEP |
Sustainable Livestock Systems Group, SAC, Edinburgh, EH9 3JG, UK
 |
Abstract |
|---|
Key Words: estradiol • genetics • lamb survival • management • maternal behavior • sheep
|
INTRODUCTION |
|---|
). Although labor has been identified as an important factor in good sheep welfare, labor costs have the most detrimental financial impact on farm profitability in the United Kingdom (Stott et al., 2005). An alternative response to high levels of shepherding has been the development of lambing management systems that require lower inputs, such as the "easy-care" systems developed in New Zealand (Fisher, 2003). Here, rigorous culling policies for ewes that needed lambing assistance or that have failed to rear a lamb to weaning have resulted in systems in which very low levels of labor input result in levels of lamb mortality similar to those achieved with a much greater input in traditional systems. Lower input systems are now becoming increasing attractive to sheep farmers in the United Kingdom and elsewhere as farm incomes and subsidy payments decline. These systems rely on optimizing the ability of the animals within them to take care of themselves, through appropriate behavioral responses and resistance or resilience in the face of common health and welfare challenges. Understanding the factors involved in improved lamb survival, and the role played by maternal behavior and the ewe-lamb interaction, can help in the development of management practices that enhance expression of these behaviors, and so improve lamb survival. In this review, the biology of the behavioral interactions between ewe and lamb and the factors that affect their expression are considered. The possibility of using genetic selection and appropriate management to improve behavioral expression is addressed. |
LAMB MORTALITY AND SHEPHERDING |
|---|
; Binns et al., 2002; Fisher, 2003; Southey et al., 2004; Sawalha et al., 2007). The vast majority of these mortalities occur within the first 3 d of postnatal life (Huffman et al., 1985; Nowak et al., 2000; Sawalha et al., 2007). The main causes of lamb mortality are related to trauma experienced during the birth process, failure of neonatal adaptation to postnatal life (e.g., inability to maintain body temperature, low lamb vigor, poor establishment of a maternal bond), infectious disease, functional disorders, and predation. The relative prevalence of any of these causes of mortality varies by location and farm management system. However, the single greatest predictor of lamb mortality is birth weight (Smith, 1977; Meyer and Clarke, 1978; Dalton et al., 1980; Hinch et al., 1983; Gama et al., 1991; Fogarty et al., 2000). Heavy lambs may experience difficult deliveries and die during birth (Smith, 1977; Meyer and Clarke, 1978; Dalton et al., 1980), whereas low birth weight lambs are more likely to experience starvation and hypothermia (Scales et al., 1986).
Management practices, such as winter feeding of pregnant ewes (Waterhouse, 1996), have reduced lamb mortality over the last 50 yr, and in many countries, increased shepherding and housing at lambing have been used to improve lamb survival. Lamb mortality in housed flocks tends to be lower than the average; for example, figures of approximately 9% mortality are given for mainly housed flocks (Green et al., 1993; Binns et al., 2002). Housing and intensive shepherding at lambing have reduced the incidence of stillbirths (Binns et al., 2002), because ewes with dystocia can readily be identified and lambing assistance given. In addition, lambs that are protected from hypothermia and predation, disease, or ill health can be treated promptly, triplet lambs may be fostered onto suitable ewes, and the practice of individually housing parturient ewes and their newborn lambs in small pens reduces lamb abandonment. However, there is an increased risk of mortality because of infectious disease during housed lambing (Binns et al., 2002). Housing pregnant ewes at a relatively high stocking density disrupts the behavioral patterns of the parturient ewe, which is motivated to seek isolation or seclusion (Poindron et al., 1997), even in housed systems (Gonyou and Stookey, 1983). Preventing this behavioral response brings parturient ewes into close contact with one another, which may increase the frequency of mismothering and attempted lamb stealing (Gonyou and Stookey, 1985).
In outdoor lambing situations, some authors have questioned the role of shepherding in improving lamb survival (Fisher and Mellor, 2002; Fisher, 2003). For ewes unaccustomed to the presence of humans, a sudden increase in shepherding around lambing time can act as a source of stress for the ewe. Fear, stress, or disturbance during labor is known to cause an involuntary suppression of uterine contractions in mammals (Naaktgeboren, 1979), inhibit oxytocin release (Lawrence et al., 1992), and increase the risk of dystocia and birth trauma (Haughey, 1980). In addition, disruption after birth can affect the development of the ewe-lamb bond and may cause the ewe to leave the birth site early. Time spent at the birth site is correlated with lamb survival in twin-bearing Merino ewes (Stevens et al., 1982; Alexander et al., 1983, 1984; Putu et al., 1988; Cloete, 1992; Nowak, 1996), and leaving the ewe undisturbed for at least 6 h is recommended to improve bonding (Murphy et al., 1994). However, in other studies in which the sheep may be more accustomed to shepherding, a role for supervision and shepherding to improve survival and the overall welfare of the ewe and lamb has been supported (Burfening and van Horn, 1993; Pattinson et al., 1994; Waterhouse, 1996).
Ewe breeds that are generally reared under intensive conditions at lambing, with a high degree of human intervention and assistance in the lambing process, experience more difficult deliveries than breeds that have been managed under more extensive management, when managed under similar conditions (Dwyer et al., 1996; Dwyer and Lawrence, 2005b). Assistance with delivery may therefore have reduced the natural selection pressure on ease of birth in the ewe. This is supported by selection studies to increase lamb-rearing ability, in which one of the main impacts of selection has been an increase in ease and speed of delivery (Knight et al., 1988; Kilgour and Haughey, 1993; Cloete and Scholtz, 1998). Thus, although intensive shepherding may currently be required by some breeds of sheep, this may be to the detriment of those sheep and to the development of low-input systems without specific selection to promote suitable behavioral and physical characteristics in the ewe.
|
BEHAVIORAL INTERACTIONS BETWEEN THE EWE AND LAMB AT PARTURITION |
|---|
), frequent low-pitched bleats or "rumbles" (a specific lambing vocalization made by the ewe to communicate with her lamb; Shillito and Hoyland, 1971; Dwyer et al., 1998), and standing still to facilitate access to the udder by the lamb. These behaviors serve 2 main functions: first, the ewe expresses nurturing behavior to facilitate the successful transition of her lambs from pre-to postnatal life, and second, she forms an exclusive selective attachment for her own lambs (Poindron et al., 1984; Lévy et al., 1995). Licking or grooming the lamb serves to dry the lamb, to clear placental membranes from the nose and mouth, and to stimulate activity and respiration (Lent, 1974; Alexander, 1988; Nowak et al., 2000). In addition, this behavior promotes the formation by the ewe of an olfactory memory for the lamb (Baldwin and Shillito, 1974; Poindron et al., 1980; Alexander et al., 1986; Poindron et al., 1988; Lévy et al., 1991; Hernandez et al., 2001), and ewes then restrict their maternal care to those lambs. Low-pitched bleating may act to reduce stress in the lamb (Dwyer et al., 1998) and aids in the later development of maternal recognition by the newborn lamb (Nowak, 1990). However, these behavioral responses are affected by cues from the lamb, in particular, the presence of amniotic fluids in the coat of the lamb, which increases maternal licking, the number of low-pitched bleats, and udder acceptance by ewes (Lévy and Poindron, 1984).
During this immediate postpartum period, the lamb performs a series of behaviors directed toward standing, locating the udder, and sucking. Initial movements are raising and shaking the head, followed by rolling onto the sternum, bleating, pushing up on the knees, and then attempting to stand, first by standing on the hind legs, and then also by extending the forelegs. These behaviors can proceed rapidly, with some lambs standing within a few minutes of birth, and most lambs standing within 30 min of delivery (Dwyer, 2003). Once the lamb is able to stand, it displays directional responses toward any large object, particularly if it moves and bleats (Vince et al., 1985), and it orientates along the side of the ewe toward the udder. Lambs are attracted to smooth, warm, and yielding surfaces, such as the udder, and to olfactory cues provided by the inguinal wax in the udder region (Vince, 1993), which aid the lamb in seeking the udder. Tactile stimulation of the face and forehead of unsuckled lambs elicits upward movements of the head and neck, and "munching" movements of the mouth (Vince et al., 1984), to facilitate teat location and sucking. Sucking in most lambs occurs within 1 to 2 h of birth (Dwyer, 2003), and for this to occur, it is imperative that the lamb is able to stand and show coordinated udder-seeking behaviors.
During the behavioral development of the newborn lamb, the behavior of the ewe also develops, with grooming progressing from the face and neck of the lamb to the anogenital region as the lamb moves along the body of the ewe. Experienced ewes arch the back and widen their hind legs to make the udder more accessible as the lamb reaches this region (Vince, 1993). Thus, although the behavior of the ewe cannot ensure successful sucking by the lamb, she can aid the lamb in locating the udder and make early successful sucking more likely. Behavioral or other visual cues from the lamb can also enhance maternal responsiveness. Parturient ewes are very attracted to newborn lambs but are less interested in lambs only a few hours older. Their maternal behavior is disturbed if their own neonate is exchanged for a 12- to 24-h-old lamb that is already dry and more active. In contrast, exchanging the ewe’s own lamb with a newborn alien lamb does not result in noticeable perturbations in maternal behavior (Poindron and Le Neindre, 1980; Poindron et al., 1980). Likewise, although ewes initially express maternal behavior toward stillborn lambs similar to that toward live lambs, this behavior wanes over the first few hours after delivery without appropriate behavioral responses from the lamb, particularly if she subsequently delivers a live littermate to the stillborn lamb (Dwyer and Lawrence, 2005b).
|
FACTORS AFFECTING THE EXPRESSION OF EWE MATERNAL BEHAVIOR |
|---|
Primiparous ewes are often less competent as mothers than are experienced ewes, and the mortality of their lambs is higher (Wiener et al., 1983; Owens et al., 1985; Gama et al., 1991; Morris et al., 2000). Primiparous ewes tend to have a longer labor than experienced ewes and are slower to begin grooming their lambs after birth (Dwyer and Lawrence, 1998, 2005b). They are more disturbed by the behavior of the lamb and more likely to circle, back away, or walk forward over the top of the lamb as it attempts to reach the udder (Poindron et al., 1984; Dwyer and Lawrence, 1998, 2000b), which results in delayed sucking in the lamb (Dwyer, 2003). Primiparous ewes are also more likely to show fearful behavior toward the lamb (e.g., retreating from it), they may be more aggressive (i.e., butting or threatening the lamb), and in some cases they may fail to show maternal behavior and abandon their lamb (Dwyer and Lawrence, 1998). However, on average, when compared with multiparous ewes, primiparous ewes show equivalent amounts of grooming behavior over the first 2 h after delivery and make a similar number of low-pitched bleats (O’Connor et al., 1992; Dwyer and Lawrence, 2000b). Experience of being a mother, gained during the initial contacts of the ewe with her lamb, allows her to learn to respond appropriately, and she becomes less likely to prevent subsequent sucking attempts (Dwyer and Lawrence, 1998).
Maternal Nutrition
Ewes that are undernourished during pregnancy give birth to lightweight lambs (reviewed by Mellor, 1983; Robinson et al., 1999) with increased mortality rates (Jordan and Mayer, 1989; Kleeman et al., 1993; Hinch et al., 1996). Additional adverse effects of maternal undernutrition include reduced udder weight and mammary development (Mellor and Murray, 1985; Mellor et al., 1987), delayed onset of lactation (Mellor et al., 1987), reduced colostrum yield (Mellor and Murray, 1985; Hall et al. 1992; O’Doherty and Crosby, 1996), and reduced total milk production (Jordan and Mayer, 1989; O’Doherty and Crosby, 1996). In addition to these effects, gestationally undernourished ewes also display behavioral impairments that will affect the quality of her maternal relationship with her lamb. Undernourished ewes take longer to interact with their lambs (Thomson and Thomson, 1949), display more aggression to the lamb, spend less time grooming and more time eating after birth (Dwyer et al., 2003), and are more likely to desert their lambs (Putu et al., 1988; Lindsay et al., 1990) than well-fed ewes. In specific tests of the strength of attachment between ewes and their lambs, undernourished ewes were less attached to their lambs than adequately fed ewes (Dwyer et al., 2003). However, in studies in which maternal nutrition was manipulated by altering pasture allowance (via sward height) in late gestation, the effect of nutritional treatment on maternal responses to the ewe’s handling of her lambs within 12 h of birth was small (Everett-Hincks et al., 2005), although the ewes with the greatest pasture allowance tended to stay closer to their lambs compared with the ewes with the least allowance. Inadequate maternal nutrition during pregnancy can therefore compromise lamb survival through its impact on lamb prenatal development and maternal lactation and by reducing the quality of maternal behavior and the strength of the ewe-lamb interaction.
Breed Effects
Several studies have compared breed differences in maternal behavior, using different breeds and different behavioral measures. The breeds chosen generally reflect the prevalent or commercially important lines in the countries where they were studied, for example, behavioral comparisons among the Merino, Perendale, Romney, Border Leicester, Cheviot, Dorset Horn, and crossbreds in Australia and New Zealand (e.g., Whateley et al., 1974; Alexander et al., 1983), among Romanov, Lacaune, Prealpes de Sud, and Ile-de-France in France (e.g., Poindron et al., 1984; Le Neindre et al., 1998), and among Dalesbred, Scottish Blackface, Suffolk, and Soay breeds in the United Kingdom (Shillito-Walser, 1980; Dwyer and Lawrence, 1998, 2000a; Table 1). Because these studies compared different breeds by using a variety of behavioral measures, it is hard to draw any clear conclusions, except when comparing breeds within the same study.
|
). These breeds represent a relatively unselected and extensively managed breed (i.e., Scottish Blackface), and a breed that has undergone considerable amounts of genetic selection for lean tissue growth and is generally managed intensively (i.e., Suffolk). These breeds showed significant and repeatable differences in all aspects of maternal behavior investigated. Suffolk ewes were slower to begin grooming their lambs after birth; groomed their lambs in a series of short bouts, so spent less time licking lambs; made fewer low-pitched bleats to their lambs; and accepted a lower proportion of the sucking attempts of their lambs than did Blackface ewes (Table 1). Suffolk ewes were also more likely to express fearful (withdrawing), aggressive, or rejection behaviors toward the lambs (Table 1), particularly as primiparous ewes, and to express these behaviors even as multiparae, which was not seen in Blackface ewes (Figure 1). When offered a choice between their own and a similar alien lamb in a Y-maze, Suffolk ewes took longer to approach their own lambs and spent less time with their lamb than Blackface ewes (Pickup and Dwyer, 2002a; Table 1). In addition, they had shorter suckling bout lengths, were more likely to terminate suckling bouts, and were generally further from their lambs than Blackface ewes (Dwyer and Lawrence, 1999b, 2000a). These results demonstrate that significant variations in maternal care exist between breeds in behaviors important for the survival of the lamb, and this results in differences between breeds in lamb mortality when managed under identical conditions (Dwyer and Lawrence, 2005b).
|
, 1990). When ewes’ responses to handling of their lamb were scored, Merino ewes also rated lower than other breeds (Whateley et al., 1974). In comparisons of French breeds, Romanov ewes also show better maternal care (e.g., more licking, grooming, and lamb acceptance, and less aggression) than the other breeds (Poindron et al., 1984; Le Neindre et al., 1998). Thus, it is clear that considerable breed differences exist in the quality of expressed maternal behavior. In general, hill, upland, and more primitive breeds, which have been subjected to less human intervention, show the highest levels of maternal care, whereas more intensively selected and reared animals display greater variability in maternal behavior and express the poorest quality of maternal care (reviewed by Dwyer and Lawrence, 2005b). Maternal Temperament
In several studies, maternal behavior has been assessed by using a composite measure of ewes’ reactions when their lambs are handled by a shepherd, called the Maternal Behavior Score (MBS; O’Connor et al., 1985). This score shows variation within and between breeds and is related to both lamb survival and weaning weight (Whateley et al., 1974; O’Connor et al., 1985). In general, ewes with a low MBS have higher lamb mortality, although survival does not increase with an increase in MBS above the average (Everett-Hincks et al., 2004; Sawalha et al., 2007). Heritability estimates of this measure for both Scottish Blackface (Lambe et al., 2001) and Coopworth ewes (Everett-Hincks et al., 2004) are relatively low (h2 = 0.09 to 0.13). The low heritability of this trait may reflect the fact that this measure quantifies both the ewe-lamb relationship (which is affected by the behavior of both the ewe and lamb) and the underlying emotivity or temperament of the ewe, as well as her previous rearing experience. Romanov ewes, for example, are considered to be better mothers (in terms of licking, grooming, and attachment to the lamb) in comparison with the Lacaune breed (Le Neindre et al., 1998). However, Romanov ewes display greater flight from humans and stand further from their handled lambs than Lacaune ewes (behavior that would have earned them a lower MBS). These responses are believed to be a result of greater emotivity of the Romanov breed (Boissy et al., 2005), in comparison with the Lacaune, rather than a poorer quality of maternal care.
In studies in which Merino ewes were selected for temperament by measuring their responses to a variety of tests, the "calm" ewes spent more time grooming their lambs than did "nervous" ewes, and bleated more frequently to their lambs (Murphy et al., 1998). Lamb mortality in these lines was also lower in the calm ewes compared with the nervous animals. Ewes previously selected for their ability to rear lambs showed behavioral differences in an approach-avoidance test, indicative of increased calmness (Kilgour and Szantar-Coddington, 1995). Thus, temperament may also contribute to individual differences in the quality of maternal care expressed by ewes. Temperament traits are believed to show moderate heritability; for example, heritability of distress or high-pitched bleat frequency is 0.48 (Boissy et al., 2005), and heritability of behavior in the arena and box tests is approximately 0.23 (Martin et al., 2004). Selection of ewes on the basis of their temperament may therefore be a route to improve lamb survival.
Lamb Behavior
As discussed previously, the responses of the parturient ewe can be affected by the sensory and behavioral cues she receives from her lamb. In behavioral studies of breed differences between Blackface and Suffolk ewes, significant variations in lamb behavior were also observed, with Suffolk lambs taking longer to stand and suckle after birth than Blackface lambs (Dwyer and Lawrence, 1999b; Dwyer et al., 1996). Suffolk lambs were also significantly more vocal than Black-face lambs (Dwyer et al., 1998). Thus, it is possible that some of the apparent differences in maternal behavior seen between breeds could be due to differences in stimulation received from lambs differing in behavior. To investigate this possibility, we carried out an embryo transfer study between the 2 breeds to produce 4 different combinations of ewes and lambs (Blackface ewes with Blackface lambs, Blackface ewes with Suffolk lambs, Suffolk ewes with Blackface lambs, and Suffolk ewes with Suffolk lambs; Dwyer and Lawrence, 1999a; Dwyer et al., 1996). These results demonstrated that the behavior of the ewe and lamb at parturition were largely independent of one another, with ewes spending equivalent amounts of time grooming the 2 different breeds of lambs, despite differences in lamb vigor (Figure 2; Dwyer and Lawrence, 1999a). Likewise, time taken by the lamb to stand and reach the udder was not affected by differences in maternal grooming attention, although ewes did modify the subsequent sucking behavior of their lambs (Dwyer and Lawrence, 2000a). This indicates that variation in maternal behavior cannot be attributed to lamb responses, and appears to be intrinsic to the ewe.
|
|
CONSISTENCY IN EXPRESSION OF MATERNAL BEHAVIOR |
|---|
The intense focused period of maternal care around parturition declines rapidly, with grooming behavior infrequent or absent within a few hours of birth (Dwyer and Lawrence, 1998). This period coincides with completion of the development of lamb recognition by the ewe (Keller et al., 2003), and a quiescent period following the initial sucking behavior of the lamb (Dwyer, 2003). Further development of the relationship occurs over the next 12 to 24 h, with an increase in the ability of the lamb to recognize its mother (Nowak, 1990). Thereafter, the ewe-lamb interaction is characterized by frequent sucking interactions, a close spatial relationship, and increased maternal vigilance, behaviors which are believed to increase lamb survival (Dwyer and Lawrence, 2005b).
Ewes that express higher levels of maternal care at parturition (i.e., higher levels of maternal grooming, udder acceptance, and low-pitched bleating) continue to show higher levels of other maternal behaviors related to lamb survival, in comparison with ewes with poorer maternal care. At 24 h after delivery, Blackface ewes appear to show better distance recognition of their lambs, and are more attracted to their own lambs than are Suffolk ewes (Pickup and Dwyer, 2002a). Blackface ewes maintain a closer spatial relationship to their lambs than Suffolk ewes throughout lactation (Dwyer and Lawrence, 1999b, 2000a), and show a higher frequency of vigilance (or "head-up") postures (Pickup and Dwyer, 2002b). In addition to their better acceptance of lamb suckling behavior at birth (Table 1; Dwyer and Lawrence, 1998, 1999b), Blackface ewes continue to accept more suckling attempts by their lambs, and suckling bouts are longer than those of Suffolk ewes throughout lactation (H. E. Pickup and C. M. Dwyer, unpublished results). Thus, ewes show a consistency in their expression of maternal care throughout lactation, and maternal behaviors expressed at parturition are indicative of their continuing quality of maternal care.
Between Pregnancies
As described previously, primiparous ewes show impairments in the expression of maternal behavior in comparison with multiparous ewes. However, a comparison of the behavior of the same ewes in successive pregnancies revealed that ewes were consistent in their behavior across parity for caregiving behaviors (e.g., maternal grooming; Figure 3) and for rejection or lamb avoidance behavior, although aggressive behaviors were not repeatable (Dwyer and Lawrence, 2000b). These results suggest that, although the behavior of the ewe will improve in the following pregnancy, the ewe’s behavior in her first parity is indicative of her behavior in subsequent years, and that a ewe expressing poor maternal care in her first pregnancy is likely to continue to do so in other pregnancies. This repeatability of maternal behavior suggests an underlying genetic or physiological determinant of maternal behavior, or both, that is not affected by environmental conditions that may differ across pregnancies.
|
|
PHYSIOLOGICAL CONTROL OF MATERNAL BEHAVIOR |
|---|
). The immediate onset of maternal behavior at parturition is triggered by the central release of oxytocin (Kendrick et al., 1987; Lévy et al., 1992), primarily from the centrally projecting oxytocinergic neurons of the paraventricular nucleus of the hypothalamus (Kendrick, 2000). This central release of oxytocin, matched by a peripheral release to entrain uterine contractions during labor, is brought about by the stretching of the vagina and cervix (i.e., the Ferguson reflex) that accompanies the passage of the fetal lamb along the birth canal (Kendrick et al., 1988, 1991), and both oxytocin release and maternal behavior can be abolished by peridural anesthesia (Krehbiel et al., 1987; Lévy et al., 1992). The priming roles of estradiol and progesterone, particularly estradiol, for the onset of maternal behavior appear to be achieved by their actions in increasing transcription of mRNA for oxytocin (Broad et al., 1993) and its receptor (Broad et al., 1999) in specific areas of the ovine brain linked to maternal behavior. Activation of oxytocinergic neurons brings about modulation in neurotransmitter release in the olfactory bulb, which is important for the formation of olfactory memory and the selective behavior of the ewe for her own lamb (Keverne et al., 1993; Lévy et al., 1993; Kendrick, 2000).
Investigation of circulating steroid hormone concentrations throughout gestation in Scottish Blackface and Suffolk ewes demonstrated that Blackface ewes have elevated estradiol concentrations and estradiol-to-progesterone (E:P) ratios in comparison with Suffolk ewes (Dwyer et al., 1999, 2004). Furthermore, estradiol concentration, and the E:P ratio, is correlated with some maternal behaviors, specifically maternal grooming and low-pitched bleating (Shipka and Ford, 1991; Dwyer et al., 1999, 2004). This suggests that the breed differences in maternal behavior seen in these animals may be mediated via differences in circulating estradiol. In addition, ewes that are underfed during pregnancy have differing physiological profiles during gestation compared with well-fed ewes. Specifically, undernutrition is associated with higher plasma progesterone in late gestation (O’Doherty and Crosby, 1996) and a lower E:P ratio at birth (Dwyer et al., 2003). Thus, elevated progesterone in underfed ewes, and a lower E:P ratio, might contribute to the poor maternal behavior and high level of maternal desertion seen in these animals. Circulating estradiol concentrations do not, however, contribute to the behavioral differences seen between primiparous and multiparous ewes (Dwyer and Smith, 2007), suggesting that the effects of experience on maternal behavior may be mediated by other factors, such as regulation of the oxytocin receptor and estradiol receptor-
(Broad et al., 1999; Meurisse et al., 2005).
|
FACTORS AFFECTING THE BEHAVIOR OF THE LAMB |
|---|
) that must be coordinated with the birth process and behavioral responses after birth for a successful transition to be accomplished. Thus, the behavior of the lamb is also important in ensuring survival, and several studies have shown that lamb survival is enhanced in lambs that stand and suckle quickly (Alexander, 1958; Owens et al., 1985; Cloete, 1993; Dwyer et al., 2001).
The expression of lamb behavior at parturition is influenced by lamb factors (e.g., breed or line, sex), prenatal influences (e.g., prenatal nutrition, litter size), ewe factors (e.g., placental sufficiency, condition score, parity), and the birth process (Dwyer, 2003). Lamb behavioral progress is retarded in males in comparison with ewe lambs, in larger litter sizes compared with smaller sizes, in lambs that have experienced a difficult delivery, and in low birth weight lambs in comparison with larger lambs (Dwyer, 2003). In addition, lamb behavior, particularly reaching the udder and suckling, is slower in the lambs of primiparous ewes compared with lambs of multiparous ewes, and in ewes that have mobilized large amounts of backfat during gestation (Dwyer, 2003). Undernutrition during pregnancy, leading to a reduction in birth weight, will therefore have an impact on lamb behavior, as does placental insufficiency (Dwyer et al., 2005). A number of studies have considered whether deficiencies or supplementation of specific trace elements can improve neonatal lamb vigor. Subclinical cobalt deficiency has been reported to increase the time taken by the lamb to stand and suckle after birth and to increase lamb mortality (Fisher and MacPherson, 1991). However, marginal cobalt deficiency has no impact on lamb neonatal behaviors or survival, although periconception cobalt deficiency reduces postnatal lamb activity and exploration (Mitchell et al., 2007). Supplementation of pregnant ewes with selenium may reduce lamb mortality (Kott et al., 1983; Langlands et al., 1991; Munoz et al., 2006), although no data on lamb behavior are given in these studies. Supplementation with vitamin E, fatty acids, or both is also considered to improve lamb survival and to reduce the time taken by lambs to reach the udder and suckle (Williamson et al., 1996; Capper et al., 2006). Thus, nutritional management of the pregnant ewe can enhance the behavioral activity of her lambs at birth and improve survival.
As described previously, breed differences in lamb vigor at birth have been reported in a number of breeds and in crossbred lambs (Slee and Springbett, 1986; O’Connor and Lawrence, 1992; Dwyer et al., 1996; Dwyer and Lawrence, 1999a). In addition, line differences within breed (Dwyer et al., 2001; Cloete et al., 2002) and sire effects within breed (Dwyer et al., 2005) have been reported. There are few estimates of the heritability of lamb behaviors, and those that do exist suggest a heritability similar to lamb survival and MBS (e.g., h2 = 0.16; C. M. Dwyer and J. Conington, unpublished data). Our results do, however, indicate a significant maternal component to lamb behavior, although whether this is a genetic effect or a permanent environmental effect is still to be elucidated. In addition, whether these effects can be attributed to differences in maternal behavior, uterine capacity, or other maternal influences is yet to be determined.
|
IMPLICATIONS FOR LOW-INPUT SHEEP MANAGEMENT |
|---|
). The general finding that these ewe breeds tend to have more difficult deliveries and a poorer quality of maternal care (Dwyer and Lawrence, 2005a,b) indicates that more intensive management has kept animals within the flock that might not have delivered or reared a lamb in a less intensive system. Without specific interventions to improve survival traits in these flocks, movements to systems with less labor at lambing are likely to cause a significant increase in ewe and lamb mortality and in animal welfare problems, at least in the short term.
Although the present estimates of heritability of maternal and lamb behaviors are low, these are of an order similar to those of other health and welfare traits (e.g., lamb survival; Sawalha et al., 2007). Furthermore, selection for improved lamb survival has been carried out successfully (Knight et al., 1988; Kilgour and Haughey, 1993; Cloete and Scholtz, 1998), demonstrating that this selection is possible. However, selection on behavioral traits is difficult because these traits are time-consuming to measure and can often be recorded only at very specific times. Identification of suitable proxy measures is therefore likely to improve our ability to record these traits on farm. Currently, we have developed lamb vigor scoring systems (where, for example, lambs are scored from 1 to 4 on their activity within 5 min of birth and their suckling ability over the first 3 d of postnatal life), which are in use on commercial farms and which show significant correlation with more detailed lamb behavior measures and that detect breed differences in behavior (C. M. Dwyer, unpublished results). Genetic analysis of these data are underway, and may allow lamb behavior measures to be recorded and selected more readily on farm. The MBS is often used as a proxy for maternal behavior; however, the confounding of this measure with maternal temperament and lamb behavior limit its application. Direct selection on maternal temperament may be an alternative strategy to improve expression of maternal behavior, as has already been done in Australia (Martin et al., 2004), although the consequences of selection on this trait for other behaviors, such as flocking or antipredator responses, have yet to be determined. Selection on temperament does, however, have the advantage of being measurable in young ewes before investment in reproduction has taken place (Kilgour, 1998). The correlation of behavioral traits with some aspects of maternal physiology, and the existence of significant breed differences in these measures also offer the future possibility of developing gene marker tests that predict maternal behavior.
In addition to the genetic effects, both ewe and lamb behavior are affected by environmental factors operating during the prenatal period, particularly nutrition. This involves both undernutrition, as occurs routinely with pregnant hill ewes, and deficiencies in specific nutrients. Although undernutrition can impair the behavior of the ewe and lamb (Dwyer, 2003; Dwyer et al., 2003), in addition to its impact on other processes, such as lactation, with detrimental consequences for lamb survival, to date, the effects of deficiencies in trace elements and other nutrients have concentrated specifically on the lamb, and impacts on ewe maternal behavior have not been investigated. There is, however, increasing evidence that nutrition during early pregnancy, or even before conception, may have a greater impact on lamb development and subsequent health than has previously been appreciated (Ashworth et al., 2007; Mitchell et al., 2007), and this may affect the development of ewe-lamb bonding.
The onset of maternal behavior, particularly of primiparous ewes, is dependent on a coordinated sequence of neuroendocrine events and sensory stimuli, and disruptions to this process can result in behavioral disturbances (Lévy and Poindron, 1987; Lévy et al., 1995). Management practices that either deliberately (by moving recently lambed ewes to small pens) or inadvertently (through disruption to the flock) move ewes away from the birth site early may hinder the normal development of maternal selectivity as the ewe transfers her attraction from the amniotic fluids on the ground to those in the coat of the lamb. Parturient multiparous ewes are more sensitive to the physiological signals that underpin maternal behavior and may begin to express maternal care toward neonatal lambs before giving birth themselves or during labor. Housing ewes at a high stocking density can bring parturient ewes into closer contact with newborn lambs than would occur in a more natural situation, in which parturient ewes can choose seclusion, thereby leading to an increase in mismothering and lamb stealing. In addition, newborn lambs are initially attracted to any moving object (Vince, 1993), and housing and some management practices can retard the development of ewe recognition by the lamb (Poindron and Schmidt, 1985; Val-Laillet and Nowak, 2006), thereby weakening the development of the ewe-lamb bond. Minimizing disruption and stress around lambing time therefore allows the normal sequence of events in the development of behavioral interactions between the ewe and lamb to occur undisturbed.
In conclusion, in this review the behaviors surrounding the successful onset of maternal care in the ewe, the behavioral development of the lamb, and the formation of a selective attachment between the ewe and lamb have been described. This process is a vital step in the survival of the lamb and is fundamental to the ability of the lamb to acquire nutrition and protection during early postnatal life. Maternal behaviors show a consistency both within and between successive pregnancies, indicating that there may be underlying permanent characteristics of the ewe that lead to her showing a particular style of maternal care. Although the genetic basis of these behaviors has not yet been fully explored, the existence of significant breed differences in maternal behavior indicates that at least some of the variation in maternal care has a genetic basis. In addition, physiological differences exist between breeds in some aspects of the neuroendocrine processes that underlie maternal behavior, indicating that these breed differences in behavior may have a hormonal basis. Currently, selection on the basis of maternal behavior is difficult and relies on proxy measures that may be only partly related to maternal care. The possibility of developing gene tests, which may identify young ewes that will show different qualities of maternal care, will significantly improve our ability to select for maternal behavior. The development of ewe-lamb bonding is, however, essentially an interaction between 2 partners, and the behavior of the lamb is also important in ensuring its own survival. There is some evidence that these lamb behaviors can be influenced by genetics, and hence that selection for lamb vigor would improve lamb survival. In addition to the genetic variation in these behaviors, several environmental factors also have an impact on the quality of the maternal relationship with the lamb. Therefore, alongside selection for desirable behavioral traits, management, particularly of nutrition and the avoidance of stress at parturition, can play a significant role in optimizing the behavioral development of the ewe-lamb bond.
|
Footnotes |
|---|
2 Presented at the Sheep symposium at the annual meeting of the American Society of Animal Science, San Antonio, TX, July 8 to 12, 2007.
3 Corresponding author: cathy.dwyer{at}sac.ac.uk
Received for publication July 5, 2007. Accepted for publication August 9, 2007.
|
LITERATURE CITED |
|---|
-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Res. 442:171–174.[CrossRef][Medline]This article has been cited by other articles:
|
|
 |
|
  M. L. Thonney, P. A. Martinez-Hernandez, J. B. Taylor, and D. L. Thomas Sheep symposium: Biology and management of low-input lambing in easy-care systems J Anim Sci, April 1, 2008; 86(14_suppl): E244 - E245. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
Top
Abstract
INTRODUCTION
