What makes a good mother : components and comparative aspects of maternal behaviour in ungulates.

Abstract

Proc. Aust. Soc. Anim. Prod. Vol. 17 WHAT MAKES A GOOD MOTHER?: COMPONENTS AND COMPARATIVE ASPECTS OF MATERNAL BEHAVIOUR IN UNGULATES G. ALEXANDER (INVITED REVIEW) 25 SUMMARY This review examines the components of maternal and offspring behaviour in The large literature on non domestic species is drawn to the ungulates. attention of scientists who work with domestic animals. The review identifies behavioural traits of demonstrated or putative value for Survival of Offspring, The mechanisms of control of maternal behaviour and of especially in sheep, mutual recognition between mother and young are also briefly reviewed. The possible use of behavioural traits in selection programs for improving lamb survival, and in designing systems of husbandry for lambing is considered. INTRODUCTION There are few, if any species of ungulate, in which the young can survive substitute that provides sustenance and behaviour is therefore essential in any infant animals, although factors other mortality (Alexander 1984). mammal, and certainly no species of in the absence of maternal care, or a protection. A knowledge of maternal program aimed at reducing mortality of than behaviour may be major causes of The large literature on maternal behaviour in mammals covers quantitative and qualitative descriptions of behaviour in a wide variety of species It deals with the growing body of representing many mammalian families. experimental evidence about factors governing the onset and maintenance of maternal behaviour, and about the senses and sensory cues involved in mutual recognition between mother and offspring. The literature includes books and Lehrman 1961; reviews that deal with mammals generally (Hediger 1955; Rheingold 1963; Harper 1970; Shillito-Walser 1977; Rosenblatt 1980; Gubernick and Klopfer 1981), with ungulates (Fraser 1968; Lent 1974) and with sheep specifically (Alexander 1960, 1980; Hersher et al. 1963; Squires 1975; Gonyou Poindron et al. 1984). 1983/4; The primary objects of the present review were to draw the large literature on non-domestic species to the attention' of people who work with domestic animals, and to search for and identify behavioural traits that might be correlated with superior mothering ability, especially in sheep. These traits could be used in selection programs or in the design of husbandry The review examines maternal procedures aimed at reducing infant mortality. behaviour in the 'ungulate' families wh$ch have an evolutionary relationship with sheep and where members. mostly produce a single offspring each' year. Offspring behaviour and the role of themale are also considered briefly. The ungulates represent about 200 species of quadrupedsr that are predominantly horned and herbivorous'and include most of 'the animals farmed by humans; The - Suidae (pig ' family') whose members, mostly produce several large * litters of immature young each year are largely excluded from the review. It is recognized that some of the behavioural traits might be only indirectly relevant to modern livestock and farming% conditions, yet their presence might reflect a superior, CSIRO, Divisionof Animal Production, P.O. Box 239, Blacktown, N.S.W.,. 2148. . 26 Proc. Aust. Soc. Anim. Prod. Vol. 17 innate mothering ability. It was not practicable to cite more than a fraction of the hundreds of papers describing maternal behaviour; recent papers are given precedence, and the reader is referred to Lent (1974) for a comprehensive review of earlier In contrast with the extensive, detailed papers dealing with ungulates. literature on domestic ungulates, the copious literature on maternal behaviour in wild ungulates is sparse on detail of peri-partum events, for the obvious reason that these are difficult to observe in the wild. Even with zoo animals, few observers seem prepared to mount the necessary surveillance. FACTORS SHAPING MATERNAL BEHAVIOUR IN UNGULATES Consideration of the major influences likely to have shaped mother and evolution should facilitate behaviour ungulates during their Young identification of significant behavioural traits. Ungulates are generally mobile, social animals, and since their young are entirely dependent on maternal milk supply initially, there is a need for the mother to develop a bond with her offspring, and to recognize, maintain contact with, and suckle her own offspring to the exclusion of alien young, which could monopolize the limited milk supply. The ungulate mother needs to graze or browse throughout most of the daylight hours, to meet her nutritional requirements, which are about 50% higher during lactation than in advanced pregnancy (Weston and Hogan 1986). Behaviour patterns that allow grazing, as well as any watering, without the mother losing track of the offspring, are therefore necessary. The position of ungulates in the food chain means that they are subject to The young are of an attractive size for the mammalian and avian predation. Ryan 1972; predators that usually share their habitat (Rowley 1970; Nowasad Predator avoidance would Gluesing et al. 1980). Estes and Estes 197% 1975; therefore be expected to be a. feature of maternal,behaviour. Small ungulate young such as lambs (Alexander and McCance 1958), caribou (Hart et al. 1961) and ,piglets (Curtis 1970) are prone to hypothermia during the post-partum drying of the coat, or longer in 'Suidae; and newborn young are also inexperienced in coping with environmental hazards,such as steep slopes, streams Behaviour 'of the mother might therefore be expected to provide and bogs. environmental protection for the newborn., , . COMPONENTS OF MOTHER'AND YOUNG BEHAVIOUR Pre-partum isolation The' females of many species tend to leave the social group during the days These species include giraffe (Lang-man 1977),, horse or hours prior to birth. (Tyler 197203), zebra (Klingel 1969), antelope (Sekulic .1976) ,, impala (Jarman 1979), feral goat (Rudge 1970), Barbary sheep (Haas 1959), Big horn sheep Sh,illito and (Shackleton and Haywood 1985), feral Soay sheep (Grubb 19% Sharafeldin et al. 1971 i Hoyland 1971) land domestic ,sheep (Fraser 1926; Gonyou 1983/4). However, isolation KilgOUr 1972; Whitelaw and Watchorn 1975; for parturition is by no means the rule for domestic sheep (Stevens, et al. '1981) or cattle (Edwards and Broom 198% and appears subordinate to selection of a The tendency to seek isolation is birth site in feral goats (O'Brien 1983); less marked in primiparas than in multiparas, for. example in domestic goats _ (Lickliter 1984/5a)* With sheep8 the tendency for isolation 'can be exploited for for the purpose of identification of lambs during indoor lambing, by ;Proc. Aust. Soc, Anim. Prod. Vol. 17 27 providing cubicles for sheep to enter, but with a high step which prevents lambs from leaving (Gonyou and Stookey 1981)h At the pre-partum stage the previous season's offspring may be driven off, as observed for example, in hog deer (Miller 1975) or reedbuck (Jungius 1970), but this behaviour was not observed in feral Soay sheep (Grubb 1974). Birth in isolation should facilitate formation of an exclusive bond where birth takes place in the presence of other between mother and newborn; parturient females aberrations in bond formation are common (Welch and Kilgour 1970; Alexander et al. 1983a). In many species, parturient females are attracted by a recent or imminent birth, and in some species, such as moose, isolation is maintained by vigorous aggression towards encroachment by others of the same species (Bogomolova and Kurochkin 1984). Selection of a birth site There is little objective evidence about factors that determine the precise site of birth and features that might be attractive to the parturient female of any ungulate species, except feral goats (O'Brien 1983) which are likely to choose birth sites th,at are protected either by overhead cover or by Subjectively, proximity to vertical surfaces that reduce wind velocity. mountain sheep (Ovis dalli) are said to be attracted by the security of high Geist 1971) and domestic sheep are said to favour cliffs (Pitzman 1970; depressions and slopes, and proximity to hedges or walls (Smith 1965; Whitelaw and Watchorn 1975) and Soay sheep to seek a sheltered site (Shillito and Hoyland 1971) . Domestic sheep show a consistent preference to lamb at the highest end Other species such as moose of a paddock (Alexander, unpublished data 1982). 1974) and a variety of deer and antelopes (Lent 1969; KOk 1975; (Stringham Jarman 1979) are said to seek the seclusion of thick vegetation for parturition. There would be survival advantages in selecting a birth site that provided protection from weather, and safety from misadventure, but .the limited literature indicates that neither wild nor domestic ungulates display wisdom here. Goats may be exceptional (0,'Brien 1983), but studies with other species Sheep in an environment as varied as O!Brien% study area would be revealing. have been reported to seek shelter more often as parturition approaches (Hunter 1954), but generally, when sheep lamb in shelter they are themselves cold; such Miller 1968; Winfield et al. 1969; as soon after being shorn (Hunter 1954; In addition, newborn lambs a+. the young of other Lynch and Alexander 1977). species, such as red deer and lechwe, have been observedmired, drowned or - abandoned after tumbling down a steep incline, when born in close .proximity to Kilgour 'et al, natural hazards (Lent 1969; Pitzman 1970; Arman et al. 1978; 19,83) l . In many species, including domestic' and mountain sheep, the exact birth site frequently appears to be at the location where the foetal fluids are spilt Arnold and Morgan Pitzman 19.70; Kilgour 1972; (Fraser' 1965;.., Smith 1965; .1975);.* The female appears to be 'strongly attracted to this Sp0.t; however, if the birth process is prolonged ,the animal may wander away and give birth . elsewhere. 28 Pro& Aust. Soc. Anim. Prod. Vol. 17 an essential 'first stage in the bonding process discussed below (Levy and Alexander et al. 1986), but it can lead to neglect if the Poindron 1984; newborn rolls from the birth site immediately after birth. As reported for domestic sheep (Kilgour et al. 1982), horses (Tyler 1972-3) and red deer (Arman et al. 1978), the mother concentrates on the spilt fluids and fails 'to attend to her offspring. The attraction to the fluids can also lead to interference in births by other parturient females (Lent 1974), and to attraction or permanent attachment of females to alien newborn young. This is well documented for sheep (Fraser Inexperienced ewes are particularly prone to having their newborn lambs 1926). stolen by experienced ewes (Alexander et al. 1984). . Nesting Obvious thermal protection for the young is provided by Suidae only, whose members build nests about 2 m across and 1 m high of grass and shrubs (Atwell Stolba and Wood-Gush 1981; Martys 1982; Jensen 1986). Among Bovidae 1976; (sheep and cattle family) pawing the ground and scraping out a shallow depression where the fluids have been spilt is frequently observed just before this behaviour could be regarded as vestigial nest-building or during birth; (Fraser 1926; Pitzman I97Oi Sharafeldin et al. 1971; Arnold and Morgan 1975; Whitelaw and Watchorn 1975). These 'birth beds' remain the focus of activity during birth and for several hours thereafter (Pitzman 1970; Kilgour 1982), and the animals may return to them during the next few days. Parturition Normal delivery in most ungulates follows a regular pattern (Lent 1974) and rarely lasts more than 1-2 h. The female usually lies during labour, but birth is often completed by the female standing, and the cord breaks when However, mares usually remain - stretched, without maternal intervention. recumbent for 10 min or more, allowing a significant transfer of blood from the Primiparous cattle (Edwards and Broom placenta to the foal (Rossdale 1967). 1982) and sheep (Alexander 1960) tend to remain recumbent for many minutes after delivery whereas multiparas are usually on their feet almost immediately. The delay in standing usually delays the start of grooming. The offspring are usually born in the anterior position (nose and forefeet foremost).Some ungulates, such as horses and zebra (Klingel 1969) and perhaps cattle (Duffy 1972) appear to suspend parturition when disturbed by humans or predators, but sometimes to the detriment of the foetus. Because of environmental control of the breeding season, mediated by photoperiod and perhaps by other factors, such as forage supply (Bunnell 1982), females of most ungulate species tend to mate synchronously, and give birth in spring and summer when forage is plentiful (Rutberg 1984). The concentration of 80 per cent of births in the space of an oestrous cycle (2-3 weeks), typical of the wildebeest for example, has been labelled a predator defence by Estes '(1976). The predators may bedeterred by large aggregations of calving females; and the presence of predation-prone young for a limited period only, '=Y This interpretation of the value of synchronous restrict the numbers killedbirths has been disputed by Rutberg (1984) on the grounds that the American bison,, which calve synchronously, do not aggregate for calving. The distribution of births throughout the 24 h of the day varies widely In wildebeest there is a peak between 6 a.m. and 12 noon, between species. regarded by Estes (1976) as a mechanism for avoidance of nocturnal predators. In'horses most births' occur during the hours of darkness (Rossdale 1968ai Tyler 4nc)rr - 18 whereas there appears to be no consistent peak of births in sheep ' Proc. Aust. Soc. Anim. h3od. Voi?.' 17 29 Sharafeldin et al. 1971; Tomar 1979) or cattle (Edwards 1979) (George 1969; despite individual reports of peak lambing or calving at certain hours (George While the endocrine events that lead to birth George and Barger 1974). 1969; in ungulates have been well researched (Nathanielsz 1976), it is clear that the environmental factors that influence the hour of birth are poorly understood. The hour of feeding is, however, known to influence the hour of birth in domestic sheep (Gonyou et al. 1981). It is well documented that prolonged or difficult birth (dystokia) inhibits maternal behaviour in sheep (Wallace 1949; Alexander 1960; Shelley Winfield et al. 1972) and cattle (Neumann et al. 1974; Edwards and Broom 1970; 1982 ), probably through pain and shock. Dystokia appears to be prevalent in Whitelaw and Watchorn 1975; Elving et al. certain breeds (George 1975, 1976; Birth problems also occur in other species including musk ox (Norment 1986). 1973)f whitetailed deer (Townsend and Bailey 1975) and wildebeest (Estes and Birth difficulty also affects Estes 1979), no doubt with similar results. behaviour of the newborn, and may delay or prevent successful sucking (Haughey 1980). Grooming of the newborn Grooming has been described for a variety of species including red deer (Arman 1974), bontebok (David 1975), zebra (W<st 1976), cattle (Brownlee 1950; Selman et al. 1970ai Edwards and Broom 1982) and sheep (Alexander 1960; Morgan Bareham 1976). and Arnold 1975; Grooming appears to be an extension of the attraction to the spilt foetal fluids, and usually begins by consumption of the remnants of the foetal membranes. It grades into a thorough licking of the newborn, usually beginning with the head, the first part of the offspring to move, and continues onto the body after the newborn has stood, with particular attention being paid to the anogenital region. The direction of the licking appears to be against the lie of the hair (Meier 197% Fluids on the .ground. and soiled vegetation are also sometimes consumed, as by mule deer for example (Goldberg and Haas 1978). Grooming is initially intense>-but becomes spasmodic within half an hour or so of birth in sheep and after several hours in horses (Rossdale 196833); bouts of grooming can be interspersed by episodes of grazing or eating hay at least in In sheep the amount of grooming of sheep and cattle ,(Edwards and Broom 1982). individual lambs is less for multiples than for singles, and is reduced for the lambs born later in a litter (Holmes 1976; Atroski and Osterberg 1979). Beyond this immediate post partum period, grooming of the young in most species is confined to brie`f occasional episodes. Several functions of grooming have been postulated, bstly with little' or Bareham 1976) Edwards and Groom ' no experimental evidence (Lent 1966, 1974; They include stimulation of respiration, muscle tone, circulation and 1982). excretion, drying to reduce heat loss, removal of birth odour-to avoid attracting predators, hair-care to increase thermal insulation and finally the bonding and learning of offspring odour by the mother (Poindron et al. 1984). < Grooming. is minimal or Camelidae, Hippapotamidae). ' absent in ungulate families (Suidae, . Placentaphaqia The placenta, or 'afterbirth'; in most ungulates is voided within 'about but there appears to be wide variation between species, even 6 h of birth; within the same family. The median period appears to be about 1 h in Equidae as . in horses, (Rossdale 1967) and zebras (Whist 1976) and in Cervidae such as caribou (Lent 196% It is frequently longer in, Bovidae; for example,. about 3 h . 30 Proc. Aust. Soc. Anim. Prod. VoZ. 17 in sheep (Arnold and Morgan 1975), about 4 h in cattle (Edwards and Broom 1982) though only about 1 h in hartebeest (Gosling 1969). In discussing the possible attraction of afterbirth to predators, David (1975) and Estes and Estes (1979) claim that there is a survival advantage in delaying the dropping of the placenta until the newborn is strong enough to run from any predator. Complete placentaphagia is common in some ungulate families such as Cervidae, for example in mule deer (Goldberg and Haas 1978), and Bovidae, including domestic cattle (Brownlee 1950 i Edwards and Broom 1982). Partial consumption of the placenta is sometimes seen in sheep (Arnold and Morgan 1975) 1978). species such as giraffe (Kristal and Noonan and many other Placentaphagia is not seen in Equidae (Klingel 1969; Tyler 1972-3), Camelidae, or Suidae (Frgdrich 1974). Placentaphagia is postulated to minimize the risk of predation in species that remain near the birth site for several days or longer Townsend and Bailey 1975). Female elephants appear to eat (Gosling 1969; little or none of the foetal membranes or placenta, but are reported to disperse the birth detritus or to stamp it into the ground and cover it (Leuthold and Leuthold 1975); with such a large animal as a newborn elephant, this disposal can scarcely be regarded as a predator defence. Also, 'afterbirths' are a substantial, readily available source of food for potential predators such as foxes (Alexander et al. 19671, and it can be argued that not to eat the placenta would be a better defence than consuming it. Nutrition and endocrine functions have also been suggested for placentaphagia (Townsend and Bailey 1975; Edwards and Groom 1982), but experimental evidence is lacking. Maternal behaviour and offspring's excretions Maternal licking of the ano-genital region appears to facilitate defaecation and urination in some, species including domestic cattle (Kovalcik et al. 1980; Metz and Metz 1986) and zebra (West 1976), but it is not essentialfor excretion, at least in sheep (Grubb 1974). Many ungulates, including domestic cattle (Selman et al., 1970a), Barbary sheep (Haas 1959), red deer (Arman 1974), white tailed deer (Faatz 1977) and hartebeest (Gosling 1969) Consumption of offspring's consume 'the faeces and/or urine of their young. excretions does not appear to have been recorded in domestic sheep. Like placentaphagia, removal of the odour of the excretions is said to minimize the risk of predation (Gosling 1969; Stringham 1974). , Reactions of group members to newborn In most species, non-parturient fe-males appear to pay only desultory attention to the newborn. However, female elephants show excitement and interest in birth by another female and assist in the dispersal of birth' detritus (Leuthold and Leuthold 1975). Pony mares are reported to gather around a parturient mare ,and may interupt the progress of labour (Rossdale 1968b), and non-parturient 'mountain sheep may also display interest in newborn lambs (Geist , 1971) 0' Suckling behaviour A variety of maternal cues appear to aid the ungulate newborn in 'its These include warmth and softness of bare skin initial search for the udder. swine, Welch and Baxter sheep, Vince 1986; ( goats, Stevens and* Linzell 1974; Alexander 1,986) and maternal orientation and geometry (sheep, Smith 1971;, et al. 1964),. A hunched stance appears to facilitate suckling in most species, whereas 'some suckle initially in the lying position (red deer, Ax-man 1974; '. white tailed deer, Langenau and Lerg 1976; steenbok, moose, Stringham 1974; It is important at this time that the mother remains still . Robinson'.1977)o I (Alexander 1960),. . Maternal facilitation of early post-partum sucking appears to be important FPOC. Aust.. Soc. Anim. Prod. Vol. 17 31 for the intake of colostrum and the development of effective blood levels of maternal antibodies by the offspring (Selman et al. 1971; Kim et al. 1983). Many calves of dairy cattle appear slow to suck for the first time because of the large dairy type udder and the positioning of the teats low to the ground (Selman et al. 1970bi Kovalcik et al. 1980; Edwards 198la). Similar problems have been observed with Dorset Horn sheep with pendulous udders and Merino sheep with greatly enlarged 'bottle' teats (Alexander, unpublished; Hayman et al. 1955). On the other hand, calves of some beef breeds such as the Saler show little aptitude for bottle feeding, compared with dairy breeds. The maternal presence is necessary for these beef breeds to survive (Le Neindre et al. 197% Many reports show real species differences in the frequency and duration of suckling bouts (Lent 1974), but these do not appear to be significant survival factors. Ungulate mothers do not normally permit sucking by offspring other than their own, although a high incidence of cross-suckling has been reported in domestic cattle (Edwards 198lbi Lewandrowski and Hurnik 1981) and a lower incidence in groups of sheep with large litters (Hess et al. 1974). Occasional cross suckling has also been reported for white-tailed deer (Faatz 1977). Spatial association of mother and offspring The degree of association between mother andsoffspring during the postpartum period is commonly used to divide ungulate species into two major classes (Lent 1974), described as gghidersgg, with young that lie concealed, and However, types with ggfO1lowersg', with young that remain with the mother. intermediate behaviour patterns such as moose (Stringham 1974) are common and , both types of behaviour have been described for the same species, for example in giraffe (Langmann 1977; Pratt and Anderson 1982). The concept has been modified'several times to accommodate problems in classification (Rails et al. It has been suggested that isolation for bir,th by followers represents a 1986). vestigial hiding phase (Langman 1977): Most species of, ungulate are hiders; the offspring remain concealed near the birth site while the mother feeds, sometimes se.veral kilometers away.' , 'O'Brien (1984) drew attention to individual variability and to, environmental effects on the distance the mother moves from the hidden. offspring; those remaining close 'were termed 'stayersn.~ and thos>e moving : away were termed 'leavers'.. The young cf hider species are. suckled as infrequently as 2-3 times daily, and appearto lack 'the endurance to: travel.. .The~*process of concealment. usually 'appears tb be initiated by the offspring ;.themselves, as seen in a variety of species-:', (Harper 1970) incladin.g;water buck. (Spinage ,1969), red deer (Glutton-Brock and Guinness 1975 ), mule deer:.(Truett,W77), and goats (Lickliter The characteristics of-the. sktes of concealment of'goat *kids 5havebeen 3984) closely examined '(O'Brien 1983.) and. feature putative protection from predators. Thre $ho,ice of shelteredsites by*.red. deer calves'more *than 'a, day arid .weather. .The:hiding; strategy&s not old has also been 'recorded (Ke,lly and .1Drew*j1976`)~o b%n:.hot climates the .screen&, *of vegetation may reduce4 air ' .+ithout hazards. movement without providing shade, and tcalf, ,mortality:under such conditions has been.docu&nted (,&&hand ~exander.~3966).: Zhe: dtzratkon of 'the ,hidingLphase is a characteristic of the..species;.; ,it may persistfor aI .few days :only,. .as in O'Brien 1984; Lickliter b9.84/5b), Lent ,1974; cattle and goats (Rudge 19,70; for a month as in giraffe (Langman 1977) and white-tailed deer (Hirth 1985) or even 2 months as with reedbuck:(Jungius 1970)*~andUganda~ kob :.(Le&hold 1967). Hiding is replaced 'by following behaviour and of-ten by'.aggregation of the young into nurserygroups (Lent l974). l 32 Proc. Aust. Soc. Anim. Prod. Vol. 17 With a minority of ungulate species, the 'followers', the young normally leave the birth site and follow the mother closely within hours of birth while she grazes or travels to water. The follower species inhabit open grassland (Lent 1974) and include the horse (Fraser 1980a), caribou (Miller and Broughton 1973), bontebok (David 1975), bison (McHugh 1958), wildebeest (Estes 1976) and mountain and domestic sheep (Pitzman 1970; Morgan and Arnold 1974). In this class, mother and offspring remain within earshot of each other for days or weeks; suckling is frequent, and initially may occur several times hourly (Lent Travelling in hot weather can, however, lead to mortality of lambs due to heat exhaustion (Smith 1961; Morgan et al. 1972). 1 9 7 4 ) l . Hiding and following are considered by many observers to represent With hiders, concealment and different strategies in predator defence. immobility coupled with placentaphagia and consumption of offsprings' excretions are believed to be the main defences. With followers, predators could be deterred or repelled by the mother, or avoided by flight. In an evolutionary sense hiding may represent a remnant of an ancient it seems reasonable to suggest that followers with their nesting phase; precocious young represent ,an advanced stage in. the evolution of behaviour of ungulate mothers and young. Maternal defence against predators Flight is the common strategy with followers (Harper 1970; Valdez and Alamia 1977) but vigorous defence of the offspring has been reported for a Tyler 1972-3). variety of species (Lent 1974; Berger 1978; Such species include elk, musk ox, moose, zebra, Dal1 sheep, bighorn sheep and horses. However, domestic sheep have been observed to remain undisturbed by the presence a potential predator of sheep (Alexander et al. 1967), and Geist of foxes, (1971) reported that mountain ewes were much less protective than the large Giving birth in the presence of many mountain goats with their lethal horns. other parturient females, as in caribou for example, is also regarded as a predator defence (Bergerud 1974). Care of multiples The few references to maternal behaviour of ungulate females, other than Suidae, producing litters of more than one offspring deal largely with pen Atroshi and 6sterberg 3979; situations (Holmes 1975, 1976; Owens et al. While problems with grooming and suckling of 'litters have been 1980). identified, the problems of maintaining contact with all members of a litter under field conditions are much greater than for 'a single offspring. This is indicated, for example, by the high lamb mortality due to accidental separation of twin lambs from their mothers during the first day of 'life (Stevens et al. Events at birth can lead, to separation at that, time,. or to uneven 1982). grooming of litter mates and hence to uneven maternal bonding of ewes to lambs: Such events include this can lead to. later separation (Kilgour et al. 1983). litter mates being born several metres apart, straying of one of the litter * during the grooming of the other(s), interference by other parturient females, separation due to physical characteristics of the birth site, such as slope and vegetation, different susceptibilities of lambs to 'chilling in inclement weather, and interference.by humans. Ewes of some sheep breeds appear to. leave their lambs more readily than others in response to human interference (Morgan et al. 1974r. Separation frequently occurs when ewes move from the birth site to water Even when all members of a litter appear to have been groomed or graze. normally, many ewes appear satisfied if accompanied by one lamb only, especially if the movement from the birth site occurs within 4 h'of birth (Alexander et al. Proc. Aust. Soc. Anim. Prod. Vol. 17 33 Alexander 1984). 1983; It appears that the strength of bonding, or the ewe's awareness of her litter size depends on the time spent on the birth site The importance of the birth site or 'birth beds' in (Kilgour et al. 1983). bonding of mountain sheep has been stressed by Pitzman (1970). The ability to care for twins appears to vary between breeds, and improves with experience rather than with age (Alexander et al. 1984). Permanent separation beyond the first day after birth is rare. Offspring behaviour Species vary widely in the rate of progress of their young but the newborn of most species suck within an hour of birth. The wildebeest appears to be the species with the most precocious young, which stand within 10 min o,f birth and suck within 20 min (Estes 1976). The young of some other species take several hours to suck for the first time (Lent 1974). The rate of progress within a species such as sheep also varies widely, possibly associated with differing susceptibilities to hypothermia (Slee and Springbett 1986). Estes and Estes (1979) distinguished three stages in the development of young ungulates. A short 'immobile' stage, when the young cannot stand or run, is followed by a 'feeble' stage when they lack the speed and endurance of This is followed by a 'vigorous' stage when the young are as able as adults. adults in avoiding predators. The feeble stage in hiders corresponds with the hiding phase, but probably lasts no more than 2-3 days in followers. Very young offspring of some species such as nyala (Anderson 1980) I contribute to predator defence by adapting a prone immobile posture when disturbed, for example, by handling. Lent (1974) indicated that this response was not limited to hiders but had not been observed in Bovidae, the sheep and However, the prone response is common in young lambs after cattle 'family. handling during the feeble stage (Alexander unpublished). From an early age the offspring also play a significant role in the maintenance of contact between mother and young, as was shown by a study in which crossbred lambs were less frequently separated from their Merino mothers than purebred Merino lambs during the 'first day of life (Stevens et al. 1984 Also, in a recent study (Nowak .et al. 1987) young crossbred lambs were shown to be more efficient in recognizing their dams than were Merino lambs. The role of the mother in maintaining contact with. the offspring may have been overemphasized (Stevens et al. 1982). l Role of the male' The male has a general role in the care of offspring through defence of harems and territories (Lent 1974), in klipspringer, 'for example (Dunbar and Dunbar 1974): but the male is usually repelled by the female if he approaches the offspring (Spencer-Booth 1970). The male is usually exclud