From birth to colostrum: early steps leading to lamb survival

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From birth to colostrum: early steps leading to lambsurvival

Raymond Nowak, Pascal Poindron

To cite this version:Raymond Nowak, Pascal Poindron. From birth to colostrum: early steps leading to lamb survival. Re-production Nutrition Development, EDP Sciences, 2006, 46 (4), pp.431-446. <10.1051/rnd:2006023>.<hal-00900627>

https://hal.archives-ouvertes.fr/hal-00900627

https://hal.archives-ouvertes.fr

Reprod. Nutr. Dev. 46 (2006) 431–446 431c© INRA, EDP Sciences, 2006DOI: 10.1051/rnd:2006023

Review

From birth to colostrum: early steps leading tolamb survival

Raymond N*, Pascal P

Laboratoire de Comportements, Neurobiologie et Adaptation, UMR 6175 CNRS-INRA-UniversitéFrançois Rabelais-Haras Nationaux, Unité de Physiologie de la Reproduction et des Comportements,

INRA, 37380 Nouzilly, France

Abstract – New-born lambs have limited energy reserves and need a rapid access to colostrumto maintain homeothermy and survive. In addition to energy, colostrum provides immunoglobulinswhich ensure passive systemic immunity. Therefore, getting early access to the udder is essential forthe neonate. The results from the literature reviewed here highlight the importance of the birth siteas the location where the mutual bonding between the mother and her young takes place. Attractionto birth fluids by the periparturient ewe leads to intense licking of the lamb. Grooming not onlydries, cleans and stimulates the newborn it also facilitates bonding through learning of its individualodour. Ewes having twins should ideally stay on the birth site for at least six hours in order toestablish a strong bond with both lambs and favour lambs survival. However, primiparous ewes orewes having high levels of emotivity are more likely to exhibit poor maternal behaviour. In addition,difficult parturition and weather conditions have an indirect effect on the behaviour of the motherand are other major causes of lamb death. On the lamb’s side, rapid access to the udder and earlysuckling are extremely important. Delayed lactation or insufficient colostrum yield may be fatalespecially since suckling has strong rewarding properties in the establishment of a preference forthe mother, which in turn increases lamb survival. Insufficient access to the udder in mothers leavingthe birth site too soon after parturition, especially in twin-bearing ewes, could also partly account forthe high incidence of loss of mother-young contact and subsequent death in such lambs. Strategiesto improve neonatal survival should be aimed at maximising lamb vigour, colostrum production,and mutual mother-young bonding through adequate feeding in late pregnancy and selection onbehaviour.

energy reserve / colostrums / suckling /maternal behaviour / bonding / ewe / lamb / nutrition /survival

1. INTRODUCTION

The successful transition of the neonatefrom the warm protective uterine wombto the external environment is a real chal-lenge [1] and the behaviour of the lambafter birth, in combination with that of themother, will deeply influence its chances ofsurvival [2]. Neonates need to be vigorousin order to rapidly seek the udder, locate

* Corresponding author:[email protected]

the teat and suckle and to do so they musthave well-adapted behaviour patterns im-mediately after birth. Early mother-younginteractions are also crucial to ensure thata strong bond is established between theewe and her neonate so that food is reg-ularly supplied to the lamb. The primaryfunctions of early maternal care are there-fore to provide the lamb with colostrum tosatisfy its metabolic needs and to protectit from aggression from the outside en-vironment. The mother-young interactions

Article published by EDP Sciences and available at http://www.edpsciences.org/rnd or http://dx.doi.org/10.1051/rnd:2006023

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http://dx.doi.org/10.1051/rnd:2006023

432 R. Nowak, P. Poindron

that lead to successful suckling by newbornlambs are the results of complex physi-ological, morphological, and behaviouralchanges that ensure extra-uterine survivalat a time when the young is entirely depen-dent upon its mother for the provision offood. Yet many lambs do not adapt to thishuge change in their life style.

Neonatal mortality, in both intensiveand extensive systems, remains a strongconcern for sheep production. Mortality of15–25% is common in farming systemsworld-wide. Most preweaning lamb deathsoccur within the first week of life [2–4],emphasising the importance of the imme-diate post-partum period for lamb survival.The survival of the neonate depends onthe complex interactions between rearingability of the mother, lamb’s viability, andclimatic conditions around lambing [3–6].In extensive systems, the majority of lambdeaths are attributed to two main causes:dystocia from prolonged or difficult birth,and the starvation-mismothering-exposurecomplex. Lamb deaths attributed to thestarvation-mismothering-exposure com-plex have contributing factors such asadverse weather conditions, inadequateenergy reserves, thermoregulatory prob-lems, delayed lactogenesis, insufficientcolostrum yield, aberrant maternal or lambbehaviour, competition with siblings orudder defects. This review will focus onthe physiological and the behaviouralfactors at play during the first hours ofmother-young interactions that take placeon or near the birth site. The birth site is anarea of a few square metres where the ewestays to give birth and provide maternalcare, and where the newborn has to findthe udder to ingest vital colostrum. Therethe ewe must spend several hours with herlamb(s) so that the intimate mother-younginteractions help develop strong mutualbonding. Independently of climatic andother environmental conditions, thereare three main types of factors that mayinfluence lamb survival at this time: the

state of physiological adaptation of thelamb and the ewe at the time of parturition,the quality of the care the mother willdispense to the neonate and the behaviourof the neonate itself.

2. NEONATAL AND MATERNALPHYSIOLOGICAL ADAPTATION:GETTING SET FOR THE QUESTFOR COLOSTRUM

2.1. Energy reserves of the neonate andenvironmental conditions

The first few hours after birth are criticalfor the survival of the newborn lamb sinceit must counteract the massive heat loss in-curred from its transition from the warmuterine environment to the external world.During the first 15 min after birth, the inter-nal temperature of a lamb decreases by 1 to2 ◦C below the intra-uterine environmentof 39 ◦C. Lambs must increase their heatproduction by up to 15 times the prenatallevel to compensate for this heat loss [7].The cooler the external environment, thefaster this metabolism must be to main-tain homeothermy and the rate of heat lossis heightened by wind velocity, humidityand the amniotic fluids evaporating fromthe birth coat. To maintain homeothermybefore any colostrum is ingested, the new-born must metabolise its brown fat energyreserves and increase muscular activity byshivering [8,9]. Brown fat provides the ma-jor source of energy but constitutes only2–4.5% of the body weight of the lamb.Large neonates have more available lipidper kilogram of body weight than smallones. Fat reserves are disproportionatelylow in small lambs and in lambs being bornfrom ewes that had been undernourishedduring pregnancy [10], hence giving themeven less chance to survive.

The amount of energy reserves is there-fore the first critical condition for survival,

Behaviour, nutrition and lamb survival 433

especially when weather conditions are un-favourable. If energy reserves directly in-fluence the length of time the lamb can sur-vive without any colostrum intake, it is theavailable carbohydrate, not fat, that is themain factor limiting the length of time thata newborn can resist inclement weather.The high mortality rate observed duringor shortly after periods of bad weather arelargely the results of hypoglycaemia whichin turn produces hypothermia and death,before total depletion of the fat body re-serves [4]. The combination of wind andrain, as well as low temperatures, are welldocumented predisposing conditions thatcause lamb mortality [11–14]. Wind speedalone has also been highlighted as a veryimportant factor increasing heat loss andlamb mortality [15]. Heat loss dependsmainly on surface area while heat produc-tion is linked to body weight [9]. Hencesmall lambs are more predisposed to ex-posure and hypothermia than large lambs,because the former have a higher surfacearea to volume ratio and higher rate of heatloss per unit of body weight [16].

2.2. Colostrum

Colostrum is produced just before par-turition and contains dense nutrients aswell as high levels of immunoglobulin, en-zymes, hormones, growth factors and neu-roendocrine peptides. Because colostrumis the unique source of food for theneonate, insufficient intake is the secondmajor factor (after body reserve) that af-fects neonatal survival. Colostrum con-tains approximately 7% fat, 4% casein,5% lactose and 82% water [17, 18] andprovides approximately 2 Kcal of energyper mL [19, 20]. It is estimated that 180–290 mL.kg−1 body weight are required bythe lamb in the first 18 h after birth [1]but not all mothers can fully cover their in-fant’s need.

The amount of colostrum accumulatedin the udder before parturition and the pro-duction of milk afterwards depends on thesize of the litter. Twin-bearing ewes gen-erally yield more colostrum than single-bearing ewes, but the onset of lactation isslower in the former and they do not pro-duce as much colostrum per lamb [21–23].This has serious implications for twinssince they are often already disadvantagedby lower birth weights and lower energyreserves than singles. Therefore, inade-quate supplies of colostrum diminish evenmore their chance of survival. In the studyby McNeill et al. [22], 30% twin-bearingewes were estimated to have insufficientcolostrum available for their lambs afterbirth. In addition, about 10% of the single-bearing ewes also produced insufficientcolostrum for their lamb. Good nutrition ofthe ewe is essential to ensure that an ad-equate supply of colostrum is available tothe lamb and that subsequent milk produc-tion rates are sufficient to cover the needsof the growing lamb [24–26].

A further function of colostrum is totransfer antibodies from the mother to theyoung before its own immunological pro-tection becomes fully functional [17]. Forspecies having an epitheliochorial placen-tal, such as sheep, the process of trans-fer of immunoglobulins from the mother’scolostrum is of paramount importance toneonatal survival, since the immunoglob-ulins do not cross the placental barrier.Once suckling is achieved, the serumimmunoglobulins rise rapidly during thefirst hour and peak about 24 h afterbirth [20]. Immunoglobulin levels in theblood are directly related to the pro-duction of colostrum, since larger vol-umes of colostrum are associated withlarger amounts of immunoglobulins [27,28]. This process of passive immunoglob-ulin absorption in the intestine ceases atabout 24 h of age and is referred to asintestinal closure. Therefore any delay insuckling by the lamb, due to low colostrum


yield or to poor teat-seeking activity, re-duces its chances of obtaining sufficientimmunoglobulins to be protected from in-fection by pathogens [29].

2.3. Birth weight, litter size,and suckling drive

Most deaths of lambs are invariablyconcentrated in the first days after birth [3,30] and are typically associated withbirth weight by a curvilinear relationship.Lambs with either very high or very lowbirth weight are more at risk than lambshaving intermediate birth weights and theoptimum birth weight ranges between 3and 5.5 kg [4, 9]. Mortality rate in twinsis generally 1.5–3.0 times that of singles.Birth difficulties and dystocia are the maincauses of death of large, single-born lambs.By contrast, lambs with low birth weightare predisposed to death from starvationand exposure, due to their lower energyreserves, weakness, immaturity and an ab-normally high birth coat/birth weight ratio.

Mortality rates in singles and twins inthe same birth range are usually simi-lar [31]. However, in Merino sheep, mor-tality of twins can be above that of sin-gles of the same weight, suggesting thatfactors other than birth weight may beinvolved [32]. Deficient maternal care inMerino ewes, especially those bearingmultiples, is mainly attributed to their poorability to maintain contact with both oftheir twin lambs [33]. Disparity in thevigour of twin lambs may also be a causeof lamb deaths from desertion by Merinoewes, since weak vigour may lead to un-even bonding and the death of one, orboth lambs. Over 40% of twin lambs thatwere abandoned and perished in the studyby Steven et al. [32] were the weakest ofthe pair. Inadequate teat-seeking activityin weak lambs is also likely to exacer-bate this phenomenon, since rapid rewardof initial suckling is an important factor

to sustain suckling drive in young lambs.Small lambs often have a lower sucklingdrive than lambs of heavier weight and thisis a combined effect of low birth weight,low energy reserve and general lamb weak-ness. Neonates that take longer to standup and to suckle have reduced chance ofsurvival since the suckling drive and thechances of ever suckling successfully arereduced considerably if they have not in-gested any colostrum in the first six hoursof birth [34–36].

3. BEING BORN TO A CARINGMOTHER

3.1. Seeking isolation and selectinga birth site

The early development and survival ofthe newborn lamb depend entirely on thecare provided by its mother. In sheep,which are gregarious, this begins witha tendency of ewes to separate them-selves from the flock as parturition ap-proaches. Even under intensive manage-ment, prelambing ewes choose to isolatethemselves if they are given the opportu-nity by providing cubicles in the shed [37,38]. Under extensive conditions, however,it is not always clear whether parturientewes actively seek isolation [39] or areleft behind by the flock [40]. Nonethe-less in all instances, there is a reductionof gregariousness of ewes around lambingwhich is not due to the bonding processwith the neonate, since it already existsprior to lambing [41]. This shift in so-cial motivation optimises the establishmentof satisfactory mother-offspring relation-ships, while minimising the risk of inter-ference by other pre-parturient ewes. In-deed, disturbances in the establishment ofthe mother-young relationship are commonamong ewes lambing in the presence ofother parturient females [33, 42]. Twentypercent of pre-parturient Merino ewes may


be attracted to lambs of other ewes and in-terest ranges from brief inspection, groom-ing, suckling and even stealing of the new-born [43]. Unfortunately, the alien is oftenabandoned when the ewe delivers her ownlamb.

Seeking shelter may contribute fur-ther to isolation from the flock. How-ever domestic preparturient ewes usuallyonly seek shelter in cold, windy and wetweather. Again, this appears to vary ac-cording to the breed [44]. In general, adultMerino sheep with a full fleece make lit-tle use of shelter unless wind speed is over40 km.h−1, however, prelambing shearingmay increase sheltering [45]. In contrastLacaune ewes, which do not have a thickfleece, choose to give birth in shrubby siteswhen the wind speed is over 10 km.h−1,even if there is no rain [39]. Shelter is notthe only parameter females may use to se-lect a birth site, even though the clues thatewes rely on are not necessarily obvious.Some studies indicate that the distributionof birth sites is not random, and Merinoewes seem to prefer the high end of thepaddock as lambing areas [44]. In most in-stances, the exact site of birth is determinedby the place where the foetal fluids are firstspilled [43].

3.2. Grooming the lamb

Grooming of the lamb by the ewe dur-ing the first postpartum hours depends onthe attraction for the foetal fluids. Maternallicking not only dries, cleans and stimu-lates the lamb, it also entrains additionalmaternal care and facilitates the forma-tion of a strong bond with the newbornlamb through recognition of its odour [46].It may be delayed in primiparous ewesor those that have experienced difficultbirths [43,46,47]. With multiple births, theewe seems to lose interest in the first-bornlamb when the second lamb is born. De-spite this shift of attention, second-born

lambs do not receive as much groomingas first-born twins [48–50]. Because ewestake longer to lick multiple-born lambsdry, these are predisposed to hypother-mia in adverse conditions. While groom-ing, the dam emits frequent low-pitchedbleats or rumbling noises with the mouthclosed, and occasional high-pitched open-mouth bleats [51, 52]. Low-pitched mater-nal bleats are emitted almost exclusively inthe presence of the lamb and like licking,decline over time. These are thought to qui-eten the newborn and to provide cues forlater recognition of the dam. In contrast,the rate of high-pitched bleats increaseswith time and they are used for distal com-munication

3.3. Getting bonded to the whole litter

Ewes remain attracted to the birth sitefor several hours after parturition and thisis generally where the mother-young re-lationship is formed. Under optimal con-ditions, ewes rapidly develop a selectivebond with their newborn lamb(s). Theprimary developmental mechanism impli-cated in the establishment of the mother-young bond is a rapid learning of thelamb’s distinctive phenotypic “olfactorysignature” [53, 54]. Immediately after par-turition ewes respond maternally to alienyoung as well as their own. Recent stud-ies have demonstrated that 30–60 minof immediate post-partum contact with aneonate may be sufficient for the ewe tobecome familiar with that lamb’s uniquesignature and discriminate her lamb fromalien ones [55]. Once established, this ma-ternal bond is characterised by the exclu-sive nursing of the ewe’s own lamb, alongwith the rejection of all alien young thatapproach her udder.

The first hours postpartum thereforerepresent a critical time for the establish-ment of the maternal bond towards heryoung (reviewed in [56]). Under extensive


conditions, abnormal behaviour or exter-nal disturbances at this stage can lead toseparation and death of young, especiallyin ewes giving birth to twins. In Merinos,the incidence of permanent separations ofewes and lambs range from 25 to 50% [32,33] and a further 30% of twin-bearing ewesmay become temporarily separated fromone of their twins in the first few days af-ter parturition. The ewes separated frompart of their litter appear satisfied that onelamb only is following. By contrast, cross-bred Border Leicester ewes separate fromtheir twin lamb less frequently than pure-bred Merino [13]. However, the role of thelamb’s behaviour in these separations fromthe mother is probably of some importanceeven though it is not fully understood [57,58]. Proper establishment of a bond de-pends on the time spent on the birth siteor nearby. Poorly bonded mother-youngunits that leave the birth site too soon afterparturition have higher incidence of sep-arations and higher mortality [24, 33, 59].Ideally, ewes should remain on their birthsite for at least six hours after parturitionwith the whole litter in order to attachstrongly to all the lambs and optimise theirchance of survival. However, this is rarelythe case for Merino ewes. Most ewes leavethe birth site rapidly to find food and wa-ter and their move can be hastened bydisturbances caused by humans, dogs ornervousness [60]. Hunger caused by sparsepasture cover and poor ewe conditions atparturition can motivate them to leave thebirth site [61] and increase the probabilityof interference from other parturient ewes.In addition, the inherent temperament ofthe Merino and their strong gregariousnessmay cause them to move away from thebirth site too soon after parturition, wellbefore strong ewe-lamb attachments havebeen fully formed.

Even when the various elements andcues that normally contribute to the on-set of maternal behaviour are optimal,primiparous ewes are often less competent

than experienced ewes, and the mortal-ity of their lambs is higher. Primiparousewes tend to have longer labour than mul-tiparous ewes and are slower to begingrooming their lambs [50]. They are alsomore likely to show fearful behaviour to-wards the lamb, they may be more ag-gressive and in some cases they may failto show maternal behaviour and abandontheir lamb. In inexperienced mothers, thenewborn may be seen as a novel and po-tentially fearful stimulus leading to initialdisturbances in up to 50% of mothers insome instances [54], with more than 20%of primiparous ewes still failing to nursetheir young after three hours. However,after mothers have gained maternal expe-rience at their first lambing, they showimproved maternal care in their subsequentpregnancies [62].

4. SUCKLING AND GETTINGATTACHED TO THE MOTHER

4.1. Finding the teat

Because lambs are born with little en-ergy reserves, it is vital that they findthe teat and ingest colostrum as soon aspossible. The expulsion process results inan intense physiological and behaviouralstimulation of the neonate [63]. This sus-tained arousal promotes exploration of themother’s body and perception of sensorycues which will guide the neonate towardsthe udder. They find the udder by ex-ploring the underneath of the ewe’s bodyfrom the chest to the udder. In particularthey spend time nosing the axillary and in-guinal areas of the udder until the teat isfound. Thermotactile cues play a crucialrole in the search for the teat since lambsmake munching movement once they comeinto contact with the mother’s body [64].Lambs also respond to the smell of am-niotic fluids and inguinal wax with headmovements, oral activity, exploration, and


increased breathing and heart rates [65,66].Most lambs begin to suckle within the firsttwo hours of delivery, however, significantdifferences between breeds in the early be-haviour of lambs have been reported [51,67–69]. Birth weight, gender and litter sizemay also influence the time lambs take tostand and find the teat. Male lambs are usu-ally slower than females in the expressionof early behaviour and twins slower thansingletons, although some authors suggestthat this twin effect is a function of reducedbirth weight.

4.2. Getting attached to the mother

Ewes move away from their birthsite within hours after parturition. Sinceneonates need to suckle hourly, followingthe mother is their best survival strategy inorder to keep in the vicinity of the sourceof colostrum. In addition, once the motherand her litter have joined the flock of ewesmany of which are lactating, the motherwill remain the only source of food, dueto the existence of exclusive nursing. It istherefore highly beneficial to the lamb toget rapidly attached to its dam. Most lambscan discriminate between their mother andan alien maternal ewe 12 to 24 h afterbirth [70, 71] and this ability still improvesmarkedly during the first few days postpar-tum [72]. While recognition of the motherat 24 h is based primarily on cues thatlambs can perceive at close quarters, theycan clearly discriminate their mother froma distance of several metres when 3 daysold [73]. The development of early recog-nition of the dam varies according to breed,sex, and litter size [71, 72]. Twins com-monly take more than two days beforethey begin to show a preference for theirdam. Even then, behavioural differencesstill persist between singles and twins [73].

The development of a preference for themother by 24-h old lambs depends mainlyon their first successful suckling bouts.

When suckling is prevented during the firstfew hours after birth, the lambs’ discrim-inative ability is impaired by 24 to 48 h,an effect that cannot be attributed to over-all reduction of colostrum intake [74, 75].The longer neonatal suckling is prevented,the longer the preference for the mothertakes to develop [76]. These effects areunique to the neonatal period since theyare not observed when suckling is tem-porarily prevented later in life. That is,preventing a three-day-old lamb from ac-cessing the udder for a few hours does notaffect the preferential relationship that hadalready been established between the damand offspring as measured 24 h later [74].In a related study Napolitano et al. [77]have shown that lambs that are permitted tosuckle only during the first day after birthand then remain with their dam without be-ing allowed to suckle, still display a strongpreference for her at one month of age.

Ingestion of colostrum plays a key rolein this rewarding process [75, 78, 79].Both ovine or bovine colostrum, collectedwithin hours after parturition, were as ef-ficient, while ewe milk obtained at threeweeks of lactation was less effective [79].Non nutritive liquids ingested in equiva-lent small amounts (2.5% to 5% birth bodyweight) did not facilitate the establish-ment of a preference for the mother [75,79]. Even an isocaloric solution of lac-tose, the main sugar found in colostrum,was not followed by any specific be-havioural output, suggesting that energyintake per se is not the primary factorcontrolling the development of this earlyfilial bonding. However, when lambs in-gested larger amounts of fluids (up to 10%birth body weight), the development of apreference for the mother was facilitatedboth by colostrum and non nutritive fluids.Therefore, beyond a threshold, the volumeof ingesta can also facilitate early filialbonding independently from any caloricor nutritional input [75]. Thus, ingestingcolostrum is not just a way of getting


nutrients and energy supply for the lamb.Through the cascade of neurophysiologicalevents that are triggered during suckling,colostrum ingestion also shapes the be-haviour of the neonate with biochemicaland visceral mechanical stimulation. Re-cent studies have also demonstrated thatnon nutritive sucking facilitated early filialbonding [80].

5. STRATEGIES TO IMPROVENEONATAL SURVIVAL

The interactions taking place betweenthe ewe and her litter during the firstpostpartum hours are vital for the estab-lishment of mutual bonding. This in turnrepresents an excellent “life insurance” forthe lamb and a primary key of the re-productive success of the ewe. While thismutual bonding usually develops withoutdifficulties, there are still possibilities toimprove it (e.g. primiparous or nervousmothers, twin-bearing ewes), and hence in-crease lamb survival.

5.1. Acting on the mother

5.1.1. Management at parturition

Various aspects of ewe behaviour maycontribute directly or indirectly to the inci-dence of lamb mortality. Good shelter- andisolation-seeking behaviour by the prepar-turitent ewe can increase lamb survival.In studies with Merino ewes, provisionof shelter reduced lamb mortality in poorweather by up to 50% [13, 14, 81]. Even inintensive systems, parturient ewes offeredaccess to cubicles in lambing sheds showeda marked preference to lamb in the cubiclesrather than in open pens [38]. This resultedin a reduction of ewe-lamb separation andlamb stealing by preparturient ewes, com-pared to control pens without cubicles [37].

Time spent at the birth site has also beenshown to correlate with lamb survival in

Merino ewes [32, 33, 59, 82]. Characteris-tics of the birth site per se appear to be lessimportant than the ewe remaining undis-turbed with her lambs for at least 6 h [24].Thus, isolation from the flock at parturi-tion facilitates formation of the ewe-lambbond without interference from other ewes,and appears to be an important ewe traitfor the survival of the lamb. Managementpractices where ewes and lambs are movedtoo early from the birth site may disruptthe normal transfer of maternal attentionfrom the birth site to the lamb and hin-der the formation of the ewe-lamb bond.This is likely to be particularly detrimen-tal to primiparous mothers or nervous ewesin general which are more easily disturbedby external disturbances than experiencedand calm ewes (primipara: [54], nervousmothers: [83]). Fear, stress or disturbanceis known to cause involuntary suppressionof uterine contractions in mammals duringlabour. For ewes unaccustomed to humanpresence, close supervision may act as asource of stress and unnecessarily delay orprolong parturition. Thus a low stress en-vironment for lambing ewes is likely to beassociated with better welfare for the ewe,and improved lamb survival.

5.1.2. Nutrition during pregnancy

Ewes that are under-fed during preg-nancy give birth to low birth weight lambswith heightened mortality rates. Additionaladverse effects of maternal undernutritioninclude reduced udder development as wellas colostrum production and quality (seeBanchero et al., pp. 447–461). Nutritionalsupplementation during mid or late preg-nancy can be used to reduce lamb mor-tality by increasing the birth weight ofthe lamb [84, 85], increasing colostrumand milk production [26, 86, 87]. Indeed,ewes that are underfed during pregnancyhave differing physiological profiles dur-ing gestation compared to well-fed ewes.


Low nutrition is associated with higherplasma progesterone in late gestation [88],and a lower ratio of oestradiol to proges-terone at birth [89]. High plasma proges-terone is negatively related to colostrumand milk yield and therefore may threatenthe survival of newborn lambs. In addition,progesterone and oestradiol are involvedin the onset of maternal behaviour, andhigh ratios of oestradiol to progesteroneare correlated with maternal grooming be-haviour [90]. Therefore nutrition of theewe during gestation and at parturition canalso influence her maternal behaviour. Ele-vated progesterone in underfed ewes mightcontribute to poor maternal behaviour.Under-fed ewes actually take longer to in-teract with their lambs [91], display moreaggression, spend less time grooming andmore time eating after birth [89], and aremore likely to desert their lambs [61].

5.1.3. Individual differences and breeddifferences

Ewes may differ in the maternal carethey express, e.g. the amount of groom-ing behaviour, responses to the lamb’ssuckling attempts, likelihood of desertion.These differences usually persist over suc-cessive births [62] suggesting that theyare intrinsic to the individual. One of themost frequently explored sources of ma-ternal behaviour variation is breed dif-ferences. Many breeds have been com-pared, and different behavioural measuresrecorded. The chosen breeds generally re-flect the prevalent or commercially impor-tant races in the countries where they havebeen studied: for example, behaviouralcomparisons between the Merino, Peren-dale, Romney, Border Leicester, Cheviot,Dorset Horn and crossbreds in Australiaand New Zealand [92], between Romanov,Lacaune, Préalpes du Sud, and Île-de-France in France [47, 93] and betweenDalesbred, Scottish Blackface, Suffolk and

Soay breeds in the UK [62]. Because thesestudies used a variety of behavioural mea-sures that differed between studies, it ishard to draw any clear conclusions, exceptwhen comparing breeds within the samestudy.

Nonetheless, observations in Australiaand New Zealand suggest that Merinosare generally poorer mothers than otherbreeds: as mentioned above they spendless time on the birth site, and have amuch higher incidence of both permanentand temporary desertions of their lambsthan other breeds [94]. When ewes’ re-sponses to handling of their lamb werescored, Merino ewes also rated lower thanother breeds [92]. In French and Britishbreeds, Romanov and Scottish Blackfaceewes are considered to show better ma-ternal care (more licking, grooming andlamb acceptance; less aggression) than theother breeds [47, 93]. Thus it is clear thatconsiderable breed differences exist in thequality of expressed maternal behaviour. Ingeneral, hill, upland and harsher breeds,which have been subjected to less humanintervention, show better quality of mater-nal care, whereas more intensively selectedand reared animals display greater variabil-ity in maternal behaviour and make thepoorest mothers.

5.1.4. Selecting for better mothers

Attempts to select for better mothershave been carried out following variouscriteria. For example, in flocks selectedto improve lamb survival to weaning, themain outcome of the selection process isan increase in the speed and ease of partu-rition [95], swift parturition clearly emerg-ing as an important parameter for lambsurvival. As a matter of fact, prolongedlabour can increase the possibility of braintrauma and hypoxia in the neonate [96]and therefore impair suckling, locomotoractivity and thermoregulation [20, 97, 98].


Similar responses are seen in ‘easy-care’Romney ewes [99].

Maternal behaviour has also been as-sessed using a composite measure of ewes’reactions when their lambs are handledby a shepherd [100]. This score showsvariation within and between breeds [92,100] and is related to both lamb survivaland weaning weight. Heritability estimatesof this measure for Scottish Blackfaceewes [101] are relatively low but there wasgood reliability.

The consistency displayed by individu-als may reflect their underlying emotivityor “temperament”, which may or may notinfluence maternal behaviour per se. Ro-manov ewes, for example, are consideredto be better mothers (in terms of licking,grooming and attachment to the lamb) incomparison to the Lacaune breed [93]. Yet,Romanov ewes display greater flight fromhumans and stand further from their han-dled lambs than Lacaunes, a behaviour thatwould have earned them a lower maternalbehaviour score in the studies by Whateleyet al. [92] and O’Connor et al. [100].These responses are believed to result fromgreater emotivity of the Romanov breedrather than a poorer quality of maternalcare. In contrast, in studies where Merinoewes were selected for temperament bymeasuring their responses to a variety oftests, the ‘calm’ ewes spent more timegrooming their lambs than did ‘nervous’ewes, and bleated more frequently to theirlambs [83]. Lamb mortality in these lineswas also lower in the ‘calm’ ewes com-pared to the ‘nervous’ animals. Ewes pre-viously selected for their ability to rearlambs also show behavioural differencesin an approach avoidance test, indicativeof increased ‘calmness’ [102]. Thus, tem-perament may also contribute to individualdifferences in the quality of maternal careexpressed by ewes.

Within-breed studies indicate that ewematernal behaviour may be affected bygenotype even when that characteristic

had not been included in the selectioncriteria [103–105]. For example, Merinoewes selected for superfine wool wereless maternally responsive and had higherlamb mortality than broader wool Meri-nos [103]. Blackface ewes selected for lowcarcass fat were quicker to groom theirnewborn and stayed closer to it immedi-ately after delivery than ewes selected formore carcass fat [104]. In other studieswhere improved maternal ability was theaim, lamb survival was greater for Merinoewes selected for fertility and success inrearing multiple offspring, than for uns-elected or divergently selected lines [95,106]. This selection criterion decreased de-sertion of lambs, although the main effectappeared to be an improvement in partu-rition, such as ease and speed of delivery.The ‘easy-care’ Romney sheep producedin New Zealand show a similar abilityto give birth unaided [107]. These datasuggest that some aspects of maternal be-haviour are under genetic control, althoughfew estimates of genetic parameters (her-itability, phenotypic and genetic correla-tions) exist. Similarly, in studies whereMerino ewes were selected for tempera-ment, the ‘calm’ ewes spent longer timegrooming their lambs than did ‘nervous’ewes, and bleated more frequently to theirlambs [83]; mortality was also lower in theline of ‘calm’ ewes than in the line of ‘ner-vous’ animals. Potentially, therefore, it ispossible to improve maternal care throughgenetic means.

5.2. Acting on lamb behaviour

5.2.1. Strategic feeding for the lamb

Lamb survival relies largely on early ac-cess to colostrum and the formation of fil-ial bonding. Therefore optimal colostrumavailability and vigour of the lamb mustbe achieved. This is particularly true whenpractices are designed to increase produc-tivity through an increase in lambs born per


ewe which in turn are likely to carry a costin terms of lamb deaths (e.g. reduced birthweight, mother-young separation). Foodsupplementation during late pregnancy intwin-bearing ewes is certainly to be re-garded as a priority. In addition to itspositive impact on the mother [61] foodsupplementation is likely to directly im-prove the survival of the neonate throughincreased weight [84, 85, 108], increasedcolostrum and milk yield [86, 87, 109] andincreased growth rate of lambs [110]. Ahigher production of colostrum may alsoimprove lamb survival indirectly by facil-itating early filial bonding and improvingfollowing behaviour when the ewe movesaway from the birth site.

5.2.2. Breed differences and selection

The strain and breed differences ofearly behaviour and bonding ability oflambs [71, 95, 103, 104, 111, 112] suggesta breeding route to improve lamb sur-vival. In Merino sheep divergently selectedfor multiple rearing ability, the high linelambs were quicker to progress from stand-ing to sucking than the low line [95], andhad improved survival. In additional stud-ies on selection for other characteristics,e.g. lean tissue content had an unexpectedpositive effect in improving lamb activ-ity at birth [104]. Since vocal activity oflambs correlates with their ability to bondto their dam [113], it may be worthy totake this parameter or related ones in selec-tion plans. Recently, it has been found instudies where Merino ewes were selectedfor temperament, that when isolated fromtheir mother the distress-like behaviourexpressed by ‘nervous’ lambs was exac-erbated compared to ‘calm’ lambs [114].The meaning of this behavioural differ-ence is unclear but it suggests that thereare genetic influences on neonatal lamb be-haviour, which appear to be independent ofbreed effects on other traits that influence

behaviour. In addition, the strong effect ofthe sire on lamb behaviour suggests thatbreeding sires for improved lamb vigour isfeasible. Thus appropriate selection of sirebreeds or individual rams is also likely toimprove lamb survival. This may be par-ticularly effective if applied to vulnerablegroups, such as first parity ewes, wherebreeding management for vigorous lambsis likely to have the most significant wel-fare benefits.

6. CONCLUSION

The farming strategies that will help theneonate to adapt successfully post-natallymust start long before the lamb is born.Choice of breed or strain of sheep bestadapted to rearing condition (e.g. “calm”sheep, easy care type of ewe for extensiveconditions), but also specific managementaimed at satisfying the need of multiple-bearing ewes are the first steps to consider,since they all have some influence at partu-rition on the behaviour of both the ewe andthe lamb. The second and potentially veryimportant step is that of strategic feeding ofpregnant ewes. Short term feeding in latepregnancy will ensure that maternal andlamb physiology will be optimally tuned tomeet the challenge of the drastic environ-mental changes caused by birth. Finally,ensuring that mother and twins maintainclose contact for at least six hours after par-turition is a further factor of lamb survival.

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From birth to colostrum: early steps leading to lamb survival