Anim. Res. 55 (2006) 489–510 489c© INRA, EDP Sciences, 2006DOI: 10.1051/animres:2006040

Original article

Adaptive abilities of the females and sustainabilityof ruminant livestock systems. A review

Fabienne Ba*, François Bb, Jacques Ac,Pascal D’d, Yves Cc

a Unité Élevage et Productions des Ruminants, ENITA Clermont, BP 35, Site de Marmilhat, 63370Lempdes, France

b Agro-M, UMR Élevage des Ruminants en Régions Chaudes, 2 place Viala, 34060 MontpellierCedex 1, France

c INRA-PHASE, Unité de Recherches sur les Herbivores, Theix, 63122 St-Genès-Champanelle, Franced INRA, UE des Monts Dore, Le Roc, 63210 Orcival, France

(Received 12 May 2006 – Accepted 26 September 2006)

Abstract – In a systemic approach, the breeder can be considered as the decisional component ofthe livestock system, whereas animals are usually depicted to be part of its biotechnical compo-nent. The animal itself is a biological system whose ability to survive, grow, reproduce and copewith the environnement and livestock practices play a major role in the ability of the livestock sys-tem to sustain. In such a conceptual representation of the system, the reproductive females drawa peculiar attention since they determine in a great part the productivity and the durability of thesystem through their abilities to maintain their own production level (milk production, numericproductivity) and to save their reproductive efficiency (repeated pregnancies and lactations) overyears. Considering the animal level and its lifespan, it is clear that the abilities to adapt rely on be-havioural and physiological regulatory processes. The study of the biological mechanisms involvedin the adaptation to undernutrition is particularly interesting since regulatory processes implied inenergy metabolism may interfere directly or indirectly with the reproductive function, and conse-quently, with the durability of the livestock system. A biological significance of such relationshipsbetween nutrition and reproduction is given that they allow the female to be informed about theassociated risk of entering a productive process facing the uncertainty of the nutritional context.Although the general mechanisms implied in the ability to adapt to the underfeeding constraint areconserved among ruminants, the thresholds (or priorities) may largely differ according to the breedwithin the same species. Hence, in order to evaluate the ability of the ruminant livestock systemsto perpetuate in hard environments (maintaining their production levels) or to assess sustainableobjectives (opening bushy landscapes by increasing grazing pressure), animals’ inherent adaptivepotentialities have to be well known.

adaptability / nutrition / reproduction / perennity / livestock systems sustainability

* Corresponding author: blanc@enitac.fr

Article published by EDP Sciences and available at http://www.edpsciences.org/animres or http://dx.doi.org/10.1051/animres:2006040

490 F. Blanc et al.

Résumé – Capacités adaptatives des femelles et durabilité des systèmes d’élevage. Synthèsebibliographique. Dans une représentation systémique du système d’élevage, l’éleveur incarne lacomposante décisionnelle du système, tandis que l’animal constitue, avec la ressource, sa compo-sante biotechnique. L’animal lui-même peut être considéré comme un système biologique soumisà un environnement contraignant, dont les aptitudes à survivre, croître, se reproduire et s’adapterjouent un rôle fondamental dans la pérennité du système d’élevage. Les femelles reproductricestiennent une place particulière dans cette représentation car non seulement elles déterminent unelarge part de la productivité du système par leur propre niveau de production (production laitière,productivité numérique), mais elles en assurent également sa reproductibilité au cours du temps (in-vestissement reproductif). A l’échelle de l’individu et de sa durée de vie, les modalités d’adaptationreposent sur des processus de régulations comportementales et physiologiques. De tels processusont été particulièrement mis en avant par les études portant sur l’aptitude des femelles de rumi-nants à s’adapter à la contrainte nutritionnelle (comportement alimentaire au pâturage et aptitudeà constituer et mobiliser les réserves adipeuses). L’adaptation à la sous-nutrition revêt un intérêtparticulier pour la pérennité des systèmes d’élevage en milieux difficiles dans la mesure où les pro-cessus de régulation du métabolisme énergétique interviennent sur la fonction de reproduction etsont par ailleurs susceptibles d’informer la femelle, à des moments-clés de son cycle de produc-tion, du risque associé à l’enclenchement d’une nouvelle gestation. Si les mécanismes digestifs,métaboliques et hormonaux impliqués dans l’adaptation à la sous-nutrition sont identiques chez lesruminants, les seuils de réponse varient selon le génotype (espèce, race), révélant ainsi des diffé-rences de potentiel adaptatif. Par ailleurs, si certains échecs biotechniques peuvent être imputés àune moindre efficacité de la réponse adaptative, d’autres peuvent en revanche se révéler cohérentsdu point de vue du fonctionnement biologique de l’organisme et de la gestion de priorités telles quela survie de l’individu ou l’investissement maternel. Ainsi, lorsqu’il s’agit d’évaluer l’aptitude dessystèmes d’élevage à être pérennes il convient en particulier d’avoir une bonne connaissance despotentiels adaptatifs des animaux.

capacités adaptatives / nutrition / reproduction / pérennité et durabilité des systèmes d’élevage

1. INTRODUCTION

The sustainability of livestock systemsand their ability to adapt to new biocli-matic, technical or socio-economic con-texts can be considered from two pointsof view. The first concerns the decisionalcomponent of the system, which drives el-ements of the biotechnical system towardsshort term objectives that are neverthelessconsistent with long term strategies. Thesecond considers that the ability of a live-stock system to be perennial and respondto some of the challenges of sustainable de-velopment, closely depends on the animaladaptability [70]. This last point of viewappears to be relevant for different live-stock systems. In harsh areas the perennityof livestock farms depends on the capac-ity of the animals to survive and reproducein situations of serious food restriction(drought, pastoral rearing in arid zones). Inupland, wet or rough areas, it relies on their

ability to maintain their performance levels(growth rates, milk production) while mak-ing an efficient use of low quality food re-sources they are incited to graze to answerto socio-economic challenges, like open-ing up areas suitable for leisure activities,maintaining fire-breaks, enhancing land-scapes of value [44] and biodiversity [73].In more intensive systems, female adapt-abilities are also largely requested becauseof high reproductive rhythms and environ-mental constraints [74].

In such contexts, the sustainability oflivestock farming systems and their abilityto change depend on the potential of theanimals to adapt to feeding constraints andbiological rythms, and on the efficiency ofthe physiological (digestive, metabolic andhormonal) and behavioural regulations thatare involved in coping responses.

The first objective of this review is to fo-cus on the mechanisms at work in the adap-tive processes. They are considered to have

Livestock sustainability and animal adaptation 491

a significant impact on the productivity andthe perennity of the livestock farming sys-tem since they will determine the ability ofanimals to maintain or not their productionand reproductive functions. The second ob-jective is to illustrate how the analysis ofresponse profiles to an increased constraintis a way to assess the animals’ adaptivepotentials. Such an approach consists inquantifying the elasticity of the responses(range of response variation according tothe variation of the constraint [9]) and inidentifying disruption thresholds that re-veal failures to adapt. This should lead to amore dynamic analysis of the animals’ re-sponse in connection with the past, presentand future variation of the level of con-straint.

The review considers underfeeding asthe constraint applied to the reproductivefemale. This animal model has been cho-sen because of its major contribution to theoverall performance of the herd, and in re-lation to the role that females play in theperennity of the system through their re-productive function.

The review first focusses on the be-havioural and physiological componentsof the adaptive response and defines theconcepts of elasticity, rebound and failureto adapt (disruption). The interactions be-tween nutrition and reproduction are thenemphasised as they illustrate how twoadaptive strategies (individual survival vs.maternal investisment) may coexist or con-front each other according to the level ofconstraint. At last, the review focusses onthe relationship between adaptability andlongevity of females according to theirgenotype and the level of constraint.

2. CAPACITIES OF FEMALESTO ADAPT TO THEIRENVIRONMENT

Any animal can be considered as a bio-logical system placed in an environment in

which it must carry out three essential andinterdependent functions: to take in nutri-ents, to resist biotic (interspecific, intraspe-cific) and abiotic constraints and finallyto disseminate its genes (fitness). Thesethree functions rely on the expression ofthe behavioural repertoire of each species,as well as on the physiological functioningof the organism.

2.1. Behavioural componentof the adaptive response

Nutrient intake by herbivores resultsfrom the expression of intake and feedselection behaviour. Herbivores are ableto use heterogenous resources by devel-oping selective grazing strategies whichallow them to elaborate a diet of bet-ter nutritional value than what is avail-able to them as a whole [2]. Food se-lection and intake behaviour depend onthe interaction between the animal’s char-acteristics (morpho-physiology, nutritionalrequirement level) and the nature of theavailable vegetation (availability, structure,nutritional value and palatability) [7, 63]).

Under environmental constraints, be-havioural adaptations can emerge. This hasbeen reported with red deer hinds (Cervuselaphus) subjected to high stocking den-sities at pasture [8]. When the spatialconstraint is severe, social tensions canbe observed among fellow animals (in-crease of agonistic encounters, Fig. 1a)as inter-individual distances are reduced.When animals are held in small enclo-sures, subordinate individuals have lesspossibilities of escaping the aggressionsof dominant individuals by fleeing andavoidance behaviour. When spatial dis-persion is not possible, subordinate in-dividuals may develop behavioural pat-terns that lead to spreading activities overtime such as desynchronised or acceler-ated activity rhythms (increase of dailyfrequency of meals while reducing their

492 F. Blanc et al.

Figure 1. Effect of stocking density on the social and feeding behaviour of grazing red deer hinds(adapted from Blanc and Thériez [8]). 1 Agonistic encounters were defined as occasions when onehind physically attacked another or made a ritualised gesture associated with attacks that caused theother animal to move away. They included ‘mild’ threats: ear threats, nose threats and displacementsand severe threats: kicks, bites, butts, pushes and chases.

duration, Fig. 1b) [8]. Such behaviouralcoping strategies limit social tensions, atthe same time enabling subordinate hindsto keep a total grazing time similar to thatof dominant individuals. For the range ofthe spatial constraint studied, the profile ofresponse to changes in grazing time can bequalified as inelastic [9]. Adaptive abilitiesof feeding and intake behaviour have alsobeen studied in cattle managed in groups.In this species, many studies revealed thatincreasing social pressure (high density,heterogeneity of groups, high level of com-petition for food) induces a decrease indaily duration and synchronisation of eat-ing, but a concomitant increase in the in-take rate which helps to maintain the intakelevel of some individuals [49, 50].

Such an ability animals have to de-velop behavioural strategies to cope to a re-stricting environment makes it possible toenvisage changes in practices, sometimesnecessary to guarantee the perennity of thelivestock system (increase in herd size forexample) or even to enhance its impact onvegetation and its contribution to environ-

mental objectives (open up woody areas byincreasing grazing pressure for example).

2.2. Characterisationof the physiological processesinvolved in the adaptive responseto underfeeding

In suckler farming systems, reproduc-tive females are rarely fed at the levelof their theoretical requirements all alongtheir productive cycle. Feeding practicesmostly consist of alternating underfeed-ing and refeeding periods. Feed restrictionscan be more or less severe depending onthe physical components of the environ-ment (climate, vegetation, accessibility offood resource) or on the management de-cisions the breeder takes to reach produc-tion cost objectives. Whilst not ignoringthe importance of other components suchas animal health and product quality, theperennity of this livestock farming systemis largely based on the animals’ ability toadapt to nutritional constraints for more orless long periods.

Livestock sustainability and animal adaptation 493

Figure 2. Metabolic and endocrine adaptations to undernutrition in the ruminant (from Chilliardet al. [26]). NEFA: non-esterified fatty acids, AA: Amino-acids, VFA: volatile fatty-acids, T3-T4:thyroid hormones.

The main effects of endocrinal andmetabolic responses to inadequate nutri-tional requirements are to maintain home-ostasis. Thus, underfeeding adaptations(Fig. 2) involve the coordinated and se-quential mobilisation (short, medium andlong term) of endogenous substrates suchas those stored in the body reserves, thenthe establishment of mechanisms for sav-ing limiting metabolites (glucose, aminoacids) and finally, a reduction in the ba-sic metabolism and energy expenditure(movements, walking). These homeostaticregulations are clearly activated when, forexample, an animal at maintenance is food-restricted [3, 17] in order to ensure its sur-vival.

But outside this transitory state, inwhich the animal is at maintenance, farmanimals, notably females, are usually inproduction. Two underfeeding situationscan be distinguished [28]: the case where

feed is not available in sufficient quantity(restricted feeding) to satisfy requirements(situation qualified as absolute underfeed-ing) and the case where feed is in sufficientquantity and quality (feed ad libitum), butits intake does not allow requirements to besatisfied (situation qualified as relative un-derfeeding).

This latter situation is frequently en-countered in highly productive dairyfemales: at the beginning of lactation,requirements increase more rapidly thanintake capacity [51]. During this periodwhich lasts for several weeks (10 to11 weeks in dairy cows), specific adaptivemechanisms are activated. They enable theanimal to evolve towards a new nutritionalstate (positive energy balance) which is at-tained when intake once again enables re-quirements to be satisfied. The processesat work in this relative underfeeding sit-uation follow an adaptive cascade which

494 F. Blanc et al.

involves high mobilisation of lipids, and toa lesser degree, of body proteins. They al-low supporting an increase in milk produc-tion whilst intake remains limiting [40]. Inthis particular case, the development of thedigestive tract (weight and metabolism ofthe splanchnic tissues) operates indepen-dently of weight variations in other tissuesand progressively allows voluntary intaketo increase. The state of body reserves andthe ability of the female to mobilise themat the start of lactation play an importantrole in the expression of dairy potential.But the loss of adipose mass at the start oflactation can be very variable insofar as therelative underfeeding level depends on themilk production level, the animal’s appetiteand the feed input level [24,25]. Neverthe-less, a loss of 10 to 40% of adipose massis classically observed during the first sixweeks of lactation in cows and ewes. It caneven reach 80% in animals in an under-feeding state [22]. Thus, females in poorbody condition at parturition are particu-larly sensitive to the effects of underfeed-ing at the start of lactation [4,21]). Adiposereserves, which take account of the rema-nent effects of previous feeding conditions,and the female’s ability to mobilise themat the start of lactation play a determiningrole in the expression of dairy potential andin the female’s capacity to adapt to under-feeding in early lactation [32].

Situations of relative underfeeding canvary considerably depending on the nutri-tional strategies applied to the herd of fe-males. Nutritional constraint can for exam-ple be reinforced by restricting feed at thestart of lactation. In this case, analysingthe responses of dairy females to under-feeding at the start of lactation [24, 25, 32]again demonstrates the cows’ adaptive ca-pacity, at least in the medium term. In thecase of moderate under-feeding (85−90%of energy requirements covered) for 4 to11 weeks post-partum in the dairy female(cow, ewe), the reduction in energy ex-ported in milk is less than the deficit in

Figure 3. Effect of energy supply changes (UFLper day, 0 when supply equals requirements) onthe energy exported in milk production of thedairy cow. The energetic conversion ratio wasconsidered to equal 0.44 UFL per kg of milk(adapted from Coulon and Rémond [32]).

energy inputs (Fig. 3): the mobilised bodyenergy contributes more than 30% to theenergy exported by milk. When feedingrestriction is maintained for a long pe-riod (between 18 and 40 weeks), the en-ergy exported by milk reduces and adjuststo the actual energy intake [32]: adaptiveresponses diminish during lactation. Theadaptive capacities allowed by the bodyreserves diminish too when animals areunderfed during several consecutive lacta-tions [21, 76].

When the animal is not at maintenance,the teleophoretic [20] regulations are ac-tive, coordinating the metabolisms by read-justing the set points of the homeostaticregulations [6, 23]. These adaptations aresuch that the integrity of the organism canbe maintained whilst at the same time sup-porting metabolic mobilisations for pro-duction and establishing saving and recy-cling mechanisms. At an energy level, theyare expressed by an increase in the biologi-cal efficiency of certain functions. Thus, inthe cow, adipose reserves are reconstitutedmore efficiently at the end of lactation (Netenergy/Metabolisable energy = 0.60) than

Livestock sustainability and animal adaptation 495

Figure 4. Effect of the pregnancy-lactation cycle on plasma leptin concentrations in nulliparous andprimiparous goats (adapted from Bonnet et al. [18]).

during the dry period (0.40) [51], so thatthe energy deficit at the start of lactationcan be partially compensated for by in-creased energy efficiency of the subsequentreconstitution [24]. This adaptation prob-ably brings into play the endocrine andautocrine role of the adipose tissue, viathe production of leptin, which is liberatedproportionately to adiposity [34], and/orother adipokins. Leptinemia, whose shortterm nutritional regulation is significantlymodulated by adiposity [31], could be animportant energy efficiency regulator to betaken into consideration.

Thus, the more the mass of adipose tis-sue is reduced, the more the animal is stim-ulated to eat and rebuild its fat reserves.What is more, lactation reduces leptine-mia even when the animal is in positiveenergy balance and in good body condi-tion ([18]; Fig. 4), which could favour en-ergy efficiency overall, whatever the stageof lactation [31]. Conversely, the “main-tenance requirement” is higher in the fatcow [1] or ewe [30] than in the thin cowor ewe of the same frame size, probablylinked to the stimulation of heat produc-tion by its increased leptinemia. Finally, atleast in medium term, the impact of a givenlevel of underfeeding will differ according

to the animal’s physiological state and ac-cording to its body condition when it un-dergoes this food restriction.

Most analytical studies on the regula-tion of animals’ energy status have re-vealed that it is the result of a numberof biological regulations which interferewith the different metabolisms (glucidic,proteic, lipidic). Although the enzymaticways and the principal regulation pro-cesses (direct actions) are quite well de-scribed [12, 13, 26, 30], there are, how-ever, numerous indirect regulatory waysthat are expressed differently according tothe physiological and environmental con-text [12, 13, 27]) and to individuals, whichstill remain unclear. This variety of re-sponse nevertheless appears to be a funda-mental element of the animal’s capacity toadapt to variable and contrasted nutritionalsituations.

2.3. From saving to rebound: reactivityof the adaptive response

Adaptive responses of compensation orrebound are observed when a period ofrefeeding succeeds a more or less sustainedand severe phase of feed restriction. The

496 F. Blanc et al.

Figure 5. Long term adaptation of Barbarineewes placed in two situations of food restric-tion: 40% (group M) or 20% (group L) ofrequirements covered, then refeeding (150%of energy requirements covered) (10 ewes pergroup) (adapted from Atti and Bocquier [3]).

most classic example of rebound responseis that of the compensatory growth ob-served upon return to unlimited feed (graz-ing) after a period of feed restriction thatmostly occurs in the winter [48]. The di-gestive and metabolic adaptations at workin this rebound period are effective in a fewdays [48], which demonstrates the reactiv-ity of the organism to benefit from an im-provement in the nutritional conditions.

The rebound process has also beenstressed on adult females during their pro-duction cycle: ewes at maintenance [3],cows and goats in lactation [24]. It inter-venes as much on the lipogenic activitiesof the adipose tissue as on the quantitiesof lipids stored. It is likely to induce sig-nificant differences of feed balance whichhave been demonstrated by comparing twolong term feeding strategies applied to theBarbary ewe [3]. The stabilised strategy,which adjusts inputs to a level that main-tains ewes at a constant weight (mainte-nance requirements for 45 weeks: controlewes), was compared with a dynamic strat-egy consisting of a severe underfeeding(40% or 20% of their energy requirements)for 22 weeks followed by refeeding (130 to150% of requirements for their initial live

weight (Fig. 5). Measurements showed thatthe body composition of ewes underfedthen refed was identical to that of the con-trol ewes [3]. Thus, in the dynamic strat-egy, total net energy inputs (156 UFL, i.e.1108 MJ NEL) are 20% lower than thoserecorded in the stabilised strategy (188UFL, i.e 1336 MJ NEL). In terms of feedcosts, the energy spared corresponds to1.7 months of maintenance requirements.It can be interpreted by an increase in feedefficiency resulting directly from the mech-anisms of mobilisation and saving imple-mented during the chronic underfeedingand refeeding periods [12, 13, 26, 27, 30].Some of these processes involve modula-tion of energy efficiency via leptin or otheradipocyte hormones secreted in a variablemanner depending on adiposity [31].

The processes of saving and rebuildingof muscle and adipose tissues during un-derfeeding and refeeding are more or lessefficient according to species, breed or age.Thus the Barbarine ewe is also able tomobilise its adipose tissues during under-feeding and to rebuild them during refeed-ing [30]. The Barbarine ewe also appearedto be able to rebuild the entire loss of mus-cular mass during refeeding [3]. Such a re-sponse differs in the dry not pregnant adultcow subjected to variable food levels overtime: in the course of the refeeding period,dynamics of lipidic and proteic depositsdiffer and are characterised by an impor-tant growth of adipose tissues whilst re-covery of the muscular mass remains lim-ited [55, 65].

Such a profile of reconstitution of re-serves is similar to that observed in hu-mans (Fig. 6) and is interpreted accordingto Dulloo et al. [38], by a difference in thespeed of lipid and protein deposition dur-ing the refeeding phase. To take account ofrapid fat reserve recovery without modify-ing the speed in depositing proteins duringrefeeding, a model is proposed [38, 45, 46]in which the efficient deposit of adipose re-serves depends on the filling state of the

Livestock sustainability and animal adaptation 497

Figure 6. Pattern of changes in energy intake, body fat and fat-free mass during underfeeding andrefeeding in humans (n = 12). All values are expressed as a percentage of corresponding valuesduring the period previous to feeding restriction (adapted from Girardier [46]).

lipid storage compartment. Such a modelhelps to predict in man, the variations inbody composition after refeeding and de-scribes the change in body compositionof subjects when they return to their ini-tial weight following the semistarvation-refeeding cycle. At this final state, subjectsare fatter than they were at the beginning.At the stage when body fat is completelyrecovered, fat-free mass is still below thecontrol value.

In terms of adaptive potential, such amechanism based on the development ofhighly efficient energy saving can be con-sidered as an important survival factor in acontext where the energy resource is cycli-cal and submitted to random influences(climate variability). However, long termfeed management favouring a successionof underfeeding/refeeding cycles is likelyto induce a progressive deterioration of themuscular mass of the organism if refeedingdoes not last long enough, to allow the pro-teins to recover completely. Such an evo-

lution may be a problem in man (succes-sions of underfeeding periods associatedwith shortages in certain countries, treat-ment by some slimming diets for obesityassociated with overabundance or unbal-anced diet in others), it is less so in live-stock females whose lifetime is relativelyshort (a few years).

2.4. Disruptive situations: the limitsof biological regulation systems

Some production systems and associ-ated management practices, make consid-erable calls on the animals’ adaptive abil-ities, for they are characterised by anaccumulation of constraints on the ani-mal: an increase in animal density and/orin group size, stimulus-poor environments,artificialisation of some biological pro-cesses such as suckling and reproduc-tion [16]. We have previously illustratedthat the animal’s capacity to adapt to

498 F. Blanc et al.

the increasing constraints of its environ-ment is partly based on the implementationof behavioural responses. However, theemergence of highly adaptive behaviouralstrategies is limited to the range of the be-havioural repertoire of each species. Thus,seriously frustrating situations can lead tofailure to adapt [16].

Two approaches are presently beingdeveloped to improve the animals’ be-havioural abilities to adapt to their live-stock environment. The first focusses onactions on the livestock environment tomake it less constrictive for the ani-mal [74]. The second intervenes directlyon the animal to modulate the mannerin which it may experience environmen-tal events, either by acting on its own his-tory (response to stressful events occuringat a more or less early stage [66]), or byselecting animals on the basis of desiredemotional profiles [16]. This second strat-egy aims at directing the adaptive abili-ties of individual animals according to theconstraints specific to the production sys-tem. Although it can prove effective for agiven livestock system, it is at risk for itsperennity if breeding conditions change:in fact rapid and significant modificationsof the surroundings correspond to a newset of constraints which can be very dif-ferent from the environment for whichthe animals were selected. They may thenno longer be capable of developing suf-ficiently effective adaptive behaviour inchanging environments.

Disruptive situations are also observedas regards physiological responses. Rela-tive underfeeding levels applied to dairycows (about −10% of total requirements,or more in a tropical environment) are gen-erally lower than those that may be con-fronted by dairy sheep in a Mediterraneanzone. As in the dairy cow, during seri-ous energy underfeeding, the mobilisationof adipose reserves enables the ewe to acertain extent to continue producing milk.In the Lacaune ewe, as long as the en-

Figure 7. Changes of the standardised milk pro-duction (SMP, expressed in percentage of ini-tial milk production SMPi), in relation to thelevel of energy feed supply (% of total en-ergy requirements) in Lacaune dairy ewes. Eachpoint represents the mean response of 12 ewes(adapted from Bocquier et al. [14]).

ergy deficit does not exceed 20% of totalenergy requirements, the milk productionlinearly declines (reduction relative to theinitial dairy production) with the energysupply (Fig. 7). On the contrary, when theenergy supply goes below 80% of the re-quirements, the fall in milk production isdramatic [14]. This fall accounts for a dis-ruption in the homeostatic balance, charac-terised by a serious reduction in the insulincirculating rates in ewes that are severelyunderfed.

This situation arises frequently in live-stock where animals are herd-managed. Infact, the diversity of production levels andphysiological states within a large herd, fedin a single way, can cause disruption situ-ations in some sensitive individuals [11].Sensitive animals are those which, takinginto account the available food resourcesand their intake capacity, will not be ableto satisfy their requirements. Within a herd,the proportion of sensitive animals de-pends not only on the variability of nu-tritional requirements (physiological stage,production level) and the diet value (bulk,nutritional value), but also on the hier-archical status of the individuals (domi-nant, subordinate). Nevertheless, in dairyewes, feeding strategies can be set up to

Livestock sustainability and animal adaptation 499

limit such disruptive situations in sensi-tive individuals. In this way, a collectivediet does not usually lead to a problemwhen the ration is calculated to satisfythe requirements of at least 80% of theindividuals [11]. When the breeder hasproductive animals but poor quality forage,satisfying 80% of the individuals’ require-ments implies using concentrates whichwill not be valorised by low-producinganimals. To avoid such a waste, the onlysolution is to divide the herd into groupsof homogenous animals according to theirproduction level. If, however, it is acceptedthat some animals adapt (downwards) theirproduction levels to the value of the diet,the system becomes less demanding interms of inputs and to this extent satisfiesmore sustainability issues. Synchronisingnutritional requirements within a herd is arisky practice when the production factorsare not very well-controlled (feed in par-ticular) and when animals may be placedin a situation of adaptive disruption dur-ing their production cycle. So it seems that,for livestock systems in which reproduc-tion periods are not well controlled and thephysiological stages of the animals are dis-persed, the adaptive capacity of the herdconsidered as a whole may be greater thanthat of a cohort of individuals with a nar-row range of nutritional requirements [5].

3. CENTRAL ROLEOF RELATIONSHIPBETWEEN NUTRITIONAND REPRODUCTIONFOR THE PERENNITYOF THE HERD IN A SITUATIONOF NUTRITIONAL CONSTRAINT

The reproductive function is a key ani-mal component of the productivity of live-stock farming systems. Numerous studieshave emphasised the sensitivity of this bi-ological function to the nutritional statusof the female. The effects of nutrition on

the ability to reproduce can be observed atdifferent phases of the female’s productivelife: at a young age via its effects on theonset of puberty, then in adult females byits impact on the fertility rate (and on pro-lificacy) and therefore on the reproductiverhythm. More particularly, the role of en-ergy balance and the mobilisation of adi-pose reserves have clearly been demon-strated (reviews of Butler [19] for the dairycow, of Diskin et al. [37] for the suck-ler cow) and have led to approaches forintegrating and formalising the processesat work. Thus, Friggens [43] developed aconceptual framework where body lipid re-serves vary with time through the repro-ductive cycle and are the link between thecyclic nature of reproductive priorities andstrategies for dealing with environmentalconstraints. The relationship between thefemale’s nutritional state and reproductivefunction is very particular, because the en-ergy requirements for reproduction per se,i.e. ovulation and conception, are practi-cally negligible. On the contrary, initialis-ing a pregnancy has heavy consequencesfor the survival of the female if nutritionalinputs and/or its body reserves are insuf-ficient. Indeed, its requirements will in-crease during pregnancy and above all, af-ter the start of lactation. This means that,at the level of the individual female, repro-ductive priorities between the current andthe next offspring may change over timeand according to the nutritional status ofthe female.

The regulation of reproduction by thenutritional status therefore supposes, at agiven time, the implementation of mech-anisms for simultaneously evaluating theenergy balance and the state of the adiposereserves. Such an evaluation, at key phasesof the reproductive process (days follow-ing calving in the dairy cow), could be away of assessing the commitment of thefemale to a new pregnancy, thus limitingthe risk associated with reproduction [19,23]. To summarise [43], the rate of energy

500 F. Blanc et al.

mobilisation at the reproductive period isthen seen as a monitor of current environ-mental conditions, whereas body fatness isproposed as an indicator of ability to with-stand future environmental constraints andmanage the risk to invest in a new repro-ductive cycle. The ability of the dam tosupport the demands of future offspring ina constrained environment will thus largelydepend on the size of her body reserves.Such processes are advantageous for theanimal to maintain flexibility in resourceallocation and be able to cope with nutri-tional constraint.

The physiological mechanisms at workin the management of reproductive priori-ties between the current and the future off-spring appear to be very complex and arestill not understood [19]. Hormones suchas insulin and leptin are considered to playa role in the control of reproduction [68].Leptinemia (and other signals from adi-pose tissues) probably intervenes since itis linked both to the level of reserves andto the present nutritional status (cf. above),and it seems able to limit reproductionwhen it is below a threshold of about 4 to5 ng per mL (Fig. 8; [47,57,61]). Two pos-sible ways of control are suggested in theliterature. One considers that leptin (and/orinsulin) could directly mediate the effectsof energy metabolism on the reproductiveaxis, the other supposes that leptin couldmodulate the availability of metabolic fuelsin the brain or periphery (Schneider [68]).

3.1. The effects of the nutritional statusof females on their survivaland their reproductive investmentdepend on the dynamicof the production cycle

Environmental constraints, in particularthose related to food availability, the levelof technical and technological control, andthe biological peculiarities of the speciesare reasons for a variety of reproduction

Figure 8. Concentration of leptin (least squaresmeans ± SEM) in lean (P-BCS < 3) and fat (P-BCS ≥ 3) primiparous cows and lean (M-BCS <3) and fat (M-BCS ≥ 3) multiparous cows(BCS = body condition score) (adapted fromMeikle et al. [61]).

management methods [72]. Thus, in an ex-treme situation, in South Senegal (Kolda),the reproductive pattern of N’Dama cowsis characterised by great intervals of timebetween reproductive events, with an aver-age age at first parturition of 5 years and anaverage calving interval of 2.3 years [39].On the contrary, in herds in a temperate cli-mate, reproduction patterns are often closeto the theoretical biological limits of thespecies: calving interval close to one yearor even 3 lambings in 2 years in a sucklersheep flock.

In the first case (rather insecure sys-tems), the adaptive capacities of livestocksystems rely principally on the animalcomponent. The biological regulations,namely the balances between homeostasisand productive functions (teleophoresis),determine the dynamics of reproductive

Livestock sustainability and animal adaptation 501

events and the survival of females. Thesebalances lead to variable reproductionrhythms and long time steps. The analysisof these patterns [39] shows that reproduc-tion is only effective when a sufficient bodycondition coincides in time with favourablenutritional conditions. Another importantelement in these Sub-Saharan pastoral sys-tems is the decision to cull females that notalways directly depends on their ability toreproduce, since a live animal is consid-ered as a financial capital to be maintainedas a priority and at the lowest cost. Conse-quently, the survival of females within sucha system mainly depends on the animal’sability to adapt to environmental condi-tions and particularly to underfeeding.

In intensive livestock systems, high re-productive rhythms are sought (using hor-monal treatments) and practices of feed-ing, replacement, and culling support andorientate the reproductive performances offemales, as well as their survival. Forspecies characterised by long reproduc-tive cycles (i.e. cattle), as well as forthose with short but accelerated cycles (i.e.sheep), reproductive patterns tend to bevery close to physiological limits [33, 56].In fact, intervals between successive par-turitions impose very short resting periods.Thus, biological regulations of the differentfunctions are highly stimulated and workinterdependently because of the rapid suc-cession or even overlap of different phys-iological states. So these regulations canlead to disruptive states after which one ofthe functions associated with reproduction(fertility, milk production) is altered. Sucha response can then be interpreted, for thebreeder, as insufficient adaptive abilities ofthe animal, and for the female, as a strat-egy to survive. Insofar as females unableto adapt to such accelerations in rhythmare usually culled, physiological processesfavouring the survival of the individualto the detriment of its investment in thefollowing generation, are not activated insuch intensive systems. High milking dairy

cows are particularly sensitive to this riskof culling because, selected for their milkproduction level, they are less able to re-produce in the conditions desired by thelivestock farmer (a negative genetic corre-lation of −0.3 is observed between milkproduction level and fertility at first arti-ficial insemination; [15]). In this context,it appears useful to understand the inter-action between nutrition and reproductionto avoid disruption situations or functionalblockage (anoestrus).

3.2. Characterisationof the interrelationships betweennutrition and reproduction

The effects of nutrition on the reproduc-tive efficiency of females have been widelystudied in suckler farming systems. Thesestudies are particularly instructive whenwe focus on the question of the perennityof the system insofar as suckling systemsare based on a maximum use of forage re-sources. The animals concerned may there-fore often be subjected to very long, in-tense phases of food restriction. Studiesemphasise the effects of food restrictionnot only on the physiological characteris-tics of reproductive function, but also onthe sexual behaviour of females.

In dairy and suckler cattle systems intemperate zones, nutrition × reproductioninteractions come into play mainly in thedays following calving, during the acyclicperiod that follows calving [69]. An in-crease in the postpartum anoestrus dura-tion in relation with low body condition atcalving was observed in our experimentalfarms: food supply during the winter hasmore influence on the length of postpar-tum anoestrus than on overall fertility incattle [62]. Thus, a one point decrease be-low the mean body condition score induceda 10-day delay in the resumption of ovar-ian activity in multiparous cows and a 20-day delay in primiparous cows [62]. The

502 F. Blanc et al.

female therefore clearly invests in a newproduction cycle, but at a slower rhythm.This is particularly the case of primiparouscows whose growth function (includingprotein metabolism; [75]) interacts withlactation and reproduction functions. Thishas notably been observed in dairy farmingsystems with a parity × growth hormonetreatment interaction on reproduction (re-view of [29]) and body reserves [64], and aparity × body condition at calving interac-tion on reproduction [61].

Physiological mechanisms at work inregulating the reproductive function linkedto the nutritional status of cows have re-cently been the subject of bibliographicalreviews [19, 37]. In the suckler cow, mod-erate but prolonged food restriction (60to 70% of satisfied requirements) is ac-companied by a progressive reduction ingrowth of the dominant ovarian follicleand its persistence. If this underfeeding isprolonged in such a way that live weightlosses exceed 20% of the initial weight,the animals go into a state of nutritionalanoestrus [37]. This response neverthelessshows very high interindividual variabil-ity whose causes can be multiple (genetics,age, parity and adiposity). These disruptivesituations (nutritional anoestrus) can alsobe observed in the case of very severe foodrestrictions. Severe underfeeding (40% ofrequirements satisfied in the animal atmaintenance) of short duration is accompa-nied by a rapid decrease in growth rate andmaximum diameter of dominant follicles.It induces anoestrus in a high proportionof individuals (60%) in the 15 days fol-lowing the start of food restriction [37, 59].Observation of such differences in folli-cle development dynamics and ovulationbetween the studies of chronic and acutedietary restriction suggests that the phys-iological response to undernutrition maybe related to a threshold below which theeffects on follicle development are rapid.This threshold seems to lie in the range be-tween 40 and 60% of maintenance require-

ments [37]. Such a response is interpretedas a disruptive situation in which the indi-vidual’s survival function becomes a pri-ority and is developed to the detriment ofcommitment to the following generation.

Rebound type responses are to befound alongside these disruption phenom-ena. They account for a temporary increasein the system’s efficiency during under-feeding/refeeding sequences. Thus, femalelambs undergoing severe food restrictionafter weaning show significant delays inthe initiation of puberty, even a durableblockage of the reproductive function [42].Refeeding was observed to induce the on-set of puberty within a few weeks in ewelambs whose puberty was previously in-hibited by food restriction [41].

Recent observations lead us to sup-pose that interactions between nutritionand reproduction not only play at a phys-iological level but also at a behaviouralone. Indeed, ewe lambs that were severelyunderfed from weaning to 8 months ofage all reached puberty (increase in pro-gesterone concentrations over 1 ng permL) after a 3 week refeeding period, butonly 40% of them expressed oestrous be-haviour [10]. Thus, even if the effects offood restriction on sexual behaviour havebeen relatively little studied in ruminants,it is suggested that oestrous behaviour isa way of regulating the female’s responseto underfeeding. Maintaining ovarian func-tioning (not very costly), while inhibitingsexual behaviour may allow a minimisa-tion of the risk of fertilisation in a sit-uation of uncertainty for food availabil-ity, at the same time ensuring high reac-tivity in the system if the food situationbecomes more favourable. Such reactivityseems to depend on the animals’ body con-dition at the time of refeeding because, asfor leptinemia where response to overfeed-ing depends on the adiposity level [30],some limitations may exist in animals thatare too lean, as suggested by the non re-sponse of LH pulsatility to refeeding in

Livestock sustainability and animal adaptation 503

these animals [28]. As long as a disruptionthreshold has not been reached, the systemmight be able to react rapidly thanks to thecontinuation of underlying ovarian activityand to a behavioural regulation which maytemporarily block oestrus expression. Fur-ther investigations are needed to validatesuch a hypothesis.

4. ADAPTIVE RESPONSESTO UNDER-FEEDING:CONSEQUENCESON THE LENGTHOF THE PRODUCTIVE CAREERAND INFLUENCEOF THE GENOTYPE

In a steady state livestock system (with aconstant number of reproductive females),the female replacement rate largely deter-mines their productive lifetime within theherd (longevity). For the farmer, this ratemust be optimised because rearing youngfemales for replacement represents highbreeding costs. As soon as these femalesjoin the adult group, the farmer’s interestis to keep them, provided that there is noeconomic depreciation on the cull carcass.The productivity of females must there-fore be evaluated globally over their com-plete lifetime. One work carried out in thesuckler cattle system has clearly demon-strated the interaction that exists betweenthe adaptive potential of cows placed inunderfeeding situations and the durationof their productive lifetime. The compari-son focussed on the responses of two cattlebreeds, Salers and Limousine, reared andmanaged according to two feeding levels(High vs. Low) from weaning to fourth lac-tation [36]. Differences in feeding levelsbetween the High and Low groups wereoperated from mid-August to the end ofApril, first of all using the stocking rate atgrazing, then during the winter, the cowsin the High groups were fed according totheir requirements, whilst the energy re-

quirement cover rate of the Low groupswas 80%. Only one period of ad libitumgrazing, lasting 3.5 months, was commonto all the animals.

During the winter period, underfeedinghad no effect on the average milk produc-tion of the primiparous and multiparousSalers cows (−0.5 kg, ns), whilst it didaffect milk production of the Limousines(−1.0 to 1.5 kg, P < 0.01; Fig. 9).

After ad libitum grazing, the milk pro-duction of cows in the Low groups in-creased (Limousines), and even signifi-cantly exceeded (multiparous Salers) thoseof previously better fed cows (Fig. 9). Thedifferences between Salers and Limousineresponse profiles can be interpreted eitherby larger adipose reserves (at maturity) thatare more easily mobilised in the Salers, orby differences in grazing intake levels.

Whilst in the Salers, the difference of50 kg live weight observed at first calv-ing between the two feeding levels re-mained unchanged after four lactations, thesame initial difference entirely disappearedin the Limousines, without observing anydrift linked to the cull policy (the distri-bution of live weights of culled cows inthe two breeds was identical to that ofthe cows retained) (Fig. 10). Such resultscan be interpreted in the following way:the Salers cow gives priority to produc-ing milk for its calf growth, then for newpregnancies (maternal investment), whilstthe Limousine continues to grow and storereserves for itself (survival of the individ-ual). As regards the reproductive function,the Salers cows also appeared less sensi-tive to underfeeding [35]. In fact, the differ-ence in duration of post-partum anoestrusobserved between animals in the High andLow groups was lower in the Salers thanin the Limousines. Furthermore, there wasa breed × parity interaction in accordancewith the greater sensitivity of primiparouspreviously reported (respectively −7 vs.−12 days for multiparous and −15 vs.−43 days for primiparous). Over the long

504 F. Blanc et al.

Figure 9. Change over time, depending on parity, of the milk production Salers ( , ) and Limou-sine ( , ) (n = 127) cows exposed to two feeding levels in the winter: High (energy require-ments covered) or Low (80% of energy requirements covered in the winter) (adapted from D’Houret al. [36]).

term, after four lactations in a situation offood restricted resources, a difference incapacity to adapt between breeds emerged.This had direct effects on the cows’ sur-vival rate (Fig. 11), which resulted from aculling policy based mainly on the elimina-tion of empty females (reproductive failureduring the breeding period).

In suckler systems, interactions betweenproductive and reproductive abilities haveoften been measured in order to select thebest genotypes in a given environment.Some studies analysed the differences inadaptive responses between genotypes ina non-optimal situation and accounted forhow these adaptive potentials could mod-ify the productivity and efficiency of thesystem. In the suckler cow, the responsecurves describing the production level ac-cording to various food constraint levelsdiffer according to breeds [52]. For somegenotypes (group 1: Charolais, Limousin,

Figure 10. Change over time of the live weightsof Salers ( , ) and Limousine ( , ) cows ex-posed to two feeding levels in the winter: High(energy requirements covered) or Low (80%of energy requirements covered in the winter)(adapted from D’Hour and Petit [35]).

Simmental), the production level linearlyincreased with the feeding level, whilstfor others (group 2: Angus, Red Poll,Hereford), the productivity curve went via

Livestock sustainability and animal adaptation 505

Figure 11. Change over time of survival ratesof Salers ( , ) and Limousine ( , ) cows(% of cows remaining in the herd) exposed totwo feeding levels in the winter: High (energyrequirements covered) or Low (80% of energyrequirements covered in the winter) (D’Hourand Petit [35]).

an optimum (Fig. 12). Thus the breedsin group 2 had higher productivity (kg ofweaned calf per reproductive cow) in a sit-uation of food restriction. On the contrary,when inputs increased, their productivitybecame comparable to, or even lower than,that of breeds in group 1. The biological ef-ficiency of breeds in group 2 (breeds qual-ified as early maturing) diminished whenfood conditions became favourable, inso-far as the growth potential of their calveswas lower than that of calves from breedsin group 1 (late maturing breeds).

The notion of early sexual maturity des-ignates the ability of an animal to rapidlyestablish its adipose tissues to reach a givenmaturity rate. This concept is not only usedto discriminate response profiles betweenbreeds, but also to characterise the re-sponses of individuals within a same breed.In the Retinta cow reared in a semi-aridMediterranean environment, a positive cor-relation has been observed [58] betweenthe precocity of females and their pro-ductivity (total weight of weaned calves),whilst this correlation was negative for RedPoll females reared in more favourablefeeding conditions [60]. Such results indi-cate that the choice of genotype determines

Figure 12. Predicted weight of calves weanedper cow exposed at varying dry matter intakesfor nine breeds of cattle (adapted from Jenkinsand Ferrell [52]).

the adaptive potential of the animals andhas an influence on the sensitivity of thefarming system to increasing feed con-straint [52, 53]. The concept of precocityleads moreover to envisaging the regula-tion processes between production and re-production functions over the long termand in association with the dynamics ofbody development (evolution of weightand body composition) in the growinganimal.

5. CONCLUSION

The model of the reproductive femalereared in a restrictive nutritional environ-ment reveals that, according to the live-stock farming systems, the adaptive re-sponse that gives priority to the individualsurvival before maternal investment, maynot be efficient in some livestock farm-ing systems. If this strategy contributesto the perennity of the herd in systemsthat face very severe food restriction pe-riods by depressing fertility and avoidingfutile maternal investment [43], it para-doxically appears to challenge the sur-vival of individuals in most livestock farmsin temperate zones, because of the pres-sure of culling on unproductive females oron females whose reproductive activity is

506 F. Blanc et al.

simply delayed. Consequently, abilities ofanimals to accommodate to environmentalconstraints have to be considered in refer-ence to a given context and any generali-sation to quite different systems should bequestioned.

However, rearing animals adapted tochanges is a real issue of finalised researchthat aims at proposing durable and sus-tainable farming systems in various envi-ronments. Such an approach is already de-veloped in order to find out more aboutanimals’ response variations according totheir genotype [53, 54] and to identify theresponse profiles that allow better adap-tive potentials to appear. Comparative ap-proaches are interesting to quantify the re-sponse of different genotypes or differenttypes of animals (primiparous vs. multi-parous) to a variation of a single con-straint. They reveal if a type is more able toadapt and/or to produce throughout differ-ent levels of a studied constraint. These ap-proaches may, however, fail to predict whatwill be the animals’ response within a newscale of constraint levels or under a new setof constraints.

Since we emphasised that the questionof the sustainability of livestock systemspartly refers to the question of the abil-ity of animals to adapt to changes in prac-tices or in the environment, it would makesense to think of how to predict adaptive re-sponses to various management decisions.An interesting way could be to use meta-analyses that allow to integrate knowledgeand quantify the response from the findingsfrom a collection of studies [67, 71].

To understand how behavioural andphysiological adaptations operate duringthe lifespan of the animal, it is neces-sary to rely on biological knowledge ofadaptations in domestic animals. It maybe quite easy to conceive the interest ofhomeostatic regulations for the survivalof an animal at maintenance, but it ismore difficult to predict the effects ofteleophoretic regulations which are partic-

ularly active in animals selected on theirproduction level. These teleophoretic dy-namics, directed firstly towards concep-tion then the survival of the young, aredeveloped under the dependence of phys-iological (metabolic, hormonal) and be-havioural regulation processes which alsotend to guarantee the survival of the fe-male itself (homeostasis). In these twotypes of adaptation (survival of the individ-ual and survival of the species) body re-serves appear to play a fundamental rolein restoring the energy balance. The studyof animal adaptation to undernutrition em-phasises the existence of regulatory pro-cesses which seem to reveal a real capacityfor anticipation and nutritional risk man-agement. The mechanisms implied in thisaptitude to anticipate are unknown. In thesame way little is known about the inci-dence of the past nutritional trajectories offemales on their aptitude to invest in a newproductive cycle in relation to their nutri-tional status at the time of reproduction.Thus, future research should investigate amore dynamic approach of adaptive pro-cesses. Systemic modelling appears to behelpful to take account of the processes intheir dynamic dimension and makes it pos-sible to conceive memorisation phenomenalikely to induce variations in the animals’medium and long term productive trajecto-ries. Such a prospect is clearly suggestedby Girardier [46] who stated from studieson the body composition dynamics in manthat “the ultimate control of energy bal-ance would not bear on the homeostasis ofa state of body composition but rather onits dynamic stability. This is giving a his-torical dimension to the system, some sortof memory of past conditions which willaffect its further evolution”.

REFERENCES

[1] Agabriel J., Petit M., Recommandationsalimentaires pour les vaches allaitantes,

Livestock sustainability and animal adaptation 507

Bull. Tech. CRVZ Theix INRA 70 (1987)153−166.

[2] Agreil C., Fritz H., Meuret M., Maintenanceof daily intake through bite mass diversityadjustment in sheep grazing on heteroge-neous and variable vegetation, Appl. Anim.Behav. Sci. 91 (2005) 35−56.

[3] Atti N., Bocquier F., Adaptation des bre-bis Barbarine à l’alternance sous-nutrition –réalimentation : effets sur les tissus adipeux,Ann. Zootech. 48 (1999) 189−198.

[4] Atti N., Nefzaoui A., Bocquier F., Influencede l’état corporel à la mise bas surles performances, le bilan énergétique etl’évolution des métabolites sanguins de labrebis Barbarine, Opt. Méd. Sér. A 27 (1995)25−33.

[5] Atti N., Bocquier F., Khaldi G., Performanceof the fat-tailed Barbarine sheep in its en-vironment: adaptive capacity to alternationof underfeeding and refeeding periods. A re-view, Anim. Res. 53 (2004) 165−176.

[6] Bauman D.E., Vernon R.G., Effects of ex-ogenous bovine somatotropin on lactation,Annu. Rev. Nutr. 13 (1993) 347−461.

[7] Baumont R., Prache S., Meuret M., Morand-Fehr P., How forage characteristics influencebehaviour and intake in small ruminants: areview, Livest. Prod. Sci. 64 (2000) 15−28.

[8] Blanc F., Thériez M., Effects of stockingdensity on the behaviour and growth offarmed red deer hinds, Appl. Anim. Behav.Sci. 56 (1998) 297−307.

[9] Blanc F., Bocquier F., Agabriel J., D’hour P.,Chilliard Y., Amélioration de l’autonomie al-imentaire des élevages de ruminants : con-séquences sur les fonctions de productionet la longévité des femelles, Renc. Rech.Ruminants 11 (2004) 155−162.

[10] Blanc F., Fabre D., Bocquier F., Canepa S.,Delavaud C., Caraty A., Chilliard Y., DebusN., Effects of a postweaning restricted nu-trition on the initiation of puberty, plasmaleptin and the reproductive performances ofearly-bred Merino ewes lambs. 11th Seminarof the Sub-Network FAO-CIHEAM on sheepand goat nutrition, Opt. Méd. (2006) in press.

[11] Bocquier F., Guillouet Ph., Barillet F.,Alimentation hivernale des brebis laitières :intérêt de la mise en lots, INRA Prod. Anim.8 (1995) 19−28.

[12] Bocquier F., Ferlay A., Chilliard Y., Effectsof body lipids and energy balance on theresponse of plasma nonesterified fattyacids to a beta-adrenergic challenge inthe lactating dairy ewe, in: McCrackenK., Unsworth E.F., Wylie A.R.G. (Eds.),Energy Metabolism of Farm Animals,CAB International, Wallingford, UK, 1998,pp. 167−173.

[13] Bocquier F., Bonnet M., Faulconnier Y.,Guerre-Millo M., Martin P., Chilliard Y.,Effects of photoperiod and feeding level onadipose tissue metabolic activity and leptinsynthesis in the ovariectomized ewe, Reprod.Nutr. Dev. 38 (1998) 489−498.

[14] Bocquier F., Caja G., Oregui L.M., Ferret A.,Molina E., Barillet F., Nutrition et alimenta-tion des brebis laitières, Opt. Méd. Sér. B 42(2002) 37−55.

[15] Boichard D., Barbat A., Briend M.,Évaluation génétique des caractères defertilité femelle chez les bovins laitiers,Renc. Rech. Ruminants 5 (1998) 103−106.

[16] Boissy A., Fisher A.D., Bouix J., Hinch G.N., Le Neindre P., Genetics of fear in rumi-nant livestock, Livest. Prod. Sci. 93 (2005)23−32.

[17] Bonnet M., Leroux C., Faulconnier Y.,Hocquette J.F., Bocquier F., Martin P.,Chilliard Y., Lipoprotein lipase activity andmRNA are up-regulated by refeeding in adi-pose tissue and cardiac muscle of sheep, J.Nutr. 130 (2000) 749−756.

[18] Bonnet M., Delavaud C., Rouel J., ChilliardY., Pregnancy increases plasma leptin in nul-liparous but not primiparous goats while lac-tation depresses it, Domest. Anim. Endocrin.28 (2005) 216−223.

[19] Butler W.R., Energy balance relationshipswith follicular development ovulation andfertility in postpartum dairy cows, Livest.Prod. Sci. 83 (2003) 211−218.

[20] Chilliard Y., Revue bibliographique :Variations quantitatives et métabolisme deslipides dans les tissus adipeux et le foieau cours du cycle gestation-lactation. 1.Chez la ratte, Reprod. Nutr. Dev. 26 (1986)1057−1103.

[21] Chilliard Y., Physiological constraints tomilk production: factors which determinenutrient partitioning, lactation persistency,and mobilization of body reserves, WorldRev. Anim. Prod. (1992) 19−26.

508 F. Blanc et al.

[22] Chilliard Y., Metabolic adaptations and nu-trient partitioning in the lactating animal,in: Martinet J., Houdebine L.M., HeadH.H. (Eds.), Biology of lactation, CollectionMieux Comprendre, INRA Éditions, Paris,FRA, 1999, pp. 503−552.

[23] Chilliard Y., Bocquier F., Direct effects ofphotoperiod on lipid metabolism, leptin syn-thesis and milk secretion in adult sheep, in:Cronjé P.B. (Ed.), Ruminant physiology: di-gestion, metabolism, growth and reproduc-tion, CAB International, Wallingford, UK,2000, pp. 205−223.

[24] Chilliard Y., Rémond B., Sauvant D.,Vermorel M., Particularités du métabolismeénergétique, Bull. Tech. CRZV Theix INRA53 (1983) 37−64.

[25] Chilliard Y., Rémond B., Agabriel J.,Robelin J., Vérité R., Variations du contenudigestif et des réserves corporelles au coursdu cycle gestation lactation, Bull. Tech.CRZV Theix INRA 70 (1987) 117−131.

[26] Chilliard Y., Bocquier, F., Doreau M.,Digestive and metabolic adaptations of rumi-nants to undernutrition, and consequences onreproduction, Reprod. Nutr. Dev. 38 (1998)131−152.

[27] Chilliard Y., Ferlay A., Després L., BocquierF., Plasma non-esterified fatty acid responseto a beta-adrenergic challenge in underfed oroverfed, dry or lactating cows, before or afterfeeding, Anim. Sci. 67 (1998) 213−223.

[28] Chilliard Y., Doreau M., Bocquier F., Lesadaptations à la sous-nutrition chez les her-bivores, Cah. Nutr. Diét. 33 (1998) 217−224.

[29] Chilliard Y., Colleau J.J., Disenhaus C.,Lerondelle C., Mouchet C., Paris A.,L’hormone de croissance recombinante : in-térêt et risques potentiels de son utilisationpour la production laitière bovine, INRAProd. Anim. 11 (1998) 15−32.

[30] Chilliard Y., Ferlay A., Faulconnier Y.,Bonnet M., Rouel J., Bocquier F., Adiposetissue metabolism and its role in adaptationsto undernutrition in ruminants, Proc. Nutr.Soc. 59 (2000) 127−34.

[31] Chilliard Y., Delavaud C., Bonnet M.,Review. Leptin expression in ruminants: nu-tritional and physiological regulations inrelation with energy metabolism, Domest.Anim. Endocrin. 29 (2005) 3−22.

[32] Coulon J.B., Rémond B., Variations in milkoutput and milk protein content in responseto the level of energy supply to the dairy cow:a review, Livest. Prod. Sci. 29 (1991) 31−47.

[33] Cournut S., Dedieu B., A discrete eventssimulation of flock dynamics: a managementapplication to three lambings in two years,Anim. Res. 53 (2004) 383−403.

[34] Delavaud C., Ferlay A., Faulconnier Y.,Bocquier F., Kann G., Chilliard Y., Plasmaleptin concentration in adult cattle: Effects ofbreed, adiposity, feeding level, and meal in-take, J. Anim. Sci. 80 (2002) 1317−1328.

[35] D’hour P., Petit M., Influence of nutritionalenvironment on reproductive performancesof Limousin and Salers cows, in: PullarD. (Ed.), Suckler cow workers meeting,Kirbymoorside, UK, 1997, pp. 15−18.

[36] D’hour P., Petit M., Pradel P., Garel J.P.,Évolution du poids et de la productionlaitière au pâturage de vaches salers etlimousines dans deux milieux, Renc. Rech.Ruminants 2 (1995) 105−108.

[37] Diskin M.G., Mackey D.R., Roche F.,Sreenan J.M., Effects of nutrition andmetabolic status on circulating hormonesand ovarian follicle development in cattle,Anim. Reprod. Sci. 78 (2003) 345−370.

[38] Dulloo A.G., Jacquet J., Girardier L.,Autoregulation of body composition duringweight recovery in human: the MinnesotaExperiment revisited, Int. J. Obesity 20(1996) 393−405.

[39] Ezanno P., Ickowicz A., Bocquier F.,Factors affecting the body condition score ofN’Dama cows under extensive range man-agement in Southern Senegal, Anim. Res. 52(2003) 37−48.

[40] Faverdin P., Bareille N., Lipostatic regula-tion of feed intake in ruminants, in: van derHeide D., Huisman E.A., Kanis E., OsseJ.W.M., Verstegen M. (Eds.), Regulationof Feed Intake, Wageningen, Netherlands,1999, pp. 89−102.

[41] Foster D.L., Olster D.H., Effect of restrictednutrition on puberty in the lamb: patternsof tonic luteinizing hormone (LH) secretionand competency of the LH surge system,Endocrin. 116 (1985) 375−381.

[42] Foster D.L., Yellon S.M., Olster D.H.,Internal and external determinants of the tim-ing of puberty in the female, J. Reprod.Fertil. 75 (1985) 327−344.

Livestock sustainability and animal adaptation 509

[43] Friggens N.C., Body lipid reserves and thereproductive cycle: towards a better under-standing, Livest. Prod. Sci. 83 (2003) 219–236.

[44] Gibon A., Managing grassland for produc-tion, the environment and the landscape.Challenges at the farm and the landscapelevel, Livest. Prod. Sci. 96 (2005) 11−31.

[45] Girardier L., L’auto-régulation du poids etde la composition corporelle chez l’homme.Une approche systémique par modélisationet simulation, Arch. Int. Physiol. Biochim.Biophys. 102 (1994) A23−A35.

[46] Girardier L., Body energy store manage-ment during fasting and recovery: a sys-temic approach, in: Guy-Grand B., AilhaudG. (Eds.), Prog. Obesity Res. (John Libbey& Company Ltd) 8 (1999) 467−481.

[47] Giuliodori M., De La Sota R.L., Formia N.,Chilliard Y., Delavaud C., Becu-VillalobosD., Lacau-Mendigo I.M., Leptin level in-creases before post-partum first ovulation indairy cows, Biotech. Agron. Soc. Environ. 8(2004) 45.

[48] Hoch T., Begon C., Cassar-Malek I., PicardB., Savary- Auzeloux I., Mécanismes et con-séquences de la croissance compensatricechez les ruminants, INRA Prod. Anim. 16(2003) 49−59.

[49] Ingrand S., Agabriel J., Lassalas J., DedieuB., How group feeding influences intakelevel of hay and feeding behaviour of beefcows, Ann. Zoot. 48 (1999) 435−444.

[50] Ingrand S., Comportement alimentaire,quantités ingérées et performances desbovines conduits en groupe, INRA Prod.Anim. 13 (2000) 151−163.

[51] INRA (Institut National de la RechercheAgronomique), Alimentation des bovins,ovins et caprins, in: Jarrige R. (Ed.), INRA,Paris, 1988, 476 p.

[52] Jenkins T.G., Ferrell C.L., Productivitythrough weaning of nine breeds of cattle un-der varying feed availabilities: I. Initial eval-uation, J. Anim. Sci. 72 (1994) 2787−2797.

[53] Jenkins T.G., Ferrell C.L., Efficiency offeed utilization of diverse biological typesof cattle, in: Proceedings of the 7thWorld Congress on Genetics Applied toLivestock Production, Montpellier, France,2002, pp. 285−288.

[54] Jenkins T.G., Ferrell C.L., Preweaning ef-ficiency for mature cows of breed crossesfrom tropically adapted Bos indicus and Bostaurus and unadapted Bos taurus breeds, J.Anim. Sci. 82 (2004) 1876−1881.

[55] Laurenz J.C., Byers F.M., Schelling G.T.,Greene L.W., Periodic changes in body com-position and in priorities for tissue storageand retrieval in mature beef cows, J. Anim.Sci. 70 (1992) 1950−1956.

[56] Lee G.J., Atkins K.D., Prediction of life-time reproductive performance of AustralianMerino ewes from reproductive performancein early life, Aust. J. Exp. Agr. 36 (1996)123−128.

[57] Liefers S.C., Veerkamp R.F., te Pas M.F.W.,Delavaud C., Chilliard Y., Van der Lende T.,Leptin levels in relation to energy balance,milk yield, dry matter intake, liveweight, andfertility in dairy cows, J. Dairy Sci. 86 (2003)798−807.

[58] Lopez de Torre G., Candotti J.J., ReverterA., Bellido M.M., Vasco P., Garcia L.J.,Brinks J.S., Effects of growth curve param-eters on cow efficiency, J. Anim. Sci. 70(1992) 2668−2672.

[59] Mackey D.R., Wylie A.R.G., Sreenan J.M.,Roche J.F., Diskin M.G., The effect ofacute nutritional change on follicle waveturnover, gonadotropin, and steroid concen-tration in beef heifers, J. Anim. Sci. 78(2000) 429−442.

[60] Marshall T.E., Mohler M.A., Stewart T.S.,Relationship of lifetime productivity withmature weight and maturation rate in RedPoll cows, Anim. Prod. 39 (1984) 383−387.

[61] Meikle A., Kulcsar M., Chilliard Y., FebelH., Delavaud C., Cavestany D., ChilibrosteP., Effects of parity and body condition atparturition on endocrine and reproductiveparameters of the cows, Reprod. 127 (2004)727−737.

[62] Petit M., Agabriel J., État corporel desvaches allaitantes Charolaises : signification,utilisation pratique et relations avec la re-production, INRA Prod. Anim. 6 (1993)311−318.

[63] Prache S., Gordon I.J., Rook A.J., Foragingbehaviour and diet selection in domestic her-bivores, Ann. Zootech. 47 (1998) 335−345.

[64] Rémond B., Cissé M., Ollier A., Chilliard Y.,Slow release somatotropin in dairy heifers

510 F. Blanc et al.

and cows fed two levels of energy concen-trate. 1. Performance and body condition, J.Dairy Sci. 74 (1991) 1370−1381.

[65] Robelin J., Agabriel J., Malterre C.,Bonnemaire J., Changes in body compo-sition of mature dry cows of Holstein,Limousin and Charolais breeds during fat-tening. Skeleton, muscles, fatty tissues andoffal, Livest. Prod. Sci. 25 (1990) 199−215.

[66] Roussel S., Hemsworth P.H., Boissy A.,Duvaux-Ponter C., Effects of repeated stressduring pregnancy in ewes on the behaviouraland physiological responses to stressfulevents and birth weight of their offspring,Appl. Anim. Behav. Sci. 85 (2004) 259−276.

[67] Sauvant D., Schmidely P., Daudin J.J., Lesméta-analyses des données expérimentales :applications en nutrition animale, INRAProd. Anim. 18 (2005) 63−73.

[68] Schneider J.E., Energy balance and repro-duction, Physiol. Behav. 81 (2004) 289−317.

[69] Short R.E., Bellows R.A., Staigmiller R.B.,Berardinelli J.G., Custer E.E., Physiologicalmechanisms controlling anestrus and fertilityin postpartum beef cattle, J. Anim. Sci. 68(1990) 799−816.

[70] Sinclair K.D., Agabriel J., The adaptation ofdomestic ruminants to environmental con-straints under extensive conditions, Ann.Zootech. 47 (1998) 347−358.

[71] St-Pierre N.R., Invited review: Integratingquantitative findings from multiple studiesusing mixed model methodology, J. DairySci. 84 (2001) 741−755.

[72] Tichit M., Ingrand S., Dedieu B., BoucheR., Cournut S., Lasseur J., Moulin C.H., Lefonctionnement du troupeau : une interac-tion entre la conduite de l’éleveur et les com-portements reproductifs d’animaux, Renc.Rech. Ruminants 9 (2002) 103−106.

[73] Tichit M., Durant D., Kernés E., The roleof grazing in creating suitable sward struc-tures for breeding waders in agriculturallandscapes, Livest. Prod. Sci. 96 (2005)119−128.

[74] Veissier I., Capdeville J., Sarignac C., A par-tir de quelles bases peut-on concevoir desbâtiments respectueux du bien-être des an-imaux de rente, Renc. Rech. Ruminants 5(1998) 273−279.

[75] Vérité R., Chilliard Y., Effect of age of dairycows on body composition changes through-out the lactation cycle as measured with deu-teriated water, Ann. Zootech. 41 (1992) 118.

[76] Wiktorsson H., General plane of nutritionfor dairy cows, in: Broster W.H., Swan H.(Eds.), Feeding strategy for the high yield-ing dairy cow, Granada, Publ. Ltd, 1979,pp. 148−170.

To access this journal online:www.edpsciences.org