15
Restricted feeding of goats during the last third of gestation modies both metabolic parameters and behaviour Bérengère Laporte-Broux a,b , Christine Duvaux-Ponter a,b , Sabine Roussel a,b , Julie Promp a,b , Pascale Chavatte-Palmer c,d , Andrew A. Ponter c,d, a AgroParisTech UMR 791 Modélisation Systémique Appliquée aux Ruminants, 16 rue Claude Bernard, 75005 Paris, France b INRA UMR 791 Modélisation Systémique Appliquée aux Ruminants, 16 rue Claude Bernard, 75005 Paris, France c INRA UMR 1198 Biologie du Développement et Reproduction, Domaine de Vilvert, 78350 Jouy-en-Josas, France d Ecole Nationale Vétérinaire d'Alfort, UMR 1198 Biologie du Développement et Reproduction, 7 avenue du Général-de-Gaulle, 94704 Maisons-Alfort Cedex, France article info abstract Article history: Received 9 August 2010 Received in revised form 16 November 2010 Accepted 2 December 2010 Underfeeding of gestating dairy goats can occur for a number of reasons. If underfeeding is severe it can provoke pregnancy toxaemia which can lead to welfare problems and even mortality. Behaviour may also be modified in the context of underfeeding and it is important to integrate this information in management practices. The objectives of this experiment were to study the effect of restricted feeding during the last third of gestation on metabolism and behaviour of goats. Special attention was paid to the feed restricted group of goats to define characteristics which could be used to identify animals at risk before they develop pregnancy toxaemia. A total of 60 Alpine and Saanen dairy goats were used. Starting from 8 weeks before parturition the goats were allocated to one of two dietary treatments, control (C) or restricted (R). The C group was fed ad libitum (5% feed refusals) a TMR (C, n = 30) and the R group (R, n = 30) was given the same TMR but the quantity corresponded to 50% of the amount given to the C group between 8 and 4 weeks, 60% between 5 and 4 weeks, 70% between 4 and 3 weeks and 80% from 2 weeks to parturition. The R goats were also given free access to straw. Both metabolism and behaviour were modied by food restriction. The R goats put on less weight and their body condition score (BCS) decreased more steeply than the C goats during late gestation. Plasma glucose and β-hydroxybutyrate (BHB) were lower while non-esteried fatty acids (NEFA) were higher in the R goats compared to the C goats during the period of feed restriction. The R goats spent more time in activities involved with feeding and moving than the C goats. Four of the R goats developed pregnancy toxaemia as a result of dietary restriction. A principal component analysis (PCA) was performed on variables analysed before the start of dietary restriction: liveweight (LW), BCS, fasting plasma glucose, urea, NEFA and BHB. The four R animals that developed toxaemia were characterised by high NEFA and low plasma glucose together with low BCS and high urea before dietary restriction. This particular prole may therefore be used to determine which animals are at risk of developing pregnancy toxaemia. © 2010 Elsevier B.V. All rights reserved. Keywords: Restricted feeding End of gestation Behaviour Emotional reactivity Goat 1. Introduction Nutritional requirements during the last third of gestation are very high in small ruminants due to the high prolicacy of these animals. In goats, the conceptus acquires 80% of its birth weight in the last 2 months of gestation (Conway et al., 1996). This means that a pregnant goat's daily energy requirements just Livestock Science 138 (2011) 7488 Corresponding author. Ecole Nationale Vétérinaire d'Alfort, UMR 1198 Biologie du Développement et Reproduction, 7 avenue du Général-de-Gaulle, 94704 Maisons-Alfort Cedex, France. Tel./fax: +33 1 43 96 70 79. E-mail address: [email protected] (A.A. Ponter). 1871-1413/$ see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.livsci.2010.12.008 Contents lists available at ScienceDirect Livestock Science journal homepage: www.elsevier.com/locate/livsci

Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

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Page 1: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

Livestock Science 138 (2011) 74–88

Contents lists available at ScienceDirect

Livestock Science

j ourna l homepage: www.e lsev ie r.com/ locate / l ivsc i

Restricted feeding of goats during the last third of gestation modifies bothmetabolic parameters and behaviour

Bérengère Laporte-Broux a,b, Christine Duvaux-Ponter a,b, Sabine Roussel a,b, Julie Promp a,b,Pascale Chavatte-Palmer c,d, Andrew A. Ponter c,d,⁎a AgroParisTech UMR 791 Modélisation Systémique Appliquée aux Ruminants, 16 rue Claude Bernard, 75005 Paris, Franceb INRA UMR 791 Modélisation Systémique Appliquée aux Ruminants, 16 rue Claude Bernard, 75005 Paris, Francec INRA UMR 1198 Biologie du Développement et Reproduction, Domaine de Vilvert, 78350 Jouy-en-Josas, Franced Ecole Nationale Vétérinaire d'Alfort, UMR 1198 Biologie du Développement et Reproduction, 7 avenue du Général-de-Gaulle, 94704 Maisons-Alfort Cedex, France

a r t i c l e i n f o

⁎ Corresponding author. Ecole Nationale VétérinairBiologie du Développement et Reproduction, 7 avenue94704 Maisons-Alfort Cedex, France. Tel./fax: +33 1 43

E-mail address: [email protected] (A.A. Ponter)

1871-1413/$ – see front matter © 2010 Elsevier B.V.doi:10.1016/j.livsci.2010.12.008

a b s t r a c t

Article history:Received 9 August 2010Received in revised form 16 November 2010Accepted 2 December 2010

Underfeeding of gestating dairy goats can occur for a number of reasons. If underfeeding issevere it can provoke pregnancy toxaemia which can lead to welfare problems and evenmortality. Behaviour may also be modified in the context of underfeeding and it is important tointegrate this information in management practices. The objectives of this experiment were tostudy the effect of restricted feeding during the last third of gestation on metabolism andbehaviour of goats. Special attention was paid to the feed restricted group of goats to definecharacteristics which could be used to identify animals at risk before they develop pregnancytoxaemia. A total of 60 Alpine and Saanen dairy goats were used. Starting from −8 weeksbefore parturition the goats were allocated to one of two dietary treatments, control (C) orrestricted (R). The C group was fed ad libitum (5% feed refusals) a TMR (C, n=30) and theR group (R, n=30) was given the same TMR but the quantity corresponded to 50% of theamount given to the C group between−8 and−4 weeks, 60% between−5 and−4 weeks, 70%between−4 and−3 weeks and 80% from−2 weeks to parturition. The R goats were also givenfree access to straw. Both metabolism and behaviour were modified by food restriction. The Rgoats put on less weight and their body condition score (BCS) decreased more steeply than theC goats during late gestation. Plasma glucose and β-hydroxybutyrate (BHB) were lower whilenon-esterified fatty acids (NEFA) were higher in the R goats compared to the C goats during theperiod of feed restriction. The R goats spent more time in activities involved with feeding andmoving than the C goats. Four of the R goats developed pregnancy toxaemia as a result ofdietary restriction. A principal component analysis (PCA) was performed on variables analysedbefore the start of dietary restriction: liveweight (LW), BCS, fasting plasma glucose, urea, NEFAand BHB. The four R animals that developed toxaemiawere characterised by high NEFA and lowplasma glucose together with low BCS and high urea before dietary restriction. This particularprofile may therefore be used to determine which animals are at risk of developing pregnancytoxaemia.

© 2010 Elsevier B.V. All rights reserved.

Keywords:Restricted feedingEnd of gestationBehaviourEmotional reactivityGoat

e d'Alfort, UMR 1198du Général-de-Gaulle,96 70 79..

All rights reserved.

1. Introduction

Nutritional requirements during the last third of gestationare very high in small ruminants due to the high prolificacy ofthese animals. In goats, the conceptus acquires 80% of its birthweight in the last 2 months of gestation (Conway et al., 1996).Thismeans that apregnant goat's daily energy requirements just

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75B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

before parturition can be increased by 2.5 compared to thoseobserved for the same animal in early gestation (INRA, 1988).

In order to cover the requirements for foetal growth, thegoatmust either eatmore ormobilise its reserves. Food intakecan be low at the end of gestation due to: compression of therumen by the foetuses, under-development of the rumenpapillae, which reduces the rate at which the products offermentation-synthesis are absorbed (Mayer et al., 1986),breeding of goats to produce kids in thewinter, the use of poorquality conserved feedstuffs, feed cost-cutting by farmers andfinally, goats can be particularly aggressive at the food troughif feed resources are limited, so that some individuals may getvery little access to food (Conway et al., 1996).

Damhealth can be impacted negatively by feed restriction.Small ruminants are particularly prone to developing preg-nancy toxaemia at the end of gestation in situations of dietaryrestriction and it can be a major problem (Mavrogianni andBrozos, 2008).

Ketotic animals are usually in poor body condition, showdepression and can suffer from selective anorexia. Theanimals often isolate themselves from the rest of the herd.At a later stage neurological signs can develop: head and necktremors, excessive salivation, wandering, lack of blink-to-threat reflex, unusual head positioning and even blindness.Finally, coma and death occur (Sargison, 2007). If not treatedrapidly, animals in an advanced stage of the disease are likelyto die.

Goat feeding behaviour has been studied extensively. Oneaspect of feeding behaviour which has been investigated isthe ability of the goat to sort between different foodstuffs.This is influenced by the nutritional value of the diet as well asits availability. Barroso et al. (2000) have shown that whenthe food offered is plentiful but of poor nutritive value thegoat will spend a long time sorting between the differentcomponents of the diet. However, if the quantity of feedavailable is reduced, the goat will eat all that is available,including foodstuffs that are not usually consumed. More-over, agonistic activity between goats is reduced in responseto poor quality diets whereas it is increased with increasingfood quality. This may be due a large amount of time spentsorting poor quality diets, in contrast to the relatively shorttime when quality is high. Competition and aggressivebehaviour at the feeding trough probably induce, at least inanimals of low social rank, high levels of stress, which coulddecrease productivity and welfare (Bouissou et al., 2001). Tohighlight the presence of chronic stress, the modification ofemotional reactivity can be studied as shown in calves underenvironmental instability (Boissy et al., 2001). Emotionalreactivity can be assessed by exposing goats to social isolation(Fisher andMatthews, 2001) or novelty (Roussel et al., 2005).

The objective of the present experiment was to study theeffect of restricted feeding on themetabolism and behaviour ofgoats during the last third of gestation. Special attention waspaid to the feed restricted group to try and define character-istics which could be used to identify animals at risk ofdeveloping pregnancy toxaemia and to prevent its occurrence.

2. Materials and methods

The present study was carried out according to Frenchlegislation on animal experimentation (code rural: articles R

214-87 to R214-94) in line with the European Convention forthe Protection of Vertebrates used for Experimental and otherScientific Purposes (European Directive 86/609). The scientistin charge of the experiments was licensed to performexperiments on animals and the staff who applied theexperimental procedures had attended a special courseapproved by the French Ministry of Agriculture.

2.1. Animals and diets

Sixty Alpine and Saanen dairy goats were used for theexperiment. Goats were synchronized prior to mating so thatparturition occurred over a 10-day period. The goats used inthe experiment were housed on straw bedding. Following AI,all the goats were given free access to the same total mixedration (TMR; beet pulp silage 35%, perennial ryegrass hay25%, lucerne hay 29%, barley 10% and a mineral and vitaminmix for 1% on a dry matter basis), to water and to mineralfortified salt licks (containing Na 370 g, Mg 3 g, Zn 0.9 g, Mn0.75 g, Cu 0.15 g, Fe 0.4 g, I 0.1 g, Co 0.06 g, and Se 0.015 g/kg).The TMR contained 50% dry matter.

Gestation was confirmed at 60 days by ultrasonography.Starting at 89±3 days of gestation, the goatswere allocated toone of two dietary treatments: control (C) or restricted (R)according to breed, age, liveweight (LW) and body conditionscore (BCS). Litter size was not directly used because it couldnot be determined precisely at the time when pregnancydiagnosis was performed. The composition of the TMR wasmodified in the lastweeks of gestation to take into account theproportionally faster increase in protein requirementscompared to energy. The composition and proximate analysisof the diets are given in Table 1. Each dietary treatment groupwas sub-divided into two on the basis of LW. A heavy (C, 82±2.5 kg and R, 83±2.5 kg) and a light group (C, 61±1.6 kg andR, 62±1.4 kg) were defined in order to reduce aggressionbetween light and heavy R goats at the feeding trough and toadjust more precisely the amount of food given in relation toLW. All the R goats were individually blocked at the feedingtrough by a neck lock for 30 min during feeding to avoidcompetition at the trough and to ensure that all goats wereable to eat undisturbed. The C group (n=30) was fed adlibitum (5% feed refusals) the above described TMR for the lastthird of gestation and theR group (n=30)was given the sameTMRbut at a lower level. The quantity givenwas adjusted eachweek from an initial 50% of the amount given to the controlsubgroup of similar LW, with a gradual increase of up to 80%from −2 weeks to parturition. Indeed, when 3 goats pre-sented symptoms of toxaemia in the restricted subgroups(physiology measurements, see below), it was decided priorto the experiment to increase progressively the amount offeed for ethical reasons. Therefore, each restricted subgroupreceived 50% of the amount of feed given to their pair-fedcontrol subgroup for 4 weeks, 60% for 1 week, 70% for 1 weekand80% the last 2 weeks of pregnancy. In addition, the R groupreceived ad libitum barley straw (3.13 MJ Net energy, 24 gPDIN (true Intestinal Digestible Protein, when fermentable Nis the limiting factor), 46 g PDIE (true Intestinal DigestibleProtein, when fermentable Energy is the limiting factor),420 g crude fibre, 3.5 g calcium and 1.0 g phosphorus, per kgDM). This was to limit behavioural problems (such as eatinghair) that can be associated with hunger and to reduce as

Page 3: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

Table 1Composition and proximate analysis of the diets given to dairy goats duringthe experimental period.

−8 to−4 weeks 1

−4 to−2 weeks

−2 to 0 Afterparturition

Composition (% DM)Sugar beet pulp 35 30 30 28Perennial ryegrasshay

25 25 25 17

Lucerne hay 29 29 29 32Proteinconcentrate

0 5 10 17

Barley 10 10 5 5Vitamin andmineral mix

1 1 1 1

Nutrients (/kg dry matter)Net energy (MJ) 5.7 5.6 5.5 5.7PDIN (g) 72 75 77 84PDIE (g) 82 84 86 90Crude fiber (g) 292 285 287 270Calcium (g) 9.0 8.5 8.7 8.8Phosphorus (g) 2.0 2.3 2.4 2.8

NEL = Net energy for maintenance and lactation.PDIN= true Intestinal Digestible Protein, when fermentable N is the limitingfactor.PDIE = true Intestinal Digestible Protein, when fermentable Energy is thelimiting factor.

1 weeks in reference to parturition (parturition=0).

76 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

much as possible the psychological stress due to feedrestriction (Mason, 1971).

Finally, all the goats received the equivalent of 40 g perhead and per day mono-propylene glycol (DIFAGRI PICOT SA,France) mixed in the TMR, to limit the onset of ketosis. Thediets were given twice daily at 07:00 h and 15:00 h untilparturition, thereafter all the goats were fed a TMR designedto cover the requirements of early lactation (INRA, 1988).

The nutrition value of the diet was estimated usingequations (AFZ-INRA Tables, 2002) based on the chemicalcomposition of each feedstuff measured using methodsapproved by the Association Française de Normalisation andthe European Commission (AFZ-INRA Tables, 2002).

2.2. Treatment of goats which developed pregnancy toxaemia

During the experiment, four goats in the R groupdeveloped pregnancy toxaemia as assessed by physiologicalmeasurements (see below). The goats were removed fromthe experiment and each one was treated with Energidex(50 mL i.v. per day for 5 days, Energidex contains dextrose,24 g; sorbitol, 14 g; benzylic alcohol, 0.9 mL; excipient q.s.p.100 mL (Vetoquinol, France)). The ketotic goats were fed thesame quantity of feed as C group.

2.3. Measurements

The goats were weighed before the beginning of theexperiment and weekly thereafter. Body condition was scoredby the sameperson before the beginning of the experiment andevery other week thereafter. The goats were also weighed 24 hpost-parturition and the kids were weighed at birth. Blood

samples were collected weekly from the goats starting beforethe beginning of the dietary treatment period until afterparturition (parturition−8 to+6 weeks). Bloodwas collected(9 mL) by jugular venipuncture into heparinised tubes (10 mL,135 USP U lithium heparin, (Venosafe, Terumo, Belgium)) inthe morning, before feeding. The blood was immediatelycentrifuged at 2000×g for 15 min at 4 °C after collection.Plasma was removed and stored at −20 °C until required foranalysis. Plasma was assayed for glucose, NEFA, BHB and ureaonweekly samples. Three sampleswere selected for insulin andleptin measurements: before treatment, −4 weeks and−1 week prior to parturition. Glucose, NEFA and BHB wereassayed on the day immediately after sampling so that theresults could be used to identify goats developing pregnancytoxaemia (lowglucose associatedwithhighNEFAandhighBHBin addition to a reduction in feed intake).

The results concerning the kids born to these goats havebeen presented elsewhere (Laporte et al., 2009).

2.4. Assays

Weekly plasma samples were analysed by photometricmethods for glucose (Glucose-RTU®, BioMérieux, Lyon,France), NEFA (NEFA C®, Wako Chemicals, Neuss, Germany),BHB (method adapted from Barnouin et al., 1986) and urea(Urea-kit S®, BioMérieux, Lyon, France).

Insulin and leptin were analysed by radioimmunoassay,respectively based on a RIA rat insulin kit (Millipore,Molsheim, France; 100% of specificity for sheep insulin) andovine leptin (Delavaud et al., 2000). Inter-assay coefficients ofvariation were 4.3% at 3.47 mmol/L, 12.7% at 0.31 mmol/L,6.5% at 0.82 mmol/L and 8.3% at 2.99 mmol/L for glucose,NEFA, BHB and urea respectively. Intra-assay coefficients ofvariation were 9.7% at 153.8 pmol/L for insulin and 4.0% at57.45 ng/mL for leptin.

The plasma metabolites were analysed in a laboratorywhich performs, on a routine basis, the assays required by theclinicians for the farm animal clinics at the Alfort VeterinarySchool. An in-house control plasma was systematically usedas a quality control.

2.5. Behavioural measurements

The procedures used in all the situations were designed toensure that the handling protocol was standardized.

2.5.1. Time budgetGoats were continuously filmed for two periods of 12 h

(8:00 h to 20:00 h), 7 weeks and1 weekbefore parturition. Thecameras were placed on the wall in front of the goats. Due tocoat colour, it was difficult to identify the Alpine goats.Therefore only the white Saanen goats were individuallyidentified with blue paint and their behaviour observed(C, n=14 and R, n=14). Video recordings were analysed byscan sampling every 2 min which is as accurate as continuousrecordingwhen studyingmajor activities (standing, walking...)(Mitlohner et al., 2001). All the goatswere observedat the sametime and the different behaviours were noted over 5 s periodsfor each individually identified goat. The following variableswere analysed: the percentage of time spent lying down,standing immobile (no movement of the limbs), standing at

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neck-lock (either feeding or not), feeding (TMR or straw) andwalking. The number of agonistic behaviours were recorded(attack i.e. threatening, chasing, butting and avoiding behav-iour). In addition, the number of self-grooming and positiveinteractions (nuzzling, sniffing or rubbing a conspecific) wasalso noted (see Andersen et al., 2008). The time the goats spentruminating was not analysed due to the difficulties encoun-tered when trying to observe the animals when they were notfacing the camera.

2.5.2. Novel arena and novel object testsThe novel arena and object tests were performed in a

straw floored, 3.1 m×4.3 m, empty enclosure built withlaminated wood panels. This enclosure was located in aroom which is not used during normal management of thefarm. A camera was placed above the test arena. The novelarena test was performed 7 and 2 weeks prior to parturitionand again 2 weeks after parturition. Each goat was gentlypushed into the novel arena and the test lasted 3 min. Thegoat was then returned to the corridor while a road traffichazard cone was placed in the centre of the novel arena. Thegoat was then reintroduced into the novel arena for a further3 min. At the end of the tests, the goats were returned to theirhome pen. The films were subsequently analysed using theObserver 5.0® Software System for Behavioral Research(Noldus Information Technology, Wageningen, TheNetherlands). A total of 28 goats were tested 7 weeks priorto parturition (C, n=14 and R, n=14), 25 goats 2 weeksprior to parturition (C, n=12 and R, n=13) and 22 goats2 weeks after parturition (C, n=10 and R, n=12). Thefollowing variables were analysed for the novel arena test:the percentage of time spent immobile (no movement of thelimbs), walking, climbing (two limbs on the wall and twolimbs on the floor), the percentage of time spent in theentrance area (1 m×1 m), the number of vocalisations andthe number of goats performing defecations and mictions.The number of times that the novel object was sniffed(muzzle b5 cm for the object) and the latency before the firstsniff were also recorded for the novel object test.

2.6. Statistical analysis

Statistical analysis was performed using the SPADprogramme (CISIA, 1996) for principal component analysisand SAS (SAS Institute Inc., 2000) for the other procedures.When assumptions of homogeneity of variance and normaldistribution of the residuals were not confirmed, a ln(x+1)or 1/(x+1) or √x transformation was performed beforecarrying out the analyses. When the transformation did notallow the hypotheses to be confirmed, a Wilcoxon MannWhitney (non-parametric test) was used. Results are pre-sented as Lsmean±SEM. A Pb0.05 was considered to bestatistically significant and a Pb0.10 a trend.

The effect of treatment on litter size and litter weight wastested using the GLM procedure of SAS. Total weight gainduring gestation (goat plus conceptus) and goat LW lossduring the period of dietary treatment were analysed usingthe GLM procedure of SAS where litter weight was used as acovariate.

Liveweight and BCS changes were analysed using the PROCMIXED procedure of SAS for repeated measures over time

including a random female effect. The effects of time, dietaryregimen and their interactionwere tested using litterweight asa covariate. The LW and BCS in pre-experimental period werealso used as covariates in the LW and BCSmodels, respectively.

The metabolite and hormone data were also analysedusing the PROC MIXED procedure of SAS for repeatedmeasures (as above).

A principal component analysis (PCA) was performed onthe data obtained from the R group of goats (23 healthy and 4toxaemic goats) at −9 week prior to parturition, i.e., beforethe start of the period of dietary restriction. The aim was toascertain which factors could be correlated with the risk ofdeveloping pregnancy toxaemia. The variables analysedwere: LW, BCS, plasma glucose, urea, NEFA and BHB. Thequality of the representation of the individuals on each axis(cos2) and their dispersion on axis 1 and axis 2 were analysed.

The GLM procedure (SAS Institute Inc., 2000) was used toanalyse the time budget, novel arena and novel object data.The number of goats performing defecations and mictionsduring the novel arena and object tests was analysed using χ2.

Using SAS, ‘estimates’ were calculated in order to allowcomparisons time point by time point.

3. Results

3.1. Animal husbandry measurements

Even though pregnancy diagnosis was performed, 4control goats were found to be non-pregnant at the expecteddate of parturition or had aborted and somegoats experiencedan accident during the experiment (2 control and 2 restrictedgoats) and were therefore withdrawn from the study. Inaddition, 4 R goats developed pregnancy toxaemia. Therefore,25 goats in the C group and 23 goats in the R group were usedin the analyses of length of gestation, litter size and litterweight and the evolutions in LW, BCS, plasmametabolites andhormones during the experiment.

During the first 4 weeks of dietary treatment the averagequantities of diet ingested were: for light control goats: 1.9 kgDM/day, for heavy control goats: 2.4 kg DM/day, for lightrestricted goats: 1.0 kg DM/day and for heavy restricted goats:1.3 kg DM/day. When straw intake (0.4 kg DM/day) wasintegrated into the calculations, the energy intake of therestricted goats was 60% of that of the controls. During thelast 4 weeks of dietary treatment, the average quantitiesingested were: for light control goats: 1.9 kg DM/day, forheavy control goats: 2.2 kg DM/day, for light restricted goats:1.3 kg DM/day and for heavy restricted goats: 1.6 kg DM/day.When straw intake (0.4 kg DM/day) was integrated into thecalculations, energy intake of the restricted goats was 80% ofthat of the controls.

3.1.1. Length of gestation, litter size and litter weightThere was no statistical effect of dietary regimen on the

length of gestation (C, 151±2 days vs. R, 151±2 days,respectively), litter size (C, 2.1±0.2 vs. R, 2.0±0.1, respectively)nor litter weight (C, 8.56±0.60 kg vs. R, 8.63±0.44 kg,respectively). Kid mortality rate (mummified foetus, still-birthor death in first 48 h) was not different between groups (datanot shown).

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78 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

3.1.2. Goat LW and BCS changes

3.1.2.1. Before parturition. The evolution in goat LW prior toparturition is shown in Fig. 1a. There was no differencebetween groups before the start of the experimental periodbut after the introduction of the dietary regimens, the LW ofthe C goats was systematically higher than that of the R goats(Pb0.001). In addition, the litter weight and basal LWcovariates affected the evolution in LW prior to parturition(Pb0.01 and Pb0.001, respectively). Across treatments, goatLW increased more in animals which produced heavy litterscompared to goats which produced light litters. In addition,goats which had a high basal LW gained more weight prior toparturition than goats which had a low basal LW.

The evolution in BCS during the experimental period isshown in Fig. 1b. There was no difference between groups

a)

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Fig. 1. a) Liveweight and b) body condition score (BCS) measurements during thetoxaemia). One of two dietary regimens were used between−8 weeks to parturitionR group (n=23) was given the same TMR but the quantity corresponded to 50% (foamount given to the C group. Differences time point by time point between treatmperiod is indicated with an arrow.

before the start of the experimental period but after theintroduction of the dietary regimens, BCS was affected bytreatment (CNR, Pb0.001). In addition, there was an effect oftime (decrease then increase in BCS, Pb0.05) and BCS beforetreatment on the evolution in BCS prior to parturition (acrosstreatments, goat BCS decreased more in animals whichstarted with a high BCS before dietary treatment comparedto goats which started with a low BCS, Pb0.001). There wasno effect of litter weight or an interaction regimen×time onBCS.

A summary of the changes in weight during the gestationperiod and at parturition is given in Fig. 2. There was an effectof dietary regimen on total weight gain during pregnancy (C,7.54±0.88 kg vs. R, 1.44±1.26 kg, respectively, Pb0.01) andweight loss during the dietary treatment period (C, −0.43±0.80 kg vs. R, −6.65±0.92 kg, respectively, Pb0.001).

-4 -3 -2 -1 0

re parturition

RestrictedControl

******

******

-4 -3 -2 -1 0

re parturition

RestrictedControl

****

period preceding parturition (−8 weeks to parturition) in healthy goats (no: C group (n=25) was fed a TMR ad libitum for the last third of gestation andr 4 weeks), 60% (for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of theents are shown, **Pb0.01 and ***Pb0.001. The start of the dietary treatment

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79B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

3.1.2.2. Postpartum. The liveweight of the animals during thepostpartum is shown in Fig. 3a. The liveweight of the C goatswas initially higher than that of the R goats (Pb0.05).Although the difference gradually decreased, it was stillsignificant 5 weeks after parturition.

The body condition score postpartum is shown in Fig. 3b.BCS was initially higher in C goats than in R goats (Pb0.05)and the difference had disappeared by 5 weeks postpartum.

3.2. Physiological responses

3.2.1. Blood measurements

3.2.1.1. Pre-partum. Glucose concentrations gradually de-creased in both groups during the experimental period(Pb0.001, Fig. 4a) and CNR (Pb0.001). The covariate litterweight had a significant effect on glucose concentrations(Pb0.01),whereheavy littershad lower glucose concentrationsthan light litters.

PlasmaNEFA concentrations increasedwith timeduring theexperimental period (Pb0.001, Fig. 4b). There was an effect ofdietary regimen (CbR, Pb0.001) and an interaction betweenregimen and time (Pb0.001). The NEFA concentrationsincreased more in R goats compared to C goats. The covariatelitter weight had a significant effect on NEFA concentrations(Pb0.01), where heavy litters had higher NEFA concentrationsthan light litters.

Plasma BHB concentrations increasedwith time during theexperimental period (Pb0.001, Fig. 4c). There was an effect ofdietary regimen (CNR, Pb0.01) and an interaction betweenregimen and time (Pb0.001). The BHB concentrationsincreased more in C goats compared to R goats. The covariate,litter weight, tended to have an effect on BHB concentrations

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Live

wei

ght (

kg)

LW at AI LW atparturition

LW at -8wkparturition pa

NS

NS

**

Fig. 2. Goat liveweight (LW), litter weight and changes in goat LW during the pertreatment up to 24 h postpartum in healthy goats (no toxaemia). One of two dietaryfed a TMR ad libitum for the last third of gestation and R group (n=23) was given1 week), 70% (for 1 week) and 80% (for 2 week) of the amount given to the C group.***Pb0.001.

(Pb0.10), where heavy litters had lower BHB concentrationsthan light litters.

Plasma urea concentrations increased with time duringthe experimental period (Pb0.001, Fig. 4d) and there was aneffect of dietary treatment (CNR, Pb0.01).

Plasma insulin concentrations were higher in the R groupthan the C group prior to the start of treatment (Pb0.05,Fig. 5a) but this effect was reversed 4 weeks beforeparturition (Pb0.05). The concentrations of insulin decreasedwith time (Pb0.001).

There was no difference between groups for the leptinconcentrations prior to the start of the dietary treatment. Fourweeks before parturition, leptin concentrations were higherin the C group compared to the R group (Pb0.05, Fig. 5b). Theconcentrations of leptin decreased with time (Pb0.001).

3.2.1.2. Postpartum. Plasma glucose concentrations graduallyincreased in both groups during the postpartum period(Pb0.001, Fig. 6a) and RNC (Pb0.001) while NEFA concen-trations gradually decreased with time postpartum (Pb0.001,Fig. 6b) and CNR (Pb0.01). There was a trend for BHBconcentrations to be higher in the C group compared to the Rgroup (between Pb0.1, Fig. 6c). There were no consistentdifferences in plasma urea concentrations postpartum(Fig. 6d).

3.2.2. Principal component analysis of pregnancy toxaemiaThe results of the PCA are presented in Fig. 7. The variables

for each axis are shown and the variability of each variableexplained by the axis is also given (r2=variable–factorcorrelation coefficient). The first two principal components(PC 1 and 2) accounted for 29% and 25% of the variation in thedataset. PC 1 was mainly explained by high plasma glucose(r2=0.89) and low plasma NEFA (r2=−0.81) and PC 2 by

Restricted

Control

LW atrturition+24h

Litterweight

Goat LW change-8wk to

parturition

Goat LW changeAI to

parturition

**

NS *****

iod between: artificial insemination (AI) up to 24 h postpartum and start ofregimens were used between−8 weeks to parturition: C group (n=25), wasthe same TMR but the quantity corresponded to 50% (for 4 weeks), 60% (forDifferences between treatments are shown, NS non-significant, **Pb0.01 and

Page 7: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

a)

50

55

60

65

70

75

80

0 1 2 3 4 5 6 7

Week after parturition

Live

wei

ght (

kg)

RestrictedControl

***

*****+ *

b)

2.6

2.65

2.7

2.75

2.8

2.85

2.9

2.95

3

0 1 2 3 4 5 6 7

Week after parturition

BC

S (

scal

e 0-

5)

RestrictedControl

*+

Fig. 3. a) Liveweight and b) body condition score (BCS) measurements during the period postpartum (parturition to +6 weeks) in healthy goats (no toxaemia).One of two dietary regimens were used between −8 weeks to parturition: C group (n=25) was fed a TMR ad libitum for the last third of gestation and R group(n=23) was given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60% (for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of the amountgiven to the C group. After parturition the same TMR, designed to cover the requirements for lactation, was given to all the goats. Differences time point by timepoint between treatments are shown, +Pb0.1, *Pb0.05, **Pb0.01 and ***Pb0.001.

80 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

high BCS (r2=0.77) and low urea (r2=−0.64). The goatswhich went on to show clinical signs of pregnancy toxaemia(goats: 4026, 5008, 5123 and 6110) aremainly represented inthe same quadrant of the PCA whereas the other goats, whichdid not go on to develop toxaemia, are mainly represented inthe remaining quadrants.

3.3. Behavioural responses

3.3.1. Time budgetOne week after the start of the experimental period

(−7 weeks in relation to parturition) the R goats spent lesstime standing immobile (PN0.05), more time walking(PN0.001) and more time standing at neck-lock (PN0.001)

compared to C goats (Table 2). The increase in time spent inthe neck-lock was explained by an increase in feeding time(Pb0.001) in R goats compared to C goats. When studyingmore specifically the total time spent feeding, R goats ate theirTMR for 18% of the time and straw for the remaining time. Nodifference in agonistic behaviour was observed betweendietary treatments. However, the number of self-groomingand positive interactions was lower in R goats compared to Cgoats (Pb0.001).

After 7 weeks of dietary treatment (−1 week beforeparturition), R goats spent more time standing immobile(Pb0.01), more time walking (Pb0.001) and less time lyingdown (Pb0.05) compared to C goats (Table 2). However,there was no effect of dietary treatment on time spent

Page 8: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

a)

2

2.2

2.4

2.6

2.8

3

3.2

3.4

3.6

3.8

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

gluc

ose

(mm

ol/L

)

RestrictedControl

****

******

**********

Dietarytreatment

b)

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

NE

FA

(m

mol

/L)

RestrictedControl

******

***

******

***

***Dietarytreatment

c)

0.6

0.7

0.8

0.9

1

1.1

1.2

1.3

1.4

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

BH

B (

mm

ol/L

)

RestrictedControl

******

***

Dietarytreatment

Fig. 4. Plasma concentrations of a) glucose, b) NEFA, c) BHB and d) urea during the period preceding parturition (−8 weeks to parturition) in healthy goats (notoxaemia). One of two dietary regimens were used between−8 weeks to parturition: C group (n=25), was fed a TMR ad libitum for the last third of gestation andR group (n=23) was given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60% (for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of theamount given to the C group. Differences time point by time point between treatments are shown, +Pb0.1, *Pb0.05, **Pb0.01 and ***Pb0.001. The start of thedietary treatment period is indicated with an arrow.

81B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

Page 9: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

d)

2

2.5

3

3.5

4

4.5

5

5.5

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

urea

(m

mol

/L)

RestrictedControl

+**

*

***

Dietarytreatment

Fig. 4 (continued).

82 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

standing at neck-lock or feeding. When studying morespecifically the total time spent feeding, R goats ate theirTMR for 44% of the time and straw during the remaining time.The number of attacks tended to be lower in R goatscompared to C goats (Pb0.10).

3.3.2. Novel arena and novel objectOne week after the start of the restriction period

(−7 weeks prior to parturition), the R goats spent moretime in the entrance area (Pb0.05) and walked more(Pb0.05) during the novel arena test than the C goats(Table 3). No effect of dietary treatment was observed duringthe novel object test.

Two weeks prior to parturition, while no differences wereobserved during the novel arena test, the R goats sniffedmoreoften the novel object (Pb0.05), tended to sniff it morequickly (Pb0.10) and spentmore timewalking (Pb0.05) thanC goats during the novel object test.

After parturition no differences were observed betweentreatments.

4. Discussion

Although the LW of the goats was modified by thetreatment, it is interesting to note that the weight of thelitter in the two treatment groups was the same. These resultsconfirm those of Celi et al. (2008) in goats and Petterson et al.(1993) and Simitzis et al. (2009) in sheep. However, lowerbirth weights have been observed in sheep and goatsunderfed in late-pregnancy (Alexander, 1978; Koritniket al., 1981; Bajhau and Kennedy, 1990; Oliver et al., 2001;Borwick et al., 2003; Husted et al., 2007). In addition, someauthors have reported that there are modifications in organgrowth and overall foetal development following restrictedfeeding during pregnancy (Koritnik et al., 1981; Greenwoodet al., 1999). In the present experiment, the foetal compart-ment seemed to have been protected at the expense of thedam. However, when only the twin and triplet bearing goatswere studied, the birth weight of male kids born to restricted

goats was reduced compared to controls (Laporte et al.,2009), emphasizing the importance of taking into accountlitter size when studying the effect of feed restriction duringpregnancy on the offspring.

The difference between LW at the beginning of treatmentand LW 24 h postpartum indicates that the feed restrictedgoats lost on average 6.65 kg (≈10% of initial LW) betweenthe start of treatment and 24 h after parturition whereas thecontrols lost the negligible amount of 0.43 kg (b1% of initialLW). These results indicate that the requirements for thecontrol goats were met during the treatment period (stabledam LW) whereas the restricted goats were forced tomobilise body reserves because requirements were notcovered. Sahlu et al. (1995) have produced similar results.They showed that dairy goats gained very little LW between90 days of pregnancy and parturition. The metabolicenvironment at the end of gestation may result in theredirection of nutrients towards the conceptus and thereforedam LW gain at the end of pregnancy may be physiologicallydifficult to obtain.

4.1. Physiological responses

The decrease observed in plasma glucose and the increasein plasma NEFA during dietary restriction confirms thatrequirements were not covered for the R goats (Sykes andField, 1972; Schlumbohm and Harmeyer, 2008). The responseof the animals was very rapid, since within 1 week of startingthe dietary treatments there was already a differencebetween groups. Conway et al. (1996) showed that when asevere dietary restriction (35% of metabolisable energyrequirements for the last third of gestation) was started ingoats at about the same stage of gestation, a difference inglucose concentrations appeared, but only after 4 weeks. Thedifference observed between experiments may be due to thefact that in the present experiment glucose concentrationswere higher to start with compared to Conway et al. (1996).The change in plasma glucose caused by restricted feedingwas relatively small compared to the change observed in

Page 10: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

a)

2

7

12

17

22

27

32

37

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

insu

lin (

pmol

/L)

RestrictedControl

*

*

Dietarytreatment

b)

0

1

2

3

4

5

6

-9 -8 -7 -6 -5 -4 -3 -2 -1 0

Week before parturition

Pla

sma

lept

in (

ng/m

L)

RestrictedControl

*Dietarytreatment

Fig. 5. Plasma concentrations of a) insulin and b) leptin during the period preceding parturition (−8 weeks to parturition) in healthy goats (no toxaemia). One oftwo dietary regimens were used between−8 weeks to parturition: C group (n=25), was fed a TMR ad libitum for the last third of gestation and R group (n=23)was given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60% (for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of the amount given to theC group. Differences time point by time point between treatments are shown, *Pb0.05. The start of the dietary treatment period is indicated with and arrow.

83B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

NEFA concentrations. Glucose concentrations are maintainedwithin a very tight range due to its essential role inmetabolism. NEFA concentrations, however, were increased5-fold in the restricted group as they become a major energysource when requirements are not covered. The increase inthe amount of feed given to the R group of goats in the last4 weeks of gestation (60%, 70% and then 80% of controls) hada very marginal effect on glucose concentrations but a largeeffect on NEFA concentrations. This is probably due to acombination of several factors: reduced lipid mobilisationdue to more feed being ingested and improved NEFAoxidation due to higher availability of glucose.

Plasma ketone bodies (BHB) originate from two sources:metabolism of butyric and acetic acid in the wall of the rumenand incomplete oxidation of NEFA in the Krebs cycle. In

the present experiment the former source appears to bepredominant since BHB concentrations were higher in Ccompared to R goats. Harmeyer and Schlumbohm(2006) havepreviously shown that lipidmobilisation causes an increase inBHB and that liver production of ketone bodies is greater thanthat of the rumen epithelium in restricted feeding. Thisindicates that in their experiments glucose supply wasprobably more limiting than in the present experiment. TheBHB concentrations in the present experimentwere similar tothose found by others (0.4–1.2 mmol/L, Ramin et al., 2005)but significantly lower than concentrations associated withpregnancy toxaemia (4–5 mmol/L, Ford et al., 1990 andHenzeet al., 1998).

In the present experiment urea concentrations werehigher in the controls compared to restricted goats. This

Page 11: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

a)

2

2.2

2.4

2.6

2.8

3

3.2

3.4

3.6

3.8

4

0 1 2 3 4 5 6 7

Week after parturition

Pla

sma

gluc

ose

(mm

ol/L

)

RestrictedControl

***

******

+

b)

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0 1 2 3 4 5 6 7

Week after parturition

Pla

sma

NE

FA (

mm

ol/L

)

RestrictedControl

+

+

****

**

*

c)

1

1.5

2

2.5

3

0 1 2 3 4 5 6 7

Week after parturition

Pla

sma

BH

B (

mm

ol/L

)

RestrictedControl

*+

++

Fig. 6. Plasma concentrations of a) glucose, b) NEFA, c) BHB and d) urea during the period postpartum (parturition to 6 weeks) in healthy goats (no toxaemia). Oneof two dietary regimens were used between −8 weeks to parturition: C group (n=25), was fed a TMR ad libitum for the last third of gestation and R group(n=23) was given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60% (for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of the amountgiven to the C group. After parturition the same TMR, designed to cover the requirements for lactation, was given to all the goats. Differences time point by timepoint between treatments are shown, +Pb0.1, *Pb0.05, **Pb0.01 and ***Pb0.001.

84 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

Page 12: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

d)

2

3

4

5

6

7

8

0 1 2 3 4 5 6 7

Week after parturition

Pla

sma

urea

(m

mol

/L)

RestrictedControl

*

Fig. 6 (continued).

85B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

may reflect the fact that the R goats had both a lower N intakebut also recycled more N since they spent more time feedingand therefore probably salivated more (Table 2).

4.2. Pregnancy toxaemia

In the present experiment four animals in the R groupshowed clinical signs of pregnancy toxaemia. They were allcarrying 3 or 4 foetuses. They showed a very similar pattern;lowered glucose, elevated NEFA and low BCS and high urea

6129

6110

5123

5077

50165008

4063

4026

401

3145

2069

-4

-3

-2

-1

0

1

2

-5 -4 -3 -2 -1

PC1 (29%, high gluc

PC

2 (2

5%, h

igh

BC

S a

nd lo

w u

rea)

Fig. 7. Aprincipal component analysiswasperformedonparametersmeasured ingoatsa dietary restriction prior to parturition. The dietary restriction was performed by givi(week−3) and 80% (−2 weeks to parturition) of the quantity of feed given to a groupbecame toxaemic during the dietary restriction period are represented by their numb

before the experimental period had started (Fig. 7). This meansthat it may be possible to use physiological measurements topredict ketosis susceptibility before goats enter the critical riskperiod at the end of pregnancy.

4.3. Behaviour

After 1 week of restricted feeding, the time budgetanalysis showed that R goats were generally more activethan C goats. During the novel arena test, R goats also spent

6153

6152

6145

6143

6121

6093

6091

6078

6066 6051

6044

6034

60055017

5005

4022

6

0 1 2 3 4

ose and low NEFA)

(n=27) at−9 weeks in relation toparturition. The goats subsequently receivedng a TMR which corresponded to 50% (weeks−8 to−5), 60% (week−4), 70%of control goats. Each circle and number represents a goat. The four goats whicher and a black circle.

Page 13: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

Table 2Behaviour of goats measured over 12 h at −7 and −1 week before parturition. Dietary regimens (Control (C) or Restricted (R)) were started −8 weeks beforeparturition 1.

In relation to parturition −7 weeksDietary regimen

P-value −1 weekDietary regimen

P-value

Behaviour

C (n=14) R (n=14) C (n=14) R (n=12)

Time spent (%)- lying down 18.6±4.67 17.8±4.24 ns 38.7±5.21 25.5±4.90 +- standing immobile 45.7b±4.44 31.7a±4.30 * 28.3b±4.48 45.3a±4.21 **- walking 1.6b±0.41 5.1a±0.37 *** 0.4b±0.11 1.0a±0.10 ***- standing at neck-lock 33.5b±2.66 48.1a±2.42 *** 32.4±2.17 28.6±2.04 ns- feeding 27.8b±2.41 42.5a±2.19 *** 29.1±1.85 25.6±1.74 ns

Number of- attacks 1.4(3.2)±0.20 1.4(2.9)±0.18 ns† 1.5(3.6)±0.23 0.9(1.4)±0.21 +†

- avoiding behaviour 4.2±0.78 3.4±0.70 ns 0.9(1.4)±0.21 1.1(2.1)±0.20 ns†- self-grooming 2.9b(17.2)±0.12 2.5a(10.6)±0.11 **† 9.6±1.69 12.4±1.59 ns- positive interactions 15.9b±1.95 4.9a±1.77 *** 1.4(2.9)±0.21 1.3(2.6)±0.19 ns†

† transformation ln(x+1) (back-transformed value). w Wilcoxon Mann Whitney test.Means within a row for a time period with different letters are significantly different (ns = not significant; +Pb0.1; *Pb0.05; **Pb0.01; and ***Pb0.001).

1 C group was fed a TMR ad libitum for the last third of gestation and R group was given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60%(for 1 week), 70% (for 1 week) and 80% (for 2 weeks) of the amount given to the C group.

86 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

more time walking compared to C goats. After 7 weeks ofrestricted feeding, the R goats continued to walk more than Cgoats. In addition, during the novel object test, R goats sniffedmore often the novel object and tended to be quicker to sniffit compared to C goats. These results may indicate that thefeed restricted animals were more motivated to explore theirenvironment to try and find new sources of feed resulting inthem walking more. Similar results were observed in sows:

Table 3Behaviour observed during a novel arena test (3 min) and novel object test (3 min)(C) or Restricted (R) were started −8 weeks before parturition 1.

In relation to parturition −7 weeksDietary regimen

P-valueDie

Behaviour

C (n=14) R (n=14) C (n=14)

Novel arena test:Time spent in theentrance area (%)

1.9b(5.4)±0.24 2.6a(12.3)±0.24 *† 3.1(20.1)±0

Time spentimmobile (%)

64.6±5.59 61.5±5.59 ns 62.6±7.51

Time spent walking (%) 13.0b±1.45 18.4a±1.45 * 14.6±2.43Time spent climbing (%) 2.5(10.9)±0.37 2.5(11.7)±0.37 ns† 2.1(7.5)±0.5Number of vocalisations 29.3±6.09 36.7±6.09 ns 32.6±5.94

Novel object test:Time spent in theentrance area (%)

2.1(7.0)±0.36 2.8(15.4)±0.36 ns† 39.0±7.98

Time spentimmobile (%)

67.7±6.58 68.1±6.58 ns 64.3±7.81

Time spent walking (%) 2.2(8.1)±0.15 2.5(10.8)±0.15 ns† 2.1(7.3)±0.1Time spent climbing (%) 2.2(8.3)±0.42 2.2(7.7)±0.42 ns† 27.5±7.94Number of times thatthe object was sniffed

1.1(2.1)±0.15 1.3(2.7)±0.15 ns† 1.8b±0.40

Latency before the firstsniff of the object (s)

3.4(28.1)±0.31 2.9(17.9)±0.31 ns† 56.6±11.79

Number of vocalisations 29.3±6.09 36.7±6.09 ns 22.8±3.92

†Transformation ln(x+1) (retransformed value).Means within a row for a time period with different letters are significantly differe

1 C group was fed a TMR ad libitum for the last third of gestation and R group was(for 1 weeks), 70% (for 1 weeks) and 80% (for 2 weeks) of the amount given to the

an increase in the time spent exploring the environment wasreported in sows when they were given a small volume of avery nutrient dense diet (energy and protein requirementswere covered) compared to sows receiving a more diluteddiet (de Leeuw and Ekkel, 2004). De Leeuw et al. (2005)suggested that when the motivation to feed remains highexploration increases. Nevertheless, even if it is difficult tointerpret individual behaviour (de Passillé et al., 1995),

performed −7, −2 and 2 weeks from parturition. Dietary regimens; Contro

−2 weekstary regimen

P-value 2 weeksDietary regimen

P-value

R (n=14) C (n=14) R (n=14)

.29 3.1(20.5)±0.28 ns† 21.3±2.45 15.1±2.24 +

55.2±7.24 ns 57.8±4.68 61.4±4.27 ns

16.9±2.34 ns 27.4±2.16 23.9±1.97 ns2 2.5(11.4)±0.5 ns† 14.5±4.12 14.7±3.76 ns

28±5.73 ns 51.0±7.0 51.8±6.39 ns

26.7±7.69 ns 24.9±6.24 27.1±5.69 ns

60.3±7.53 ns 71.3±5.22 69.7±4.76 ns

5 2.5(10.9)±0.15 +† 14.0±2.57 16.3±2.35 ns26.5±7.65 ns 14.7±4.24 14.0±3.87 ns3.1a±0.39 * 2.4±0.54 3.5±0.49 ns

27.6±11.36 + 3.3(27.2)±0.24 2.8(15.6)±0.22 ns†

25.3±3.78 ns 40.0±6.55 48.1±5.98 ns

nt (ns = not significant; +Pb0.1; *Pb0.05).given the same TMR but the quantity corresponded to 50% (for 4 weeks), 60%C group.

l

Page 14: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

87B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

exploration was probably not related to a sensation of hungerin the present experiment but more likely related to ametabolic drive to try and cover requirements, since the feedrestricted animals had free access to straw.

It should be noted that while positive social behavioursuch as self-grooming and positive interactions were reducedin R goats compared to C goats in the first week of restrictedfeeding, agonistic behaviour was not affected by a reductionin the quantity of feed given. During feeding the animals wereblocked at the neck-lock so that the possibility to expressagonistic behaviour was limited. For the remainder of thetime they had free access to straw. Barroso et al. (2000)showed that when a poor quality feed resource is available adlibitum then goats rarely fought. Another reason which couldexplain the low levels of agonistic behaviour in the R goats isthat group hierarchy was already established (Conway et al.,1996).

5. Conclusion

In conclusion, both metabolism and behaviour weremodified by late-pregnancy restricted feeding. Nutrientrestricted goats were more active than control goats, thismay indicate a metabolic drive to search for feedstuffs whichare more nutrient dense than the actual diet. As early as−9 week parturition, animals which went on to developpregnancy toxaemia had high NEFA and low glucose, and lowBCS and high urea. This profile may be useful in determiningwhich animals are at risk from pregnancy toxaemia.

Acknowledgments

The authors would like to thank J. Tessier and his team atthe goat unit of the Institut National de la RechercheAgronomique (INRA) for care of the animals, J. Perault, C.Ficheux and S. Camous for technical assistance and J.-Y. Picot(DIFAGRI PICOT SA, France) for the gift of the propylene glycolsupplement. Special thanks goes to P. Morand-Fehr forfruitful discussion during the experiment.

References

AFZ-INRA Tables, 2002. Tables de composition et de valeur nutritive desmatières premières destinées aux animaux d'élevage. INRA Editions,Paris.

Alexander, G., 1978. Quantitative development of adipose tissue in foetalsheep. Aust. J. Biol. Sci. 31, 489–503.

Andersen, I.L., Roussel, S., Ropstad, E., Braastad, B.O., Steinheim,G., Janczak, A.M.,Jorgensen, G.M., Boe, K.E., 2008. Social instability increases aggression ingroups of dairy goats, but with minor consequences for the goats' growth,kid production and development. Appl. Anim. Behav. Sci. 114, 132–148.

Bajhau, H.S., Kennedy, J.P., 1990. Influence of pre- and postpartum nutritionon growth of goat kids. Small Rumin. Res. 3, 227–236.

Barnouin, J., Chillard, Y., Chacornac, J.P., Lefaivre, R., 1986. Microdosageautomatisé sans déprotéïnisation du 3-hydroxy-butyrate plasmatiquechez les bovins. Ann. Rech. Vét. 17, 129–139.

Barroso, F.G., Alados, C.L., Boza, J., 2000. Social hierarchy in the domestic goat:effect on food habits and production. Appl. Anim. Behav. Sci. 69, 35–53.

Boissy, A., Veissier, I., Roussel, S., 2001. Behavioural reactivity affectedbychronicstress: an experimental approach in calves submitted to environmentalinstability. Anim. Welf. 10, S175–S185.

Borwick, S.C., Rae, M.T., Brooks, J., McNeilly, A.S., Racey, P.A., Rhind, S.M.,2003. Undernutrition of ewe lambs in utero and in early post-natal lifedoes not affect hypothalamic-pituitary function in adulthood. Anim.Reprod. Sci. 77, 61–70.

Bouissou, M.F., Boissy, A., Le Neindre, P., Veissier, I., 2001. The socialbehaviour of cattle. In: Keeling, L.J., Gonyou, H.W. (Eds.), SocialBehaviour in Farm Animals. CABI Publishing, Oxon, UK, pp. 113–146.

Celi, P., Di Trana, A., Claps, S., 2008. Effects of perinatal nutrition on lactationalperformance, metabolic and hormonal profiles of dairy goats andrespective kids. Small Rumin. Res. 79, 129–136.

CISIA (Centre International de Statistique et d'Informatique Appliqueés),1996. SPAD version 3: manuel de référence.

Conway, M.L.T., Blackshaw, J.K., Daniel, R.C.W., 1996. The effects of agonisticbehaviour and nutritional stress on both the success of pregnancy andvarious plasma constituents in Angora goats. Appl. Anim. Behav. Sci. 48, 1–13.

Delavaud, D., Bocquier, F., Chilliard, Y., Keisler, D.H., Gertler, A., Kann, G.,2000. Plasma leptin determination in ruminants: effect of nutritionalstatus and body fatness on plasma leptin concentration assessed by aspecific RIA in sheep. J. Endocrinol. 165, 519–526.

de Leeuw, J.A., Ekkel, E.D., 2004. Effects of feeding level and the presence of aforaging substrate on the behaviour and stress physiological response ofindividually housed gilts. Appl. Anim. Behav. Sci. 86, 15–25.

de Leeuw, J.A., Zonderland, J.J., Altena, H., Spoolder, H.A.M., Jongbloed, A.W.,Verstegen, M.W.A., 2005. Effects of levels and sources of dietaryfermentable non-starch polysaccharides on blood glucose stability andbehaviour of group-housed pregnant gilts. Appl. Anim. Behav. Sci. 94,15–29.

de Passillé, A.M., Rushen, J., Martin, F., 1995. Interpreting the behaviour ofcalves in an open-field test: a factor analysis. Appl. Anim. Behav. Sci. 45,201–213.

Fisher, A., Matthews, L., 2001. The social behaviour of sheep. In: Keeling, L.J.,Gonyou, H.W. (Eds.), Social behaviour in farm animals. CABI Publishing,Oxon, UK, pp. 211–245.

Ford, E.J., Evans, J., Robinson, I., 1990. Cortisol in pregnancy toxaemia ofsheep. Br. Vet. J. 146, 539–542.

Greenwood, P.L., Slepetis, R.M., Hermanson, J.W., Bell, A.W., 1999. Intrauter-ine growth retardation is associated with reduced cell cycle activity, butnot myofibre number, in ovine fetal muscle. Reprod. Fertil. Dev. 11,281–291.

Harmeyer, J., Schlumbohm, C., 2006. Pregnancy impairs ketone body disposalin late gestating ewes: implications for onset of pregnancy toxaemia. Res.Vet. Sci. 81, 254–264.

Henze, P., Bickhardt, K., Fuhrmann, H., Sallmann, H.P., 1998. Spontaneouspregnancy toxaemia (ketosis) in sheep and the role of insulin. Zentralbl.Veterinarmed. 45, 255–266.

Husted, S.M., Nielsen, M.O., Tygesen, M.P., Kiani, A., Blache, D., Ingvartsen, K.L.,2007. Programming of intermediate metabolism in young lambs affectedby late gestational maternal undernourishment. Am. J. Physiol. 293,E548–E557.

INRA, 1988. Alimentation des Bovins, Ovins, Caprins. INRA, Paris. 471 pp.Koritnik, D.R., Humphrey, W.D., Kaltenbach, C.C., Dunn, T.G., 1981. Effects of

maternal undernutrition on the development of the ovine fetus and theassociated changes in growth hormone and prolactin. Biol. Reprod. 24,125–137.

Laporte, B., Chavatte-Palmer, P., Roussel-Huchette, S., Perault, J., Duvaux-Ponter,C., 2009. Consequences of maternal nutritional restriction during pregnancyon kid morphology and weight at birth. In: Chilliard, Y., Glasser, F.,Faulconnier, Y., Bocquier, F., Veissier, I., Doreau, M. (Eds.), Ruminantphysiology. Digestion, metabolism, and effects of nutrition on reproductionand welfare. Wageningen Academic Publishers, Wageningen, TheNetherlands, p. 750.

Mason, J.W., 1971. A re-evaluation of the concept of "non-specificity" instress theory. J. Psychiatr. Res. 8, 323–333.

Mavrogianni, V.S., Brozos, C., 2008. Reflections on the causes and thediagnosis of peri-parturient losses of ewes. Small Rumin. Res. 76, 77–82.

Mayer, E., Liebich, H.G., Arbitman, R., Hagemeister, H., Dirksen, G., 1986.Nutritionally-induced changes in the rumenal papillae and in theircapacity to absorb short chain fatty acids in high producing dairy cows.Proc. 14th World Congress on Diseases of Cattle, pp. 806–817.

Mitlohner, F.M., Morrow-Tesch, J.L., Wilson, S.C., Dailey, J.W., McGlone, J.J.,2001. Behavioral sampling techniques for feedlot cattle. J. Anim. Sci. 79,1189–1193.

Oliver, M.H., Harding, J.E., Gluckman, P.D., 2001. Duration of maternalundernutrition in late gestation determines the reversibility of intrauterinegrowth restriction in sheep. Neonat. Med. 6, 271–279.

Petterson, J.A., Dunshea, F.R., Ehrhardt, R.A., Bell, A.W., 1993. Pregnancy andundernutrition alters glucose metabolic responses to insulin in sheep. J.Nutr. 123, 1286–1295.

Ramin, A.G., Asri, S., Majdani, R., 2005. Correlations among serum glucose,beta-hydroxybutyrate and urea concentrations in non-pregnant ewes.Small Rumin. Res. 57, 265–269.

Roussel, S., Boissy, A., Montigny, D., Hemsworth, P.H., Duvaux-Ponter, C.,2005. Gender-specific effects of prenatal stress on emotional reactivityand stress physiology of goat kids. Horm. Behav. 47, 256–266.

Page 15: Restricted feeding of goats during the last third of gestation modifies both metabolic parameters and behaviour

88 B. Laporte-Broux et al. / Livestock Science 138 (2011) 74–88

Sahlu, T., Hart, S.P., Le-Trong, T., Jia, Z., Dawson, L., Gipson, T., Teh, T.H., 1995.Influence of prepartum protein and energy concentrations for dairygoats during pregnancy and early lactation. J. Dairy Sci. 78, 378–387.

Sargison, N.D., 2007. Pregnancy toxaemia, In: Aitken, I.D. (Ed.), Diseases ofSheep, 4th edn. Blackwell, Oxford, pp. 359–363.

SAS Institute Inc., 2000. SAS/STAT Software: User's Guide, Release 8.0. SASInstitute Inc., Cary, NC.

Schlumbohm, C., Harmeyer, J., 2008. Twin-pregnancy increases susceptibilityof ewes to hypoglycaemic stress and pregnancy toxaemia. Res. Vet. Sci.84, 286–299.

Simitzis, P.E., Charismiadou, M.A., Kotsampasi, B., Papadomichelakis, G.,Christopoulou, E.P., Papavlasopoulou, E.K., Deligeorgis, S.G., 2009. Influenceofmaternal undernutrition on the behaviour of juvenile lambs. Appl. Anim.Behav. Sci. 116, 191–197.

Sykes, A.R., Field, A.C., 1972. Effects of dietary deficiencies of energy, proteinand calcium on the pregnant ewe. J. Agric. Sci. 78, 127–133.