J. Anim Sci.
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J. Anim Sci. 2008. 86:220-225. doi:10.2527/jas.2007-0198
© 2008 American Society of Animal Science

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ANIMAL PRODUCTION

Effects of weaning lambs in two stages or by abrupt separation on their behavior and growth rate

C. Schichowski, E. Moors and M. Gauly1

Department of Animal Breeding and Genetics, Georg August University, 37075 Göttingen, Germany


    Abstract
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
A study was conducted to evaluate effects of age at weaning in combination with different weaning procedures on 2 breeds of lambs (Merinoland, Rhoenschaf). Lambs were either weaned at 8 or 16 wk of age in 2 stages or with the traditional method of weaning by abrupt separation. In the 2-stage treatment, lambs were prevented from nursing their dam for 1 wk (stage 1) before their separation (stage 2). Control animals were nursed by their dams until they were separated. Lamb BW and behavior (vocalization, agitation) were recorded before and after separation. After separation, lambs weaned at 8 wk of age had greater (P = 0.004) ADG compared with lambs weaned at 16 wk of age. Control lambs had greater (P < 0.001) agitation scores [1 = no agitation (normal behavior; i.e., feeding, resting, lying, standing, or play behavior) to 3 = high agitation (continuously moving, restlessness, or vocalization)] irrespective of weaning age and breed. On the day of separation, 2-stage lambs had scores from 1.17 to 1.35, whereas control lambs were scored from 1.70 to 1.79. After separation, lambs weaned in 2 stages vocalized up to 98.2% less (P = 0.001) than control animals. Furthermore, bleats were greater for Rhoenschaf lambs and at a weaning age of 8 wk (P < 0.05). Differences between treatments were greatest on the day of separation. Vocalization decreased continuously within the first 3 d of weaning to zero. Lambs weaned in 2 stages were less distressed than lambs weaned by the traditional method of abrupt separation based on behavioral data, but ADG until 12 and 16 wk of age did not differ (P > 0.05) for either treatment in this study.

Key Words: behavior • lamb • productivity • sheep • weaning


    INTRODUCTION
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
Suckling is a major factor in the strength of the ewe-lamb bond (Hinch et al., 1990Go). With reduced milk production, the frequency and duration of suckling decrease (Gordon and Siegmann, 1991Go; Pryce, 1992Go). Therefore, progressive natural weaning has very little apparent negative consequences on social groups of ewes and lambs. In contrast, artificial weaning imposed by the breeder can induce an important stress for ewe and lamb (Orgeur et al., 1997Go). In cattle, behavioral responses to this event can be observed for several days or weeks (Veissier and LeNeindre, 1989Go). Both ewes and lambs express their distress by an increase in bleating and locomotion activity (Alexander, 1977Go; Torres-Hernandez and Hohenboken, 1979Go). Some stressors can induce a suppression on some aspects of the immune system having negative effects on animal health, welfare (Orgeur et al., 1997Go), and performance, because the release of glucocorticoid hormones coincides with a decrease in GH (Kuhn et al., 1990Go). An alteration in growth rate may also result from the decrease of the quantity of food ingested or from an impairment of digestive function caused by weaning stress (Dantzer and Mormède, 1979Go).

Haley et al. (2005)Go described effects of an alternative weaning procedure for beef calves. Preventing nursing between cow-calf pairs before separation of the mother and young decreased the degree of behavioral changes compared with imposing both restrictions, preventing nursing and separation, together. The authors stressed the possible benefits from this procedure and recommended it for practical use. Similar studies have not been done in sheep. Therefore, the aim of this study was to measure lamb behavior and ADG after 2 different weaning procedures including traditional weaning by abrupt separation of the mother-lamb pair and a modified 2-stage treatment previously described for cattle (Haley et al., 2001Go, 2005Go).


    MATERIALS AND METHODS
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
Experimental Flock and Design

This experiment was performed in accordance with the guidelines established by the Institutional Animal Care and Use Committee of the University of Göttingen based on the German Animal Welfare law.

A total of 158 Merinolandschaf (German Merino) and Rhoenschaf (Rhoensheep) lambs were used in the study. Animals were weaned at either 8 or 16 wk. Weaning was done by 1 of 2 procedures. The traditional weaning method was by abrupt visual and acoustical separation of the ewe and lamb. The second was a 2-stage method, in which lambs were first prevented from nursing their dam for 1 wk (stage 1) before their separation (stage 2). Nursing was prevented by covering the udder of the mother with a net that was fixed on the back of the animal (Figure 1Go).


Figure 1
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Figure 1. (A) Photograph of the udder net, which prevented nursing by providing a barrier between the mouth of the lamb and the teat of the ewe. (B) Photograph showing how the net was fixed over the back.

 
All lambs in the study were born as singles within a week. They were kept indoors and bedded on straw in groups of 30 to 60 ewes (1.5 m2/ewe and lamb). All lambs had ad libitum access to hay, a standard concentrate (11.5 MJ of ME/kg, 19.5% CP), and water. At an average age of 6 or 14 wk, lambs and their mothers were randomly divided into 4 groups/breed (Table 1Go). At the time of weaning, groups of lambs (20 to 30 lambs) were separated from their mothers by moving them to a different barn with pens (1.0 m2/lamb), prohibiting visual contact and vocal communication.


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Table 1. Experimental design, number of animals per weaning method, and weaning age used in the study
 
Behavioral Observations

For identification, ewes and lambs were individually marked on the back with a color code (cattle color, Raidex, Dettingen, Germany). Lambs and ewes received the same color codes for correct allocation.

Lambs were observed for 3 h/d (from 0900 to 1200). Observation began 4 d before weaning (at 1000) and was continued for 4 d after weaning. Scan sampling was used at 30-min intervals to count the total number of vocalizations (bleats) coming from each lamb for 1 min, on a rotating basis. At the beginning of each 30-min interval, scores for agitation were recorded for each lamb. Three scores were used: 1 = no agitation (normal behavior, i.e., feeding, resting, lying, standing, or play behavior); 2 = agitation (no normal behavior, i.e., moving around, head or leg moving); 3 = high agitation (continuously moving, restlessness, or vocalization).

Statistical Analysis

All statistical analyzes were performed using SAS (SAS Inst. Inc., Cary, NC). The GLM procedure was used to obtain least squares means for lamb ADG with breed, sex, age, and method of weaning as fixed effects and birth weight as the covariate.

The following model was used:


Formula

where yijklm = the mth observation; µ= overall mean; bi = breed; sj = sex; mk = weaning method; al = weaning age; al x mk = interaction between weaning age and weaning method; and eijklm = random residual. For the analysis of birth weight, breed and sex as well as the interaction between them were set as fixed effects.

The following model was used to analyze differences in the frequency of bleats (bleats/min) using the MIXED procedure of SAS:


Formula

where yijklmn = nth observation; µ = overall mean; bi = breed; aj = weaning age; mk = weaning method; dl = day of observation; aj x mk x bi = interaction among weaning age, weaning method, and breed; aj x mk x bi x dl = interaction among breed, weaning age, weaning method, and day of observation; nm = random animal effect; and eijklmn = random residual.

To analyze differences in the agitation score, a linear model (GLM) was used with weaning age, method, and breed as fixed effects. Frequencies of agitation scores were calculated with the FREQ procedure of SAS.


    RESULTS
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
BW and ADG

German Merino lambs had greater (P < 0.001) birth weights (5.51 ± 0.10 kg) compared with Rhoensheep lambs (4.41 ± 0.10 kg). Although ADG was different (P < 0.001) between breeds at wk 12 (329 vs. 281 g) and wk 16 of age (335 vs. 268 g), lamb sex had no influence (P = 0.10) on birth weight.

Lambs weaned at wk 8 had greater (P = 0.004) ADG until wk 12 (317 vs. 294 g) and wk 16 (313 vs. 291 g) compared with lambs weaned at wk 16. However, neither the traditional nor the 2-stage weaning affected (P > 0.50) ADG at wk 12 and 16. An interaction between weaning age and weaning method influenced (P < 0.047) ADG (Table 2Go) at wk 12 and 16.


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Table 2. Average daily gains of lambs weaned at 8 and 16 wk of age by traditional or 2-stage methods1
 
Lamb Behavior

Animals weaned by abrupt separation showed greater (P < 0.001) scores of agitation compared with animals weaned in 2 stages. Development of the score levels in the different groups during the time of observation is shown in Figure 2Go. All groups showed no agitation before weaning and at 4 d after weaning (score = 1).


Figure 2
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Figure 2. Agitation score (1 = no agitation; 2 = agitation; and 3 = high agitation) before (d 0 to 3) and after (d 5 to 8) weaning (d 4) in relation to weaning age (8 and 16 wk) and weaning procedure (traditional weaning was by abrupt separation, and 2-stage weaning prevented lambs from nursing their dam for 1 wk before their separation) in German Merinoland (left) and Rhoensheep (right) lambs.

 
Agitation scores were not different between breeds (P > 0.05); however, animals weaned in 2 stages had lower (P < 0.001) agitation scores compared with traditionally weaned animals (Table 3Go). The frequency of bleats (Table 4Go) was influenced by breed (P = 0.008), weaning age (P = 0.035), and procedure (P < 0.001). Although Rhoensheep lambs bleated more (P = 0.008) than German Merino lambs (2.10 vs. 1.83 ± 0.07), traditionally weaned lambs vocalized more (P < 0.001) than lambs weaned in 2 stages (3.15 vs. 0.78 ± 0.07).


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Table 3. Average frequencies (%) of agitation scores in lambs during the observation period divided by breed, weaning age, and weaning method1
 

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Table 4. Least squares means (±SE) of bleats per minute in relation to weaning age, weaning method, and breed1
 
Number of bleats was greatest in lambs weaned in the traditional method at an age of 8 wk (Figure 3Go). No vocalization occurred on the days before weaning and after the second day of weaning.


Figure 3
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Figure 3. Least squares means (±SE) of bleats per minute after weaning (d 0) in relation to weaning age (8 and 16 wk) and weaning procedure (traditional weaning was by abrupt separation, and 2-stage weaning prevented lambs from nursing their dam for 1 wk before their separation) in German Merino (left) and Rhoensheep (right) lambs.

 
Bleat frequencies differed (P < 0.001) between the observation days and times within a day (Figure 4Go) and were greater on the day of weaning (3.71 ± 0.10/min, P < 0.001) compared with d 1 (2.86 ± 0.10/min) and 2 (1.29 ± 0.10/min) after weaning. On the day of weaning, the greatest mean bleat rate of 6.30 ± 0.25/min occurred 30 min after separation (1030). The frequency decreased until the second day after weaning to 0.84 ± 0.25 bleats/min at 1200.


Figure 4
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Figure 4. Bleats per minute (every 30 min from 0900 to 1200) during day of weaning as well as 1 and 2 d after the weaning procedure for all lambs in the study.

 

    DISCUSSION
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
Considering birth weights and growth characteristics, German Merino lambs were evidently superior to Rhoensheep lambs, confirming earlier studies (Kraus et al., 1998Go; Mathiak et al., 1999Go; Seibert et al., 2004Go). Daily growth rate may be reduced by stress, because the release of glucocorticoid hormones is accompanied by reduced GH production (Kuhn et al., 1990Go), which may lead to decreased feed intake. However, in this study, early weaned lambs (8 wk) had greater (P = 0.004) ADG compared with lambs weaned at an age of 16 wk. This is somewhat surprising, because later-weaned animals would have been expected to benefit from the additional milk received by the ewe. The availability of high-quality concentrates may have allowed early weaned lambs to compensate for the loss of maternal milk by increased feed intake, resulting in a greater total intake of energy. Furthermore, traditional and 2-stage weaning did not differ regarding daily BW gains, confirming similar results found for calves (Haley et al., 2005Go). A punctuated loss in BW due to social disturbance like mother-young separation was probably transient and unnoticed because of the relatively long-term weighing intervals (Dantzer and Mormède, 1979Go). These results may have been different under conditions with disadvantageous nutritional management and shorter weighing frequencies. Poor feed conditions may increase BW gains by lambs weaned by the 2-stage method compared with an abrupt separation.

Clear behavioral perturbations were induced by weaning for all observed lambs, independent of genotype, age, or weaning procedure. But after only a few days, clear signs of habituation occurred, and behavior returned to preweaning levels, which is in agreement with results found by Orgeur et al. (1997)Go.

As expected, results showed that younger lambs were more stressed by weaning procedures when compared with older lambs based on the observed behavioral parameters. This may be due to the stronger mother-young bond. The relationship between the ewe and its lamb(s) disengages with age of the offspring and as the lambs become more autonomous (Orgeur et al., 1997Go). The intervals between suckling increase with age, indicating that 16-wk-old lambs are more accustomed to a separation from the mother than younger lambs. With age, the distance between mother and young becomes longer. Older lambs also move more frequently and further from the ewe than younger lambs, and they do not vocalize as much as younger ones. Increased vocalization rates in lambs occur after a stressor such as separation (Torres-Hernandez and Hohenboken, 1979Go; Cockram et al., 1993Go). Younger lambs show more activity, such as running around in the stable and searching for their dam. Therefore, to abate the separation stress for lambs at weaning, weaning should occur when lambs are as old as possible.

Vocalization was different (P = 0.008) between breeds, with Rhoensheep lambs bleating more than German Merino lambs if weaned abruptly at 8 wk of age. This could either indicate that the development of the Rhoensheep breed may be slower compared with the German Merino (Kraus et al., 1998Go) or that the mother bond is somehow stronger in this breed.

Results of this study clearly demonstrate that lambs weaned with the 2-stage method vocalized less and showed less behaviors indicative of agitation after separation than animals weaned by the traditional method of abrupt separation. Similar results have been reported in horses (McCall et all., 1985Go), sheep (Orgeur et al., 1997Go), and calves (Haley et al., 2001Go, 2005Go). Although lambs weaned in 2 stages have to cope with a single stressor at a time, the denial of milk and the separation procedure, lambs weaned in the traditional way have to cope with both stressors at the same time, leading to greater stress levels expressed by more agitation and vocalization.

The greatest mean bleat rate was recorded on the day of weaning, followed by a continuous decline until 2 d after weaning. Similar results have been reported for sheep (Orgeur et al., 1997Go) and calves (Haley et al., 2005Go).

Several studies indicate that separation of mother and young induced only a weak response of glucocorticoids, provided that a visual and auditory contact exists (Levine et al., 1985Go; Hennessy and Moorman, 1989Go; Lefcourt and Elsasser, 1995Go). However, the behavioral response of separation can be different from the behavior shown before separation.

This study showed that preventing lambs from suckling before the actual separation (2-stage method) can reduce stress for weaned lambs. However, the 2-stage weaning method is very time-consuming, particularly the attachment of the udder net. Therefore, this method is practical only for small herds. Nevertheless, because detailed information on the possible benefits of alternative weaning procedures are lacking, further investigations on modified systems are needed.


    Acknowledgements
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 
The authors would like to thank G. Erhardt and the staff of the Research Station Oberer Hardthof of the University of Giessen for their generous technical support.

1 Corresponding author: Mgauly{at}gwdg.de

Received for publication April 3, 2007. Accepted for publication September 20, 2007.


    LITERATURE CITED
 Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 Acknowledgements
 LITERATURE CITED
 


Alexander, G. 1977. Role of auditory cues in mutual recognition between ewes and lambs in Merino sheep. Appl. Anim. Ethol. 3:65–81.[CrossRef]

Cockram, M. S., P. Imlah, P. J. Goddard, G. D. Harkiss, and N. K. Waran. 1993. The behavioral, endocrine and leucocyte response of ewes to repeated removal of lambs before the age of natural weaning. Appl. Anim. Behav. Sci. 38:127–142.[CrossRef]

Dantzer, R., and P. Mormède. 1979. Le stress en élevage intensif. Page 199 in Actualités scientifiques et agronomiques de l’INRA. INRA, Masson, Paris.

Gordon, K., and M. Siegmann. 1991. Suckling behaviour of ewes in early lactation. Physiol. Behav. 50:1079–1081.[CrossRef][Medline]

Haley, D. B., D. W. Bailey, and J. W. Stookey. 2005. The effects of weaning beef calves in two stages on their behavior and growth rate. J. Anim. Sci. 83:2205–2214.[Abstract/Free Full Text]

Haley, D. B., J. W. Stookey, J. L. Clavelle, and J. M. Watts. 2001. The simultaneous loss of milk and maternal contact compounds distress at weaning in beef calves. Proc. 35th Int. Congr. Int. Soc. Appl. Ethol., Davis, CA. J. P. Garner, J. A. Mench, and S. P. Heekin, ed. The Center for Animal Welfare, University of California, Davis.

Hennessy, M. B., and L. Moorman. 1989. Factors influencing cortisol and behavioural response to maternal separation in Guinea pigs. Behav. Neurosci. 103:378–385.[CrossRef][Medline]

Hinch, G. N., J. J. Lynch, R. L. Elwin, and G. C. Green. 1990. Long-term associations between Merino ewes and their offspring. Appl. Anim. Behav. Sci. 27:93–103.[CrossRef]

Kraus, M., R. Beuing, M. Gauly, and G. Erhardt. 1998. Zum Zuchtziel beim Rhönschaf im Hinblick auf Mutterschafgewicht und Fruchtbarkeit unter dem Aspekt extensiver und intensiver Haltung. Arch. Tierz. 41:99–109.

Kuhn, C. M., J. Pauk, and S. M. Schanberg. 1990. Endocrine responses to mother-infant separation in developing rats. Dev. Psychobiol. 23:395–410.[CrossRef][Medline]

Lefcourt, A. M., and T. H. Elsasser. 1995. Adrenal responses of Angus x Hereford cattle to the stress of weaning. J. Anim. Sci. 73:2669–2676.[Abstract]

Levine, S., D. F. Johnson, and C. A. Gonzalez. 1985. Behavioural and hormonal responses to separation in infant Rhesus monkeys and mother. Behav. Neurosci. 99:399–410.[CrossRef][Medline]

Mathiak, H., M. Gauly, K. Hoffmann, and G. Erhardt. 1999. Vergleich der Produktionsleistung von Schafrassen auf einem extensiv bewirtschafteten Mittel-gebirgsstandort. Zeitschrift für Kulturtechnik und Landentwicklung 40:1–6.

McCall, C. A., G. D. Potter, and J. L. Kreider. 1985. Locomotor, vocal and other behavioral responses to varying methods of weaning foals. Appl. Anim. Behav. Sci. 14:27–35.[Medline]

Orgeur, P., N. Mavric, P. Yvore, S. Bernard, R. Nowak, B. Schaal, and F. Levy. 1997. Artificial weaning in sheep: Consequences on behavioural, hormonal and immunopathological indicators of welfare. Appl. Anim. Behav. Sci. 58:87–103.[CrossRef]

Pryce, C. R. 1992. A comparative systems model of the regulation of maternal motivation in mammals. Anim. Behav. 43:417–441.[CrossRef]

Seibert, B., M. Gauly, and G. Erhardt. 2004. Productivity of different sheep breeds in extensive pasture management. Arch. Tierz. 47:147–152.

Torres-Hernandez, G., and W. Hohenboken. 1979. An attempt to assess traits of emotionality in crossbred ewes. Appl. Anim. Ethol. 5:71–83.[CrossRef]

Veissier, I., and P. LeNeindre. 1989. Weaning in calves: Its effect on social organization. Appl. Anim. Behav. 24:43–54.[CrossRef]



This Article
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86/1/220    most recent
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Right arrow Articles by Schichowski, C.
Right arrow Articles by Gauly, M.


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