Ewe maternal behavior score to estimate lamb survival and performance during lactation/Escore de comportamento materno de ovelhas para estimar a sobrevivencia e o desempenho de cordeiros durante a lactacao.
Since the maternal behavior of pregnant and lactating ewes may be linked to mortality of lambs, experience and temperament should be taken into consideration in the management of sheep flocks (Rech et al., 2008; Corner et al., 2013). In fact, ewe behavior before, during and after lambing has great influence on lamb survival (Grandinson, 2005; Ceyhan, Sezenler, Yuksel, & Yildirir, 2012; Hinch & O'Brien, 2014) due to the fact that the ability of a lamb to survive until weaning is largely determined by the establishment of maternal-filial bonds and the care and protection given by the ewe (Dwyer, 2008; Bickell, Nowak, Poindron, Ferguson, & Blache, 2010). Evaluation of maternal-filial relationship may be very important, with direct impact on productivity and on sheep production chain.
Ewes express maternal behavior soon after lambing through lamb body cleaning, low intensity bleating and acceptance of the lamb's approach near the inguinal region (Rech et al., 2011). The selection of sheep by maternal ability through the Maternal Behavior Score (MBS), described is capable of improving the productive and economic efficiency of sheep production business traditionally assessed by the weaned lamb weights per ewe. Rech et al. (2008) reported that ewes with higher MBS protected their lambs more soon after birth and weaned heavier lambs.
Several factors may influence maternal behavior (Hernandez, Matthews, Oliver, Bloomfield, & Harding, 2009; Corner et al., 2010), such as previous experience, breed, ewe body condition score, nutritional state, production system and other factors. Since young females may show little or no ability (Mariz et al., 2007; Dwyer, 2008; Dwyer, 2014), they reduce lamb viability without human interference. Fear-caused reaction by female sheep was greater in young animals than in older ones (Silveira, Fischer, & Mendonca, 2010). Pickup and Dwyer (2011) reported difference in maternal behavior soon after lambing and during lactation between different ewe breeds, Suffolk and Blackface, in which the former showed poorer maternal ability. According to Grandinson (2005), under extensive production system and with little human supervision, sheep maternal care is more important, and, therefore, the female environment and nutrition are essential for the survival and growth of progeny (Hernandez, Matthews, Oliver, Bloomfield, & Harding, 2010; Hild, Andersen, and Zanella, 2010).
Research papers on maternal-filial behavior of wooly ewe in subtropical conditions and the use of MBS as a tool to estimate their behavior are still scarce. Current study correlated MBS with the performance of lambs until weaning and provided a better understanding of the maternal-filial behavior among ewes and lambs, and their reactions. Evaluation of the maternal ability may be an important tool to improve the sheep production system.
Material and methods
The experiment was conducted at the State Agricultural Research Foundation (Fepagro), Viamao RS Brazil, 30[degrees]04' 51" S and 51[degrees]01' 22" W, between May 2009 and January 2010. Research followed rules and legal requirements on ethical procedures and welfare of animals in scientific experimentation (Process N. 19221 Research Committee of UFRGS/ Faculty of Agronomy).
The study was carried out in a 4.8 hours area with Brachiaria arrecta Napper sward. A continuous grazing method was used, and the average herbage allowance was 11.5 kg of dry matter x [(100 kg body weight).sup.-1]. Thirty-seven multiparous Corriedale ewes were used. During the breeding period and before their first lambing, the ewes' body condition score (BCS) was assessed. The BCS was based on a palpation of the lumbar region of the spine, checking the amount of fat and muscle found between the spinous and transverse process of the vertebras (Russel, Doney, & Gunn, 1969). Lambing occurred between September 21, 2009 and November 9, 2009. Twenty-six among the 37 births were monitored throughout the whole day, from birth till first lamb feeding. During this period, ewe identification, lambing time (morning or afternoon), type of lambing (single or multiple, normal or dystocic), positioning of the ewe in relation to flock (if she was isolated from the herd or not), placenta weight and behavior to lamb were recorded: whether the ewe licked and smelled the lamb(s); whether it facilitated the ingestion of colostrum and vocalized in the direction of the lamb. With regard to the lamb: lamb's vigor, vocalization, lag of time between birth and standing up, and lag of time from birth till the animal could support itself on all four legs) were registered.
The lambs were weighed and identified between 12 and 24 hours after lambing, using a manual scale, at 10 g precision. Placentas were weighed with a digital scale, at 0.5 g precision. Total placenta weight was calculated by totaling the weight of the placentas of all lambs born per ewe.
At the time of lamb weighing and identification, ewe behavior was assessed by a six-point scale (maternal behavior score, MBS) which assessed the escaping distance of the ewe, adapted from Rech et al. (2008):
1. The ewe runs away when a person approaches; she shows no interest in the lamb(s); she does not emit any vocalization and she does not return to the lamb(s) during the observation period;
2. The ewe flees and remains more than 10 m from the lamb(s), and returns during the period of observation;
3. The ewe flees and remains 5 to 10 m from the lamb(s);
4. The ewe flees and remains between 1 and 5 m of the lamb(s);
5. The ewe remains up to 1 m of the lamb(s);
6. The ewe keeps physical contact with the lamb(s).
MBSs may be grouped into two classes: worse ([less than or equal to] 2) and better (> 2). The survival rate was calculated by the ratio between the number of lambs per ewe, and the number of those that remained alive in the first 72 hours after birth and at weaning.
Weaning occurred January 10, 2010, when 33 lambs were weaned, with average age of 84 days. Animal performance was evaluated on this day. Body weight was assessed after a previous fasting of solid and liquid of at least 12 hours, using a 0.5 kg precision scale. BCS of lambs and the ewes was evaluated on that day.
The experiment was set up in a completely randomized design, where the ewe was the experimental unit. The continuous variables and normal distribution were submitted to analysis of variance to describe the maternal behavior of the ewe, and were related to lamb performance. The mathematical model used was Yij = [mu] + ti + eij where: Y ij = value of the variable tested under the ith score level, [mu] = overall mean for the variable, ti = effect of the ith level of MBS and eij = random error. The Wilcoxon Signed-Rank test, a nonparametric analysis, was performed, using the observed frequencies in the case of qualitative or discrete variables. Correlation analyses were done between variables (Spearman coefficient). Statistical analyses were performed with SAS 9.1 (SAS Institute Inc., Cary - NC, USA).
Results and discussion
Maternal behavior is influenced by the environment and animal handling techniques (Everett-Hincks, Lopez-Villalobos, Blair, & Stafford, 2005) are probably affected by factors such as strain (Dwyer & Smith, 2008), previous maternal experience (Dwyer, 2014) and maternal nutritional status (Dwyer, Lawrence, Bishop, & Lewis, 2003), described in several papers. In current assay, ewes received the same previous management, with uniform nutritional status during the experiment, resulting in similar behavior among the ewes.
Approximately 83% of the ewes kept a distance from the herd to lamb. At lambing, the ewe transforms itself from a highly gregarious animal to an isolated animal because, according to Nowak, Porter, Levy, Orgeur, and Schaal (2000), isolation is an important step towards the formation of the maternal-filial bond. Besides isolation, most ewes (95.5%) licked and smelled the offspring(s), as described by several authors in other regions of the world (Pickup & Dwyer, 2011). The set of attention behavior, including sniffing, licking and protecting the neonate, serves as an instrument for the formation of a selective maternal-filial bond (Levy & Keller, 2008). The establishment of the motherinfant bond is essential for the offspring's survival. Due to this behavior, the lambs receive proper nutrition, protection from predators, suitable environment for their development and social life (Gomez et al., 2010).
Similar to what was reported in relation to insolation attitude and offspring care, the attitude to facilitate the intake of colostrum was observed in 79% of the ewes; the mother's interest in the lamb immediately after lambing was observed in 90% of the ewes; and the vocalization of ewes and lambs after birth was observed in 100% of cases. These observations coincided with those reported in other studies (Everett-Hincks et al., 2005; Rech et al., 2008; Aita et al., 2012). Smell, visual and auditory (vocalizations) stimuli played an important role in the recognition of the lamb by the ewe (Poindron, 2005).
Ewes in current study averaged 2.25 [+ or -] 0.84 MBS, indicating high reaction to the presence of a person approaching the lamb. The frequencies of animals in MBS 1, 2, 3, 4 and 5 were respectively 9.1, 69.7, 12.1, 6 and 3%. MBS was not related to the several behavior traits at lambing, such as ewe isolation from the herd, feed facilitation, lick, smell and showing interest in the lamb, possibly because most ewes showed these behaviors almost regardless of their reaction to the person's approach. This result partly disagree with that in other studies (Everett-Hincks et al., 2005; Dwyer, 2008; Rech et al., 2008), in which most ewes with higher MBS cared and protected more their lambs than those with a lower MBS.
MBS was positively correlated to BCS during breeding (r = 0.37, p < 0.05), but not related to BCS at lambing. Moreover, results revealing that MBS was not correlated with the weight of the lamb at birth and the weight of the placenta show that there was apparently no close relationship between the ewe's nutrition at the end of pregnancy (Clarke, Heasman, Juniper, & Symonds, 1998) and maternalfilial behavior. Mariz et al. (2007) found that ewes receiving increased energy intake vocalized and licked more their offspring, but failed to change the lamb's behavior. This result adds to what was already reported in a recent publication by Asmad et al. (2014) that nutrition during pregnancy of sheep has a limited effect on performance of lambs from birth to weaning. It may be concluded that managements to increase the birth weight of lambs will not have a major effect on improving the maternal behavior to promote the ewe's care for the lamb just after delivery. Arnold and Morgan (1975) reported that in Australia only 16% of lamb deaths were related to inefficient maternal behavior and 23% resulted in the lamb's inability to suckle after standing upright.
Approximately 95% of the lambs were vigorous after birth; they took on average 26 ([+ or -] 17.8) min to stand up and 40 ([+ or -] 12.8) min to first feeding (Table 1). Latency time to stand up and have the first feeding were positively correlated (r = 0.88, p < 0.0001), while the lamb vigor tended to be negatively related to latency to stand up (r = -0 45, p < 0.10). It is important for lambs to be able to stand up and show proper search behavior for the udder since they are born with limited energy reserves and require colostrum immediately after birth to survive. Most lambs take less than 30 min to stand up after birth, and 60% ingest colostrum within the first two hours of life (Nowak, Keller, Val-Laillet, & Levy, 2007). A short time to first feeding is desirable because the survival rate is enhanced for the lambs that stand out and quickly ingest milk (Dwyer et al., 2003). This is due to the fact that lambs with low birth weight have little tissue of body reserves; they are less vigorous at lambing; they have a lower body temperature and they take longer time to stand up and ingest the colostrum (Dwyer & Morgan, 2006). Darwish and El-Bahr (2007) also observed that the increase in lamb's birth weight was associated with the speed to stand up and ingest colostrum. Assessing the amount of time lambs spend to stand up and suckle, Aita et al. (2012) observed that lambs spent between 5 and 58 min (mean 21 min) and between 9 and 120 min (mean 60 min), respectively, after birth, whereas Rech et al. (2008) reported an average of 23 min (9-62 min) to lift up and 10 min (3-30 min) to suckle.
The average lamb weight at birth, 5.0 [+ or -] 1.1 kg, showed no significant correlation with MBS (Table 1), but was correlated negatively with the number of lambs born per birth (r = -0.34, p < 0.05) and positively with average placental weight (r = 0.44, p < 0.05) and survival at weaning (r = 0.33, p < 0.05). Current assay registered that perinatal mortality of lambs caused by low birth weight, 8.0% in this study, was not affected by MBS. The limited effect of maternal-filial relationship indicates that probably other problems of newborn animals, such as reduced energy reserves, coupled with the difficulties of the environment, are more strongly related to high mortality of low weight lambs, than the maternal-filial behavior.
The lamb weight at birth depends on the type of lambing: single birth lambs are heavier than those in multiple births (Dwyer et al., 2003; Rech et al., 2008), highly correlated with placental weight (Mellor, 1983) and associated with the offspring's growth and survival potential. In current study, average lamb weights of single and twin born were 4.87 and 3.83 kg respectively. Average placental weights of lambs born from single and twin lambing were respectively 436.89 and 278.57 g. Table 2 shows average body condition score of ewes, live weight of lambs and placentas.
Ewes with low body condition score tend to look for food soon after lambing, leaving or remaining less time in lamb care. Low body condition score and weight of ewe at birth (Table 2) may explain the low MBS because, according to Aita et al. (2012), there is a positive correlation between MBS and lamb weight at weaning (r = 0.42).
Maternal-filial behavior and ewes--lambs performance in current analysis did not differ between animals classified with worse and better maternal behavior score (MBS) (p > 0.05), and showed low correlation between MBS and productive performance of lambs, for example, birth weight and weaning weight (Table 1). These data corroborate with reports by Aita et al. (2012) who also registered low MBS correlation with the age of ewe, with the ewe's weight at birth and at weaning, the behavior of isolation of the flock before lambing, with the act of licking and smelling of the lamb and vocalization, with the time the lamb spend to stand up and suckle, and with the lamb live weight gain from birth to weaning.
Similarly, Rech et al (2008) found no significant difference with the time lambs spent to stand up, latency to ingest colostrum and the attitude of cleaning the lamb in relation to MBS. Yilmaz, Karaca, Bingol, Kor, and Kaki (2011) found no effect of MBS on weaning weight and survival rate of lambs. However, these results differ from the results by Everett-Hincks, Lopez-Villalobos, Blair, and Stafford (2005) and by Ekiz, Kocak, Ozcan, and Yilmaz (2007) in which better MBS occurred in older animals with multiple births.
MBS showed no significant correlation with the performance of ewes and lambs until weaning (p > 0.05) (Table 1). According to Everett-Hincks et al. (2005), genetic selection of animals through the maternal-filial behavior in New Zealand is inefficient. Result indicates that it is important to consider the environment and management techniques to improve maternal-filial relationship and lamb survival.
Ewes showed adequate behavior of looking after their offspring, facilitating colostrum intake and vocalizing for recognition. The lack of MBS correlation with the ewe's behavior at lambing, lamb survival rate and lamb weight gain until weaning limits its use to estimate these attributes.
The authors would like to thank Dr. Zelia Maria de Souza Castilhos and MSc. Flavio Conde Albite da Silva for their very important participation and help. Graduate students were supported by grants from the Capes, Ministry of Education of Brazil. We thank two anonymous referees for their helpful comments and suggestions for the improvement of the manuscript.
Aita, M. F., Fischer, V., Poli, C. H. E. C., Osorio, M. T. M., Silveira, I. D. B., Sebolt, M. B., ... Losekann, P. B. (2012). Relacao entre o escore de comportamento materno e as caracteristicas fisiologicas de ovelhas. Revista Brasileira de Zootecnia, 41(4), 1035-1043.
Arnold, G. W., & Morgan, P. D. (1975). Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Applied Animal Ethology, 2(1), 25-46.
Asmad, K., Kenyon, P. R., Pain, S. J., Parkison, T. J., Peterson, S. W., Loez-Villalobos, N., & Blair, H. T. (2014). Effects of dam size and nutrition during pregnancy on lifetime performance off female offspring. Small Ruminant Research, 121(2-3), 325-335.
Bickell, S. L., Nowak, R., Poindron, P., Ferguson, D., & Blache, D. (2010). Maternal behaviour at parturition in outdoor conditions differs only moderately between single-bearing ewes selected for their calm or nervous temperament. Animal Production Science,50(7), 675-682.
Ceyhan, A., Sezenler, T., Yuksel, M. A., & Yildirir, M. (2012). Maternal and lamb behaviour of the Karacabey Merino ewes at pre- and post-parturition. Research Opinions Animal and Veterinary Sciences, 2(6), 402-409.
Clarke, L., Heasman, L., Juniper, D.T., & Symonds, M. E. (1998). Maternal nutrition in early-mid gestation and placental size in sheep. British Journal of Nutrition, 79(4), 359-364.
Corner, R. A., Kenyon, P. R., Stafford, K. J., West, D. M., Morris, S. T., & Oliver, M. H. (2010). The effects of pasture availability for twin-and triplet-bearing ewes in mid and late pregnancy on ewe and lamb behaviour 12 to 24 h after birth. Animal, 4(1), 108-115.
Corner, R. A., Mulvaney, F. J., Morris, S. T., West, D. M., Morel, P. C. H., & Kenyon, P. R. (2013). A comparison of the reproductive performance of ewe lambs and mature ewes. Small Ruminant Research, 114(1), 126-133.
Darwish, R. A., & El-Bahr, S. M. (2007). Neonatal lamb behaviour and thermoregulation with special reference to thyroid hormones and phosphorous element: Effect of birth weight and litter size. Beni-Suef Veterinary Medical Journal, 18(1), 120-127.
Dwyer, C. M. (2008). Genetic and physiological determinants of maternal behavior and lamb survival: Implications for low-input sheep management. Journal of Animal Science, 86(14), E246-E258.
Dwyer, C. M. (2014). Maternal behaviour and lamb survival: from neuroendocrinology to practical application. Animal, 8(1), 102-112.
Dwyer, C. M., & Morgan, C. A. (2006). Maintenance of body temperature in the neonatal lamb: Effects of breed birth weight, and litter size. Journal of Animal Science, 84(5), 1093-1101.
Dwyer, C. M., Lawrence, A. B., Bishop, S. C., & Lewis, M. (2003). Ewe-lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy. British Journal of Nutrition, 89(1), 123-136.
Dwyer, C. M., & Smith, L. A. (2008). Parity effects on maternal behavior are not related to circulating oestradiol concentrations in two breeds of sheep. Physiology & Behviour, 93(1), 148-154.
Ekiz, B., Kocak, O., Ozcan, M., & Yilmaz, A. (2007) Effects of parity and litter size on maternal behaviour in Kivircik ewes. Acta Agriculturae Scandinavica, 57(2), 81-88.
Everett-Hincks, J. M., Lopez-Villalobos, N., Blair, H. T., & Stafford, K. J. (2005). The effect of ewe maternal behaviour score on lamb and litter survival. Livestock Production Science, 93(1), 51-61.
Gomez, J. M. D., Fischer, V., Poli, C. H. E. C., Carvalho, P. C. F., Pegoraro, E. J., & Macari, S. (2010). Efeitos da oferta de forragem, do metodo de pastejo, dos dias de avaliacao e da raca no comportamento e temperamento de ovinos. Revista Brasileira de Zootecnia, 39(8), 1840-1848.
Grandinson, K. (2005). Genetic background of maternal behaviour and its relation to offspring survival. Livestock Production Science, 93(1), 43-50.
Hernandez, C. E., Matthews, L. R., Oliver, M. H., Bloomfield, F. H., & Harding, J. E. (2010). Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiology & Behavior, 101(5), 588-594.
Hernandez, C. E., Matthews, L. R., Oliver, M. H., Bloomfield, F. H., & Harding, J. E. (2009). Effects of sex, litter size and periconceptional ewe nutrition on the ewe-lamb bond. Applied. Animal Behaviour Science, 120(1), 76-83.
Hild, S., Andersen, I. L., & Zanella, A. J. (2010). The relationship between thermal nociceptive threshold in lambs and ewe-lamb interactions. Small Ruminant Research, 90(1), 142-145.
Hinch, G. N., & O'Brien, F. (2014). Lamb survival in Australian flocks: a review. Animal Production Science, 54(6), 656-666.
Levy, F., & Keller, M. (2008). Chapter 8 neurobiology of maternal behavior in sheep. Advances in the Study of Behavior, 38, 399-437.
Mariz, T. M. A., Pimenta Filho, E. C., Medeiros, A. N., Gonzaga Neto, S., Leite, S. V. F., & Torreao, J. N. C. (2007). Relacao materno-filial da raca Morada Nova recebendo dietas com tres niveis de energia, ao final da gestacao. Revista Brasileira de Zootecnia, 36(6), 1889-1893.
Mellor, D. J. (1983). Nutritional and placental determinants of foetal growth in sheep and consequences for the newborn lamb. British Veterinary Journal, 139(4), 141-150.
Nowak, R., Keller, M., Val-Laillet, D., & Levy, F. (2007). Perinatal visceral events and brain mechanisms involved in the development of mother-young bonding in sheep. Hormones and Behavior, 52(1), 92-98.
Nowak, R., Porter, R. H., Levy, F., Orgeur, P., & Schaal, B. (2000). Role of mother-young interactions in the survival of offspring in domestic mammals. Reviews of Reproduction, 5(3), 153-163.
Pickup, H. E., & Dwyer, C. M. (2011). Breed differences in the expression of maternal care at parturition persist throughout the lactation period in sheep. Applied Animal Behaviour Science, 132(1-2), 33-41.
Poindron, P. (2005). Mechanisms of activation of maternal behaviour in mammals, Reproduction, Nutrition, Development, 45(3), 341-351.
Rech, C. L. S., Rech, J. L., Fischer, V., Osorio, M. T. M., Manzoni, N., Moreira, H. L. M., & Tarouco, A. K. (2008). Temperamento e comportamento maternofilial de ovinos das racas Corriedale e Ideal e sua relacao com a sobrevivencia dos cordeiros. Ciencia Rural, 38(5), 1388-1393.
Rech, C. L. S., Tarouro, A. K., Fischer, V., Meira, A. N., Macedo, J. F., Lima, T. L., & Aita, M. F. (2011). Temperamento e comportamento materno ovino. Revista Brasileira de Reproducao Animal, 35(3), 327-340.
Russel, A. J. F., Doney, J. M., & Gunn, R. G. (1969). Subjective assessment of body fat in live sheep. Journal Agricultural Science, 72(3), 451-454.
Silveira, I. D. B., Fischer, V., & Mendonca, G. (2010). Efeito do genotipo e da idade de ovinos na reatividade medida em pista de venda. Revista Brasileira de Zootecnia, 39(10), 2304-2309.
Yilmaz, A., Karaca, S., Bingol, M., Kor, A., & Kaki, B. (2011). Effects of the maternal behavior score (MBS) on weaning weight and litter survival in sheep. African Journal of Agricultural Research, 6(6), 1393-2139.
Received on November 24, 2015.
Accepted on February 26, 2016.
License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Andreia Barros de Moraes (1), Cesar Henrique Espirito Candal Poli (1), *, Vivian Fischer (1), Neuza Maria Fajardo (1), Marta Farias Aita (2) and Gabriela Caillava da Porciuncula (1)
(1) Departamento de Zootecnia, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Avenida Bento Goncalves, 7712, 90540-000, Porto Alegre, Rio Grande do Sul, Brazil. 2Fundacao Estadual de Pesquisa Agropecuaria do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil. *Author for correspondence. E-mail: email@example.com
Table 1. Estimates of correlation (Spearman's Coefficient) between measures of behavior and performance of Corriedale ewes and their lambs, Viamao, Brazil, 2010. Correlated Variables Correlation Coefficient * SURV72 x TWLAMB 0.57 LAMBBW x PLACWEIG 0.44 MBS x LAMBWW 0.13 MBS x PLACWEIG 0.21 MBS x NLAMBBB -0.10 MBS x LAMBBW 0.36 * All correlation coefficients were not significant (p > 0.05). LAMBBW- lamb birth weight; PLACWEIG--placental weight; MBS--maternal behavior score; LAMBWW--lamb weaning weight; NLAMBBB--number of lambs born per birth, TWLAMB--total weight of lambs born per ewe; SURV72--survival rate in the first 72 hours. Table 2. Average rates of the performance variables of Corriedale ewes and their lambs, Viamao, Brazil, 2010. Mean Standard CV Deviation BCS ewe during breeding (1 to 5) 2,03 0.56 27.60 Ewe weight at lambing (kg) 58.03 4.85 8.37 BCS ewe at lambing (1-5) 2.32 0.51 22.06 Lamb weight at lambing (kg) 4.97 0.893 17.97 Lamb weight at lambing (kg) 384.86 128.29 33.33 Lamb weight at weaning (kg) 19.44 4.56 23.46 BCS lamb weaning (1-5) 2.67 0.51 19.05 Ewe weight at weaning (kg) 45.85 5.29 11.53 BCS ewe at weaning (1-5) 2.72 0.46 16.90 BCS--body condition score; CV--coefficient of variation.