Environmental and Genetic Effects of Reactivity Traits in Île-de-France x Texel Crossbred Lambs

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1 Acta Scientiae Veterinariae, : RESEARCH ARTICLE Pub ISSN Environmental and Genetic Effects of Reactivity Traits in Île-de-France x Texel Crossbred Lambs Priscilla Regina Tamioso, Laila Talarico Dias, Rodrigo de Almeida Teixeira, Bárbara Mazetti Nascimento, Gisele Ferreira da Silva & Juliana Varchaki Portes ABSTRACT Background: Reactivity in livestock species has been assessed in relation to the behavioral reactio of animals, through restrained and non-restrained tests. Environmental and genetic parameters for reactivity traits have been reported for farm animals, as sheep, providing support for the possibility of direct selection. Despite evidences, there is little information on how genetic and environmental factors affect the expression of reactivity in sheep during and after weighing. Therefore, this study aimed to estimate the environmental and genetic effects of reactivity traits in Île-de-France x Texel crossbred lambs. Materials, Methods & Results: Reactivity traits from 188 Île-de-France x Texel cross lambs, aged between 28 and 110 days-old, were assessed in two situatio: 1- During weighing: a. vocalization (VOC), b. movement (MOV), c. teion (TEN), d. exploratory behavior (EB) and e. ears posture (EP), and 2- After exiting the weighing crate, in a chute, through: a. gait speed (GS) and b. flight speed (FS) tests. For the study of environmental effects the model coidered the fixed effects of month of assessment, sex and management group and as covariates, the linear effects of type of birth, age of dam and age of lamb. The (co)variance and genetic parameters were estimated using REML in univariate analysis and the direct additive genetic effect was coidered in the model as a random effect. From all the environmental effects, month of assessment was statistically important over all the reactivity traits. Similarly, the effects of age of dam and age of lamb were significant for almost all variables. The estimates of heritability and repeatability for the behavioral variables ranged from low to moderate magnitudes, with high standard errors, for VOC: 0.19 ± 0.17 and 0.15 ± 0.05, MOV: 0.21 ± 0.07 and ± 0.02, TEN: 0.27 ± 0.19 and 0.16 ± 0.13, EB: 0.16 ± 0.12 and 0.13 ± 0.03, EP: 0.23 ± 0.19 and 0.21 ± 0.15, GS: 0.22 ± 0.16 and 0.13 ± 0.11 and FS: ± 0.13 and 0.11 ± 0.06, respectively, indicating low possibility of direct selection and lowly repeatable behavioral respoes over time. Discussion: The results showed the significant influence of type of management on the majority of variables, fact that may be explained by different management systems to which the animals were subjected, in addition to the weaning effect. The absence of significant effect of sex on reactivity variables contradicts previous findings, in which males were found to be less reactive than females. Regarding the genetic parameters, few estimates of heritability for reactivity traits have been reported for sheep, mainly assessed in the arena test. Such results differ from those obtained in the present study which were lowly and moderately heritable, but with high standard errors, probably due to the small number of animals and the structure of the relatiohip matrix. The coefficients of repeatability for the evaluated traits during and after weighing were also low, thus measurements in the first evaluatio were relatively poor predictors of the same behavioral respoes on subsequent situatio. Although a relatively small number of animals were used in the present study, it was possible to estimate genetic parameters for reactivity traits assessed during and after weighing. Thus, it is necessary to invest in selection, as reactivity has important influence on ease of handling and animal welfare. Keywords: Behavioral scores, heritability, repeatability, sheep, temperament. Received: 12 February 2015 Accepted: 6 June 2015 Published: 30 June 2015 Departamento de Zootecnia, Universidade Federal do Paraná (UFPR), Setor de Ciências Agrárias, Curitiba, PR, Brazil. CORRESPONDENCE: P.R. Tamioso [priscillatamioso@gmail.com - Fax: +55 (41) ]. Rua dos Funcionários, n.1540, Bairro Cabral. CEP Curitiba, PR, Brazil. 1

2 INTRODUCTION Information on livestock behavior and how the animals interact with huma are helpful once it contributes to optimize production systems, by improving management, domestication and welfare. In general, for animal production, there is a great interest in less reactive individuals, being the selection based on records of behavioral measures. In sheep, reactivity has been assessed through several behavioral tests. They include non-restrained tests, such as the arena test [2], aversion and flight distance tests [11], conflict and corridor tests [5], flight speed test [3,19], open-field test [2] and surprise test [22,25] and restrained methods, performed in isolation boxes [1,19] and at weighing [13,19]. It is known that reactivity in sheep may be influenced by different environmental factors, as rearing type [11], breed [22], sex [25] and age of the animal [26], among others. Such environmental effects have been studied and included in genetic models, allowing accurate identification of more and less reactive individuals. Likewise, genetic parameters for reactivity traits, as heritability and repeatability, have been reported for sheep, ranging from moderate to high magnitudes [14,15,27]. Such results provide support for the possibility of direct selection. However, there is little information about how genetic and environmental factors affect reactivity in sheep during and after weighing. The aim of this study was to estimate the environmental and genetic effects of reactivity traits in Île-de-France x Texel crossbred sheep. MATERIALS AND METHODS The study was carried out on a commercial farm, located in Reserva, Parana, South of Brazil. A total of 188 Île-de-France x Texel crossbred lambs born in June, July and August 2012, aged between 28 and 110 days old were used. All the animals were assessed once a month, during three coecutive months (July, August and September 2012) and were kept in pasture systems. The flock had undergone no previous direct selection for reactivity traits. Part of the lambs (n = 98) was weaned at 60 days of age, on average, and maintained as a single flock. All the individuals were frequently handled. The other animals (n = 90) remained with their mothers in two different management systems/treatments: lambs which 2 regularly received human contact (n = 75) or experienced little contact with huma (n = 15), handled at least once a week for about 60 min. The routine management activities included weighing, de-worming and vaccination. Behavioral observatio started right after the entry of the lamb in the weighing crate. Reactivity was assessed in two situatio: 1)- Weighing crate (AÇÔRE ) 1 [1.63 m length, 1.30 m width and 1.34 m height, and side walls formed by parallel grids]: a test was applied for 40 s and five behavioral categories from a scoring system were coidered: vocalization (VOC), movement (MOV), teion (TEN), exploratory behavior (EB) and ears posture (EP). These variables were previously described by Tamioso et al. [24]. The distribution of the scores is presented in Table 1. Three previously trained observers (OB1, OB2 and OB3) performed the evaluatio simultaneously and registered the scores, which were unanimously agreed in all assessments; 2)- Chute: after released from the weighing scale, the animals were evaluated in a chute, similar to a corridor (2.3 m long x 1.0 m high), with lateral covered walls. In this case, the gait speed (GS) and flight speed (FS) tests were used. The first one was adapted from the method described by Grandin et al. [9] and it aims to measure the animals reactivity through their mobility in a given distance (1.5 m), after released from the weighing platform into an open yard. Similarly, the flight speed test is the time taken by the animal (expressed by m/s) to cover a certain distance [7]. For the performance of GS and FS, the same distance was coidered and the evaluators were positioned at about 0.70 m from the chute. Lambs which remained in the weighing crate for more than 40 s, thus requiring the intervention of an observer to remove them, were not evaluated through these tests (n = 15). The assessments of the variables ears posture and flight speed were conducted by a single observer (OB1). They were evaluated from video footages taken during and after weighing. For EP only the prevailing posture was registered, according to description by Boissy et al. [4]. For FS the recordings were analyzed through Windows Movie Maker program. A total of 564 reactivity records from 188 lambs assessed during weighing were analyzed. The data set coisted of 91 males and 97 females, offspring of 67 dams (Île-de-France and Île-de-France x Texel) and 2 rams (Île-de-France). The estimates for GS and FS included over 549 records (84 males and

3 89 females). The study of environmental effects was carried out using the GLIMMIX procedure of SAS software [23] according to the following model: Y ijklmn = µ + MA i + Sex j + MG k + TB l + AD m + AL n + e ijklmn where Y ijklmn = the observed value of the dependent variables (reactivity traits assessed during and after weighing); µ = overall mean of the dependent variable; MA i = effect of the i-th month of assessment; Sex j = effect of the j-th sex of the animal; MG k = effect of the k-th management group; TBl = linear effect of the l-th type of birth, as a covariate; AD m = linear effect of the m-th age of dam, as a covariate; AA n = linear effect of the n-th age of lamb, as a covariate; e ijklmn = random error associated with each observation. In order to estimate the genetic parameters, the model can be described in matrix form: Y = Xβ+Za+Wp+ e where Y is the vector of observatio (reactivity traits assessed during and after weighing); β, a and p are the vectors of fixed, direct additive genetic and maternal environmental permanent effects (coidered for the estimation of repeatability coefficients), respectively; X, Z and W are the incidence matrices related to the respective effects; e is the vector of random residuals. The (co)variance components and the estimates of heritability and repeatability were obtained using the derivative-free restricted maximum likelihood method through the software Wombat [16]. RESULTS Table 2 presents the summary of the analysis of variance for the studied behavioral traits. From Table 2, it is possible to observe that month of assessment was statistically important over all the reactivity traits. Likewise, the effects of age of dam and age of lamb were significant for all variables except for ears posture and gait speed test. The estimates of (co)variance components as well as the heritability and repeatability coefficients for the reactivity variables are shown in Table 3. The behavioral traits assessed during and after weighing were lowly to moderately heritable (0.16 to 0.27) with high standard errors (Table 3). This may be explained by the small number of lambs and the structure of the relatiohip matrix. Similarly, estimates of repeatability for the reactivity variables ranged from low to moderate magnitudes (0.06 to 0.21) also with high standard errors. Table 1. Descriptive statistics of reactivity traits assessed during and after weighing, in Île-de-France x Texel cross lambs. Trait Unit Mea SD Min Max Structure VOC N Classes MOV N Classes TEN N Classes EB N Classes EP N Classes GS N Classes FS S Continuous VOC = vocalization; MOV = movement; TEN = teion; EB = exploratory behavior; EP = ears posture; GS = gait speed; FS = flight speed; Unit: N = number; S = seconds; SD = standard deviation; Mini = minimum; Maxi = maximum. Table 2. Summary of the analysis of variance for vocalization (VOC), movement (MOV), teion (TEN), exploratory behavior (EB), ears posture (EP), gait speed (GS) and flight speed (FS) tests, in Île-de-France x Texel cross lambs. Sources of variation Traits MA Sex MG TB AL AD VOC ** ** ** * MOV ** * ** ** TEN ** * ** * EB ** * * EP * ** GS ** FS ** * * * **P < 0.01; *P < 0.05; : non significant; MA: month of assessment; Sex: sex; MG: management group; TB: type of birth; AL: linear effect of age of lamb; AD: linear effect of age of dam. 3

4 Table 3. (Co)variance components and estimates of heritability and repeatability for vocalization (VOC), movement (MOV), teion (TEN), exploratory behavior (EB), ears posture (EP), gait speed (GS) and flight speed (FS) tests, in Île-de-France x Texel cross lambs. Traits σ 2 a σ 2 p h 2 ±se t±se VOC ± ± 0.05 MOV ± ± 0.02 TEN ± ± 0.13 EB ± ± 0.03 EP ± ± 0.15 GS ± ± 0.11 FS ± ± 0.06 σ 2 : direct additive genetic variance; a σ2 phenotypic variance, p: h2 : direct heritability; t: repeatability; se: d standard error. DISCUSSION Among the environmental effects, only the month of assessment was significant on all reactivity traits. Boissy et al. [5] found that the rearing type, age of dam and age of lamb were not significant on temperament traits evaluated during the arena, conflict and corridor tests. Likewise, Wolf et al. [27] reported that in Bluefaced Leicester crossbred lambs the rearing type also showed no significance on traits measured in the arena test. The authors suggested that, since the human contact influences fear reactio (especially in young individuals), the level of human-sheep contact across the farm of origin (three different farms were coidered) was probably the same. In the present study, although all the animals have been evaluated in the same farm, they were subjected to different management systems, in addition to the weaning effect, which may explain the significant influence of type of management on the majority of variables. The effect of month of assessment also corroborates such results. The absence of significant effect of sex on reactivity variables contradicts previous findings, in which males were found to be less reactive than females [5] and less reluctant to approach or make physical contact with huma or novel object [25]. According to Dodd et al. [8], behavioral differences can be expected between males and females, since ewes are more likely to have higher locomotor activity, and this fact may be justified by the sexually dimorphic glucocorticoid regulation and social motivation. In reports about the influence of environmental effects on sheep reactivity, type of birth is usually disregarded or fitted in analysis of ewe mothering temperament [21]. However, it is known that twin-born lambs are less likely to be fed by their own mothers. Thus, it is necessary to rear them artificially, which may influence their reactive behavior. Likewise, it is believed that the age of dam is also an important factor due to learning and habituation to management practices and human presence, not only the maternal experience itself. It can be also explained for the age of lamb, since adult animals are less reactive [11]. Regarding the genetic parameters, few estimates of heritability for reactivity traits have been reported for sheep. Most variables, mainly assessed in the arena test, have coefficients ranging from moderate to high ( ) [5,27]. These are different from those obtained in the present study which were lowly and moderately heritable, but with high standard errors. Similar to the variable movement assessed in this research, and its h 2 coefficient (0.21 ± 0.07), Plush et al. [21], in Merino sheep (n = 1935), found a moderately heritable estimate equal to 0.20 ± 0.05 for agitation score, a measure of frequency and inteity of locomotor activity. This favorable result supports the idea that it is possible to perform direct selection from this trait. For flight speed, most of the estimates in the literature concern beef cattle, since this method is mainly applied to this species. In these studies, the coefficients ranged from low to moderate magnitudes: 0.15 ± 0.06 and 0.33 ± 0.10 [12] and 0.35 [6]. For sheep, heritability estimates for FS were equal to 0.15 ± 0.01 (n = 1763) [3] for White Suffolk, and 0.12 ± 0.05 (n = 1847) [21], indicating low respoe to direct selection or slow genetic progress. Nevertheless, it is 4

5 suggested to invest in selection for FS in sheep, since it is an objective, easily applicable and simple method to be implemented in commercial herds, therefore, a valuable tool used for selection purposes. On the other hand, there is no data published for this species when it comes to gait speed test. The coefficients of repeatability for the evaluated traits during and after weighing were low, thus measurements in the first evaluatio were relatively poor predictors of the same behavioral respoes on the subsequent situatio. These results may be due to learning experience. Repeatability estimates for sheep have been described from moderate to high, and were obtained mainly for traits assessed in the arena test, including the number of bleats: 0.25 [14] and 0.57 [15], number of squares entered: 0.57 [18] and the number of approaches to human: 0.17 to 0.44 [27] and in isolation boxes: [3] and 0.77 [18]. In relation to the traits assessed during restraint, there are few estimates of repeatability in the literature. However, it is known that variables measured at weighing are objective and easily incorporated into management practices. Horton and Miller [13] found for sheep at different age classes repeatability coefficients for activity scores higher than 0.44, suggesting a coistent pattern among animals over time. Some research shows that flight speed in cattle is highly repeatable, ranging from 0.31 [10] to 0.68 [20]. On the other hand, for sheep, Blache and Ferguson [3] reported low repeatability equal to (coidering 1 m after exiting the isolation box) and (2 m). More studies may be necessary to test FS on a larger sample size, investigate the animals behavioral reactio and validate this methodology for different sheep breeds. Hence, although a relatively small number of animals were used in the present study, it was possible to estimate genetic parameters for reactivity traits assessed during and after weighing. CONCLUSIONS The heritability coefficients estimated for reactivity traits assessed during and after weighing indicate that selection for these traits will generate slow genetic progress. Likewise, the repeatability estimates which were low in magnitude suggest that the reactive behavior evaluated during restraint is unlikely to be perpetuated. The inclusion of the assessed traits as selection criteria in breeding programs may assist in maintaining or improving the adaptability of lambs to management systems and their welfare. MANUFACTURER 1 Balanças Açôres. Cambé, PR, Brazil. Acknowledgments. The authors would like to acknowledge the Brazilian Agency for Support and Evaluation of Graduate Education (Capes), for funding and supporting the project, as well as Julio Pisani, Odilei Prado, Vanessa Carli Bones, Carolina Abrahão, Elaine Cristina de Oliveira Sa and the staff from the commercial farm where this study was carried out. Ethical approval. All procedures involving animals were approved by the Universidade Federal do Paraná (UFPR) Ethics Committee on Animal Use (CEUA - UFPR protocol number 21/2011). After the experimental period, the animals remained on the farm of origin, under the described maintenance and husbandry procedures. Declaration of interest. The authors report no conflicts of interest. The authors alone are respoible for the content and writing of the paper. REFERENCES 1 Beausoleil N.J., Blache D., Stafford K.J., Mellor D.J. & Noble A.D.L Exploring the basis of divergent selection for temperament in domestic sheep. Applied Animal Behaviour Science. 109: Bickell S., Poindron P., Nowak R., Chadwick A. Ferguson D. & Blache D Genotype rather than non-genetic behavioural tramission determines the temperament of Merino lambs. Animal Welfare. 18: Blache D. & Ferguson D Increasing sheep meat production efficiency and animal welfare by selection for temperament. Final Report SHGEN.025. Meat and Livestock, Boissy A., Aubert A., Désiré L., Greiveldinger L., Delval E. & Veissier I Cognitive sciences to relate ear postures to emotio in sheep. Animal Welfare. 20: Boissy A., Bouix J., Orgeur P., Poindron P., Bibe B. & Le Neindre P Genetic analysis of emotional reactivity in sheep: effects of the genotypes of the lambs and of their dams. Genetitcs Selection Evolution. 37:

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