Estimating the repeatability of behavioral traits in Norduz sheep subjected to an arena test

https://doi.org/10.1016/j.applanim.2022.105704Get rights and content

Highlights

  • The degree of behavioral responses in Norduz sheep has decreased over time.

  • The between-individual variation observed in sheep behavior is consistent.

  • The repeatability of behavioral variables in Norduz sheep varied from low to medium.

Abstract

The objective of this study was to estimate the repeatability of behavioral traits in sheep subjected to a 5-min arena test. Two separate tests were conducted over two years to assess the among-individual consistency of behavioral responses in 68 nonpregnant Norduz ewes (2–5 years of age). During each arena test, five behavioral variables were measured: distance to group sheep (DTG), locomotor activity (LOC), zone boundaries crossed (CRS), vocalization (VOC), escape attempts (ESC). A linear mixed model was used to predict DTG and LOC, while a GLMM with a Poisson distribution was used to predict VOC, CRS, and ESC. Age and year were used as fixed factors in both models. The effect of the year was statistically significant on DTG, LOC, and CRS (P < 0.05). The correlations between traits changed over time. In the first year, DTG had no correlation with other variables. However, DTG had a significant positive correlation with LOC (0.54) and CRS (0.64) in the second year. The repeatability of behavioral variables was estimated as linear mixed-effects models (LMMs) and generalized linear mixed-effects models (GLMMs). To estimate adjusted repeatability, the ewes' age and the year of testing were included as fixed effects. The ID of ewes was included as a random effect in all models. The effect of age was statistically significant on LOC and CRS (P < 0.05). The repeatability of behavioral variables varied from the lowest for the ESC (R = 0.10; 95 % CI [0.000, 0.389], P = 0.319) to the highest for the VOC (R = 0.38; 95 % CI [0.054, 0.614], P = 0.006). These results indicate the consistency of among-individual variation in sheep behaviors that was measured in the arena test.

Introduction

The concept of personality or temperament, as consistent behavioral variations observed among individuals of the same species or even the same breed in response to stressors, has become an important topic in animal behavioral research due to its potential to contribute to improved livestock management, productivity and welfare (Van Reenen et al., 2013, Brown et al., 2016, Safryghin et al., 2019, Çakmakçı et al., 2021, Manrique et al., 2021). Although many species of animals have stable character traits, there is no consensus on the terms used to describe and categorize character traits (Jones and Gosling, 2005, MacKay and Haskell, 2015). Individual variations in behavioral patterns and physiological characteristics that are consistent over time and across different contexts or situations (Reale et al., 2000, Coppens et al., 2010) are most often referred to as temperament, behavioral syndrome, personality, or coping style in different animal species (Finkemeier et al., 2018). Individuals vary in behavior because they differ in state, and they adapt their behavior to these differences. The state involves labile characteristics of the individual, such as energy reserves, condition or vigor, reproductive value, physiology, morphology, which affect the cost and benefit of behavioral actions (Sih et al., 2015). In this context, individual differences in farm animals have been associated with welfare and production attributes (Finkemeier et al., 2018). Based on their flight speed, Nellore young bulls with calm temperament had higher average daily gain and body weight than intermediate and reactive bulls, as well as heavier carcasses at the end of the finishing period (Braga et al., 2018). With a higher ovulation rate and a higher number of multiple pregnancies, the reproductive performance of Merino ewes with calm temperament was superior to that of nervous ewes (van Lier et al., 2017). Fattening performance of calm Karakaş ram lambs was better to that of restless lambs (Çakmakçı et al., 2021), and the meat quality of calm Hu ram lambs was superior to that of nervous lambs (Zhang et al., 2021).

Between-individual variation in the mean values of behavioral variables in a population is often characterized by repeatability (Hertel et al., 2020). Repeatability, an index for quantifying the accuracy and consistency of phenotypic measurements, is an important tool for behavioral studies (Nakagawa and Schielzeth, 2010) that can be defined mathematically in terms of repeatable differences among individuals (Dochtermann et al., 2015). Partitioning of the variance corresponding to repeatability is a useful measure of variation for behavioral studies due to its relationship to heritability (Boake, 1989). It has some practical implications for breeding programs (Falconer and Mackay, 1996). The proportion of the variance attributed to variation among individuals is most often estimated as the intraclass correlation coefficient (Wolak et al., 2012), and it is also often considered that it sets an upper limit for the heritability of traits (Falconer and Mackay, 1996). Several studies have reported individual behavioral variation in different species of animals, see reviews by (Giles and Kilgour, 1999, Koolhaas et al., 1999, Rauw et al., 2017), including sheep (Salvin et al., 2020, Schiller et al., 2020, Bonato et al., 2021, Çakmakçı et al., 2021, Zhang et al., 2021, Çakmakçı, 2022), goat (Nawroth et al., 2017, Neave and Zobel, 2020), cattle (Van Reenen et al., 2013, Marçal-Pedroza et al., 2020, Yu et al., 2020), pig (Yoder et al., 2011, Kanitz et al., 2019), horse (Rosselot et al., 2019, Manrique et al., 2021) and laying hens (Bennewitz et al., 2014, Rozempolska-Rucińska et al., 2017). However, repeatability has been hardly addressed in studies examining personality, temperament, and coping styles in farm animals. Boake (1989) states that only traits that are consistent within individuals and different between individuals can respond to selection, and thus repeatability can be used to indicate whether efforts to measure heritability are likely to be worthwhile. Therefore, defining personality mathematically in terms of repeatability makes it possible to make general inferences about the degree to which variation in animal personality is genetically determined (Dochtermann et al., 2015). The objective of this study was to estimate the repeatability of the behavioral responses of sheep exposed to an arena test.

Section snippets

Animals

This study used 68 nonpregnant Norduz ewes (2–5 years of age), a fat-tailed breed native to the province of Van, Turkey. The ewes were tested in the fall, four months after their lambs were weaned. From early spring to late fall, the ewes were kept as a single flock on the same research farm on a natural pasture composed mainly of legumes and grass. From late fall until the next grazing season, they were housed indoors and fed alfalfa hay and a barley-based diet. The study was carried out at

The effects of age and test year on behavioral traits

Using age and year as fixed factors, a linear mixed model was used to predict DTG and LOC, while a GLMM with Poisson distribution was used to predict VOC, CRS, and ESC. The models included ID as a random effect. The models’ intercepts correspond to AGE = 2 and Year = 1 (Fig. 2). The effect of age is statistically significant on LOC and CRS (Fig. 2). The effect of the year is statistically significant on DTG, LOC, and CRS (Fig. 2). The effect of year is statistically non-significant on VOC and

Discussion

Animals differ individually in terms of their ability to cope with the social consequences of living in a group. Coping, which can be genetic, is manifested by individual differences in physiological, endocrine-immune, and behavioral mechanisms (Giles and Kilgour, 1999). These individual differences in temperament can affect how animals respond to novel environments in various social contexts (Reale et al., 2000). Farm animals can be classified according to their temperament, which has

Conclusion

Repeatability is one of the important parameters for designing effective breeding plans in animal husbandry, and it allows animal breeders to assess whether a particular trait can be improved by selection, ultimately improving management practices and animal welfare. Two separate tests, carried out over two years showed that the among-individual consistency of behavior responses was medium to low. These results indicate that the consistency of among-individual variation in behavioral variables

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The author alone is responsible for the content and writing of the paper.

Declaration of Competing Interest

The author declares that he has no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The author would like to acknowledge his gratitude to Serhat Karaca, Mustafa Can Yılmaz and Muammer Sarıbey for their assistance in the testing process and would also like to thank the staff of research farm at Van Yüzüncü Yıl University for their assistance in the handling of animals. The author is grateful to two anonymous reviewers for the thorough and constructive comments on prior versions of this manuscript.

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