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Effects of behavioral reactivity on production and reproduction traits in Dorper sheep breed
Journal of Veterinary Behavior 10 (2015) 365e368
Contents lists available at ScienceDirect
Journal of Veterinary Behavior journal homepage: www.journalvetbehavior.com
Research
Effects of behavioral reactivity on production and reproduction traits in Dorper sheep breed Dinu Gavojdian a, b, *, Ludovic T. Cziszter c, Csilla Budai a, Szilvia Kusza a a
Institute of Animal Science, Biotechnology and Nature Conservation, University of Debrecen, Debrecen, Hungary Research and Development Station for Sheep and Goats, Romanian Academy for Agricultural and Forestry Sciences, Caransebes, Romania c Department of Animal Production Engineering, Banat’s University of Agricultural Sciences and Veterinary Medicine ‘King Michael I of Romania’, Timisoara, Romania b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 January 2015 Received in revised form 23 February 2015 Accepted 27 March 2015 Available online 9 April 2015
The aim of the current research was to evaluate the effects of behavioral reactivity on production and reproduction performance in Dorper sheep, a meat breed. Temperament of animals was subjectively evaluated using a 5-point scoring system at weighing, during which sheep spent 30 seconds on the scale. The heritability of temperament was low (0.10 0.03). Estimated phenotypic (rp) and genetic (rg) correlations between temperament and litter size in ewes were negative and negligible (P > 0.05) at 0.06 0.18 and 0.08 0.09, respectively. Significant genetic correlations were found between lamb temperament and preweaning growth rate (rg ¼ 0.44 0.07, P 0.05) and postweaning growth till the age of 120 days (rg ¼ 0.52 0.08, P 0.05). Significant genetic correlations were found between lamb temperament and growth rates during their first 3 months of age. As a result, selection for calm temperaments should translate to increased growth rates of lambs. Negative correlations between temperament and production traits, both in ewes and lambs, suggested that selection against animals that are highly reactive to improve welfare and ease of handling would not have detrimental impacts on productivity. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: Dorper breed behavior genetic parameters growth rates sheep welfare temperament
Introduction Temperament in livestock species can be defined as the manner in which an individual reacts to a novel or challenging situation (Reale et al., 2000), and assessing temperament has been suggested as a useful tool for improving productivity in sheep (Dodd et al., 2012). Temperament has been shown to have an effect on lamb survival and growth rate (Murphy, 1999; Pajor et al., 2008), meat quality (Ferguson and Warner, 2008), and sheep reproductive performance (Blache and Bickell, 2011). Moreover, animals that are highly reactive to humans and handling exhibit poor adaptation to their environment and experience high levels of stress, reducing their level of welfare (Bickell et al., 2009).
Sheep temperament is regarded to be low to moderately heritable, thus making it a suitable trait for genetic selection (Lennon et al., 2009; Plush et al., 2011; Hawken et al., 2012). However, variation of temperament heritability between sheep breeds has been reported (Blache and Ferguson, 2005). When selecting sheep based on behavioral reactivity, it is important that the subsequent impact on other aspects of productivity is understood (Dodd et al., 2014). Dorper is among the very few sheep breeds to have temperament included as selection trait in the breed’s standard in native South Africa (Njisane and Muchenje, 2013). The aim of the current research was to evaluate the effects of behavioral reactivity on production and reproduction performances in Dorper meat breed. Materials and methods
* Address for reprint requests and correspondence: Dinu Gavojdian, Research and Development Station for Sheep and Goats, Romanian Academy for Agricultural and Forestry Sciences, Caransebes 325400, Romania. Tel: þ40 723 375 804; Fax þ40 356 456 400. E-mail address: [email protected] (D. Gavojdian). http://dx.doi.org/10.1016/j.jveb.2015.03.012 1558-7878/Ó 2015 Elsevier Inc. All rights reserved.
Animals and management The study was carried out at the Experimental Farm of the University of Debrecen (47 330 N/21420 E), between February and
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D. Gavojdian et al. / Journal of Veterinary Behavior 10 (2015) 365e368
July 2014. Purebred Dorper sheep were managed semi-intensively under an accelerated mating system (3 lambings/2 years). The Debrecen region has a typical Central European humid continental climate. At the research station, which is located at an elevation of 121 m above sea level. The total annual precipitation is 566 mm, with a mean annual temperature of 9.85 C. Temperatures show seasonal patterns with summer daily means of 20.3 C in July and winter daily means of 2.6 C in January. Data from 161 animals (72 ewes, 86 lambs, and their sires) and more than 720 records were analyzed for estimation of the genetic parameters for temperament and correlations of behavioral reactivity with production traits. Ewes were between 1.5 and 8 years old, with balanced age and parity within the flock and representing a diverse sampling of genetic lines (imported from Austria, Canada, Germany, and Romania). Individual lamb record data included birth type, sex, ear tag number, birth date, dam and sire, temperament (lamb, dam, and sire temperament scores), and lamb weight at birth and at 80, 120, 140, and 150 days of age (International Committee for Animal Recording [ICAR] “B” method). For adult ewes, body weight before the next reproduction season (1.5 months after litter weaning), litter size, and temperament were recorded. Lambs were weaned at 80 days and fed ad libitum with medium-quality lolium hay (8 megajoules [MJ] metabolizable energy [ME]/kg dry matter [DM]) and commercially available pellets (16% protein, 10.6 MJ/kg DM). During lactation and after weaning, the lamb’s ewes received a high-quality alfalfa hay (9.5 MJ ME/kg DM) ad libitum, and while suckling, they received concentrated supplements (200 g/d). The concentrate was comprised of corn (50%), wheat (20%), soybean meal (18%), sunflower meal (10%), calcium (1%), and a vitamine mineral supplement (1%). In addition, all animals had free access to potable water and mineral blocks. Both ewes and their lambs were kept confined on deep straw bedding, with a space allowance of 1.2 and 1 m2, respectively. All data were recorded in a single reproductive cycle to limit to the extent possible the effects of farm, year, and season. The Dorper breed was introduced in Hungary in 2008, with a current census of roughly 100 breeding ewes being registered in the breed’s herd book. The Hungarian Sheep and Goats Breeders Association manages the performance and recording scheme for the breeds. The production system focuses exclusively on meat production, with Dorper rams being used as terminal sires for the improvement of growth rates and carcass qualities in crossbreeding schemes with native breeds (Tsigai and Zackel). All research activities were performed in accordance with the European Union’s Directive for animal experimentation (Directive 2010/63/EU). Temperament assessment Temperament was assessed according to the scale test method described by Pajor et al. (2010) and Dodd et al. (2012), a subjective restraint method used to evaluate behavioral reactivity and fear response to handling. Temperament was scored at an age of 5 months for the lambs and right before admission to reproduction for the ewes. Behavior of all animals was recorded using a 5-point score system at weighing, where all animals spent 30 seconds on the scale: 1dcalm, no movement; 2dcalm with occasional movements; 3dmoderately movements; 4dabrupt episodic movements; and 5dcontinuous episodic movements. Scoring was done by 2 independent observers and videorecorded for re-evaluation, in case of divergent scoring. Based on temperament scores given, lambs and ewes were classified as either calm (scores 1 and 2) or nervous (scores 3, 4, and 5).
Statistical analysis Heritability was estimated using the threshold model described by Schaeffer (2014):
. h2temperament ¼ h2liability *z2 ðpð1 pÞÞ where h2liability is the heritability under normal distribution scale, z is the height of the normal curve at the threshold point (on the observed scale), and p is the proportion of observations in 1 category. The model included as fixed effects the lambs and birth type (singleton, twins, or triplets) and as random factors the dam and sire temperament scores. Phenotypic and genetic correlations of temperament scores of ewes and lambs with production traits were estimated using the analysis of variance described by Grosu and Oltenacu (2005). Comparisons between temperament scores for ewe weight at mating, litter size, and lamb growth rates were carried out using an analysis of variance main effects model. Chi-squared tests were performed to determine if ewe temperament influenced the litter size. All the statistical tests were done using Statistica software (StatSoft Inc.) (Hill and Lewicki, 2007). All decisions about the acceptance or rejection of statistical hypothesis were made at the 0.05 level of significance.
Results and discussions The heritability (standard error of the mean) of temperament in Dorper breed was low (h2 ¼ 0.10 0.031) and consistent with previous estimates in sheep (Plush et al., 2011; Dodd et al., 2014), which found low to moderate heritabilities for flight speed and agitation score. Conversely, Martin et al. (2004) estimated the heritability of temperament in sheep to be around 0.23 for the Allandale flock, which has been intensively selected for calm temperament over a period of 10 years. Notable breed disparities for behavior of sheep have been reported in a series of studies (Vierin and Bouissou, 2003; Pickup, 2004; Boissy et al., 2005; Konig von Borstel et al., 2011) and highlight the differences in propensity for behavioral reactions. This behavioral variation might contribute to differences for the heritability among sheep breeds. Despite that temperament was found to have a low heritability in the Dorper, given the feasibility of the scale test that can be easily applied at farm level, with both lambs and ewes being scaled on a regular basis (e.g., for drenching, performance recording), sheep breeders alone could assess the temperament of their sheep. Moreover, the scale test was found to have one of the highest repeatability (up to 0.71) when compared with other tests used to evaluate ovine behavioral reactivity (Dodd et al., 2012). Dorper lambs showed a higher behavioral reactivity (2.78 0.20) compared with their dams (2.40 0.16). Temperament scores of lambs are similar to those reported by Pajor et al. (2013) in Tsigai fattening lambs, evaluated by the same method. Habituation to handling might have contributed to the lower behavioral reactivity of ewes, as previously outlined by Erhard et al. (2006). Temperament of ewes had no significant effect (c2 ¼ 0.276, degrees of freedom ¼ 5, P ¼ 0.99) on the birth type, distribution of litter size was 53% singletons, 35% twins, and 12% triplets in ewes ranked as calm and 60% singletons, 27% twins, and 13% triplets in nervous ewes. Despite calmer ewes outperforming those ranked as nervous, and that less reactive lambs achieving higher growth rates (Table 1), differences between the 2 counterparts were not significant (P > 0.05). Results for ewes’ body weight are consistent with those previously reported (Amdi et al., 2010; Wolf et al., 2008), in which
D. Gavojdian et al. / Journal of Veterinary Behavior 10 (2015) 365e368
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Table 1 Means (SEM) for productive performances of ewes and lambs based on their temperament Trait Ewes performance Ewes weight (kg) Ewes litter size (%) Lambs ADG 0-80 d (g)b Lambs performance ADG 0-80 d (g) ADG 80-120 d (g) ADG 5 mo (g)
Cohort
Calm
Nervous
Differencesa
58.66 1.50 156.30 0.12 383.43 11.08
60.29 2.23 158.80 0.17 393.19 16.08
56.81 1.94 153.30 0.19 372.38 15.13
3.48NS 5.5NS 20.81NS
380.17 10.60 286.09 13.45 345.95 18.90
394.72 13.76 298.32 23.05 349.21 24.20
366.39 15.71 274.52 14.62 342.86 29.43
28.34NS 23.80NS 6.35NS
ADG, average daily gain; NS, not significant. a Calm versus nervous animals. b Regarded as dam effect.
no relationship was found between behavior and live weight, even if calmer ewes were heavier (þ3.48 kg, P > 0.05) than their nervous counterparts. Litter size of ewes was higher compared with data reported for the breed by Zishiri et al. (2013a), with calm ewes being more prolific (þ5%) compared with nervous animals. Growth rate of lambs from birth to weaning was attributed to maternal effects on growth rate until weaning, as previously demonstrated in the Dorper breed (Zishiri et al., 2013b). Lambs reared by calmer dams exhibited higher growth rates (þ20.8 g, P > 0.05) compared with those born by more reactive ewes. Lambe et al. (2001) found a positive genetic correlation (0.4) between ewe maternal score and lambs weight gain, demonstrating the importance of the temperament of ewes. Growth performances of lambs were higher compared with those reported by Cloete et al. (2000) and consistent with those of Snowder and Duckett (2003). Lowest growth rates were achieved by lambs during the 80-120 day interval, showing that postweaning stress affects the trait to a great extent. Less reactive lambs had higher growth rates compared with nervous lambs, in agreement with reports of Pajor et al. (2010) and of Horton and Miller (2011). Correlations, both genetic and phenotypic, between ewe behavioral reactivity and litter size and growth rates of unweaned lambs were negative in sign and not significant (P > 0.05) (Table 2). Significant negative phenotypic (rp ¼ 0.40, P 0.05) and genetic (rg ¼ 0.44, P 0.01) correlations were found between ewe temperament and body weight, thus, the more reactive the ewe the lower its body weight. In general, ewes in good body condition are desired because they tend to have higher reproductive performances (estrus onset, ovulation and conception rates, etc.) as reported by Sejian et al. (2010) and Yilmaz et al. (2011). The low heritability of temperament in the Dorper breed linked to its negligible negative genetic correlation with litter size suggests that selection for temperament traits will result in negligible genetic gain for prolificacy. Phenotypic correlations between temperament and average daily gains in lambs were nonsignificant (P > 0.05). These results
Table 2 Phenotypic (rp) and genetic (rg) correlations between temperament and production traitsa Trait
Ewe temperament rp
rg
Lamb temperament rp
rg
Ewe weight L0.40 ± 0.167 L0.44 ± 0.092 Ewe litter size 0.06 0.182 0.08 0.090 ADG 0-80 d 0.15 0.180 0.32 0.081 0.19 0.159 L0.44 0.078 ADG 80-120 d 0.27 0.156 L0.52 ± 0.085 ADG 5 mo 0.02 0.169 0.09 0.153 ADG, average daily gain. a Significant correlations are presented in bold.
are consistent with reports of Dodd et al. (2014) on relationships between behavior and carcass traits in lambs. The lack of significant phenotypic correlations between temperament and growth rates could be assigned to major environmental factors, such as the nutrition level. According to Dodd et al. (2014), the effect of nutrition might be greater than that of behavioral reactivity, thus masking the relationships between temperament and growth rate. Genetic correlations between temperament and growth rates during suckling (0-80 days) and the postweaning period (80120 days) were found to be significant (0.44 0.078, P 0.05 and 0.52 0.085, P 0.05, respectively). Thus, selection for calmer animals will have a positive impact on lambs’ growth rates during first 3 months of life and vice versa. Genetic parameter estimates for growth traits in South African Dorper breed are described by Zishiri et al. (2013b). Genetic correlations between behavioral reactivity and growth rates during the fattening period (at the age of 5 months) were found to be negative and nonsignificant (0.09 0.153, P > 0.05). Conversely, Pajor et al. (2013) reported the temperament in fattening lambs to be in close relationship with growth rate. Regrettably, because of the low number of Dorper purebreds found in Hungary, the available sample size included in the research trial was lower than desired, with some important production traits being left aside (e.g., lambs’ survival rate, ewe’s fertility). Furthermore, we consider that the current results need to be confirmed under different production systems, especially under adverse rearing conditions or extensive production systems, where the effects of temperament are expected to be more prominent. Conclusion Correlations between temperament and production traits suggested that selection against animals that are highly reactive to improve welfare and ease of handling would not have detrimental impacts on productivity. Furthermore, significant genetic correlations were found between lamb temperament and growth rates during their first 3 months of age. As a result, selection for calm temperaments should translate to increased growth rates of lambs. Acknowledgments This research was supported by the European Union and the State of Hungary, cofinanced by the European Social Fund in the framework of Hungarian National Development Agency (TÁMOP) 4.2.4.A/2-11-1-2012-0001 National Excellence Program. Conflict of interest The authors declare no conflict of interest.
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Authorship The idea for the article was conceived by Dinu Gavojdian. The experiments were designed by Dinu Gavojdian and Szilvia Kusza. The experiments were performed by Dinu Gavojdian and Csilla Budai. The data were analyzed by Ludovic T. Cziszter. The article was written by Dinu Gavojdian, Szilvia Kusza, Csilla Budai, and Ludovic T. Cziszter. References Amdi, C., Williams, A.R., Maloney, S.K., Tauson, A.H., Knott, S.A., Blache, D., 2010. Relationship between behavioral reactivity and feed efficiency in housed sheep. Anim. Prod. Sci. 50, 683e687. Bickell, S., Poindron, P., Nowak, R., Chadwick, A., Ferguson, D., Blache, D., 2009. Genotype rather than non-genetic behavioral transmission determines the temperament of Merino lambs. Anim. Welf. 18, 459e466. Blache, D., Ferguson, D., 2005. Boost lamb survivaldselect for calm ewes. Department of Agriculture, Western Australia. Available at: http://archive.agric.wa.gov.au. Accessed September 25, 2014. Blache, D., Bickell, S.L., 2011. External and internal modulators of sheep reproduction. Reprod. Biol. 11, 61e77. Boissy, A., Bouix, J., Orgeur, P., Poindron, P., Bibe, B., Le Neindre, P., 2005. Genetic analysis of emotional reactivity in sheep: effects of the genotypes of the lambs and of their dams. Gen. Select. Evol. 37, 381e401. Cloete, S.W.P., Snyman, M.A., Herselman, M.J., 2000. Productive performance of Dorper sheep. Small Rumin. Res. 36, 119e135. Dodd, C.L., Pitchford, W.S., Edwards, J.E., Hazel, S.J., 2012. Measures of behavioral reactivity and their relationships with production traits in sheep: a review. Appl. Anim. Behav. Sci. 140, 1e15. Dodd, C.L., Hocking, J.E., Hazel, S.J., Pitchford, W.S., 2014. Flight speed and agitation in weaned lambs: genetic and non-genetic effects and relationships with carcass quality. Livest. Sci. 160, 12e20. Erhard, H.W., Elston, D.A., Davidson, G.C., 2006. Habituation and extinction in an approachdavoidance test: an example with sheep. Appl. Anim. Behav. Sci. 99, 132e144. Ferguson, D.M., Warner, R.D., 2008. Have we underestimated the impact of preslaughter stress on meat quality in ruminants? Meat Sci. 80, 12e19. Grosu, H., Oltenacu, P.A., 2005. Programe de ameliorare genetica in zootehnie (Genetic improvement programs in animal husbandry), 1st ed. Ceres, Bucharest, Romania. Hawken, P.A.R., Fiol, C., Blache, D., 2012. Genetic differences in temperament determine whether lavender oil alleviates or exacerbates anxiety in sheep. Physiol. Behav. 105, 1117e1123. Hill, T., Lewicki, P., 2007. Statistics: Methods and Applications. StatSoft, Tulsa, OK. Horton, B.J., Miller, D.R., 2011. Validation of an algorithm for real-time measurement of sheep activity in confinement by recording movement within a commercial weighing crate. Appl. Anim. Behav. Sci. 129, 74e82. Konig von Borstel, U., Moors, E., Schichowski, C., Gauly, M., 2011. Breed differences in maternal behavior in relation to lamb (Ovis orientalis aries) productivity. Livest. Sci. 137, 42e48. Lambe, N.R., Conington, J., Bishop, S.C., Waterhouse, A., Simm, G., 2001. A genetic analysis of maternal behavior score in Scottish Blackface sheep. Anim. Sci. 72, 415e425.
Lennon, K.L., Hebart, M.L., Brien, F.D., Hynd, P.I., 2009. The genetics of temperament traits in Merino sheep. Adv. Anim. Breed. Gen. 18, 96e99. Martin, G.B., Milton, J.T.B., Davidson, R.H., Banchero, G.E., Lindsay, D.R., Blache, D., 2004. Natural methods for increasing reproductive efficiency in small ruminants. Anim. Reprod. Sci. 82-83, 231e246. Murphy, P.M., 1999. Maternal behavior and rearing ability of Merino ewes can be improved by strategic feed supplementation during late pregnancy and selection for calm temperament. PhD thesis, University of Western Australia. Njisane, Y.Z., Muchenje, V., 2013. Quantifying avoidance-related behavior and bleeding times of sheep of different ages, sex and breeds slaughtered at a municipal and a commercial abattoir. S. Afr. J. Anim. Sci. 43, S38eS42. Pajor, F., Szentleleki, A., Laczo, E., Tozser, J., Poti, P., 2008. The effect of temperament on weight gain of Hungarian Merino, German Merino and German Blackhead lambs. Arch. Tierzucht 51, 247e254. Pajor, F., Muranyi, A., Szentleleki, A., Tozser, J., Poti, P., 2010. Effect of temperament of ewes on their maternal ability and their lambs’ postweaning traits in Tsigai breed. Arch. Tierzucht 53, 465e474. Pajor, F., Kovacs, A., Tozser, J., Poti, P., 2013. The influence of temperament on cortisol concentration and metabolic profile in Tsigai lambs. Arch. Tierzucht 56, 573e580. Pickup, H.E., 2004. Maternal Behavior in the ewe: consistency in the expression of maternal behavior during lactation and the effect of variation in dam and sire breed on the development of offspring. PhD thesis, University of Edinburgh. Plush, K.J., Hebart, M.L., Brien, F.D., Hynda, P.I., 2011. The genetics of temperament in Merino sheep and relationships with lamb survival. Appl. Anim. Behav. Sci. 134, 130e135. Reale, D., Gallant, B.Y., Leblanc, M., Festa-Bianchet, M., 2000. Consistency of temperament in bighorn ewes and correlates with behavior and life history. Anim. Behav. 60, 589e597. Schaeffer, L.R., 2014. Course notesdthreshold models, University of Guelph, Gurlph, Ontario. Available at: http://www.aps.uoguelph.ca/wlrs/ABModels/NOTES/ thresh.pdf. Accessed September 25, 2014. Sejian, V., Maurya, V.P., Naqvi, S.M.K., Kumar, D., Joshi, A., 2010. Effect of induced body condition score differences on physiological response, productive and reproductive performance of Malpura ewes kept in a hot, semi-arid environment. J. Anim. Physiol. Anim. Nutr. 94, 154e161. Snowder, G.D., Duckett, S.K., 2003. Evaluation of the South African Dorper as a terminal sire breed for growth, carcass, and palatability characteristics. J. Anim. Sci. 81, 368e375. Vierin, M., Bouissou, M.F., 2003. Responses of weaned lambs to fear-eliciting situations: origin of individual differences. Dev. Psychobiol. 42, 131e147. Wolf, B.T., McBride, S.D., Lewis, R.M., Davies, M.H., Haresign, W., 2008. Estimates of the genetic parameters and repeatability of behavioral traits of sheep in an arena test. Appl. Anim. Behav. Sci. 112, 68e80. Yilmaz, M., Altin, T., Karaca, O., Cemal, I., Bardakcioglu, H.E., Yilmaz, O., Taskin, T., 2011. Effect of body condition score at mating on the reproductive performance of Kivircik sheep under an extensive production system. Trop. Anim. Health Prod. 43, 1555e1560. Zishiri, O.T., Cloete, S.W.P., Olivier, J.J., Dzama, K., 2013a. Genetic parameters for growth, reproduction and fitness traits in the South African Dorper sheep breed. Small Rumin. Res. 112, 39e48. Zishiri, O.T., Cloete, S.W.P., Olivier, J.J., Dzama, K., 2013b. Genetic parameter estimates for subjectively assessed and objectively measured traits in South African Dorper sheep. Small Rumin. Res. 109, 84e93.
Contents lists available at ScienceDirect
Journal of Veterinary Behavior journal homepage: www.journalvetbehavior.com
Research
Effects of behavioral reactivity on production and reproduction traits in Dorper sheep breed Dinu Gavojdian a, b, *, Ludovic T. Cziszter c, Csilla Budai a, Szilvia Kusza a a
Institute of Animal Science, Biotechnology and Nature Conservation, University of Debrecen, Debrecen, Hungary Research and Development Station for Sheep and Goats, Romanian Academy for Agricultural and Forestry Sciences, Caransebes, Romania c Department of Animal Production Engineering, Banat’s University of Agricultural Sciences and Veterinary Medicine ‘King Michael I of Romania’, Timisoara, Romania b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 January 2015 Received in revised form 23 February 2015 Accepted 27 March 2015 Available online 9 April 2015
The aim of the current research was to evaluate the effects of behavioral reactivity on production and reproduction performance in Dorper sheep, a meat breed. Temperament of animals was subjectively evaluated using a 5-point scoring system at weighing, during which sheep spent 30 seconds on the scale. The heritability of temperament was low (0.10 0.03). Estimated phenotypic (rp) and genetic (rg) correlations between temperament and litter size in ewes were negative and negligible (P > 0.05) at 0.06 0.18 and 0.08 0.09, respectively. Significant genetic correlations were found between lamb temperament and preweaning growth rate (rg ¼ 0.44 0.07, P 0.05) and postweaning growth till the age of 120 days (rg ¼ 0.52 0.08, P 0.05). Significant genetic correlations were found between lamb temperament and growth rates during their first 3 months of age. As a result, selection for calm temperaments should translate to increased growth rates of lambs. Negative correlations between temperament and production traits, both in ewes and lambs, suggested that selection against animals that are highly reactive to improve welfare and ease of handling would not have detrimental impacts on productivity. Ó 2015 Elsevier Inc. All rights reserved.
Keywords: Dorper breed behavior genetic parameters growth rates sheep welfare temperament
Introduction Temperament in livestock species can be defined as the manner in which an individual reacts to a novel or challenging situation (Reale et al., 2000), and assessing temperament has been suggested as a useful tool for improving productivity in sheep (Dodd et al., 2012). Temperament has been shown to have an effect on lamb survival and growth rate (Murphy, 1999; Pajor et al., 2008), meat quality (Ferguson and Warner, 2008), and sheep reproductive performance (Blache and Bickell, 2011). Moreover, animals that are highly reactive to humans and handling exhibit poor adaptation to their environment and experience high levels of stress, reducing their level of welfare (Bickell et al., 2009).
Sheep temperament is regarded to be low to moderately heritable, thus making it a suitable trait for genetic selection (Lennon et al., 2009; Plush et al., 2011; Hawken et al., 2012). However, variation of temperament heritability between sheep breeds has been reported (Blache and Ferguson, 2005). When selecting sheep based on behavioral reactivity, it is important that the subsequent impact on other aspects of productivity is understood (Dodd et al., 2014). Dorper is among the very few sheep breeds to have temperament included as selection trait in the breed’s standard in native South Africa (Njisane and Muchenje, 2013). The aim of the current research was to evaluate the effects of behavioral reactivity on production and reproduction performances in Dorper meat breed. Materials and methods
* Address for reprint requests and correspondence: Dinu Gavojdian, Research and Development Station for Sheep and Goats, Romanian Academy for Agricultural and Forestry Sciences, Caransebes 325400, Romania. Tel: þ40 723 375 804; Fax þ40 356 456 400. E-mail address: [email protected] (D. Gavojdian). http://dx.doi.org/10.1016/j.jveb.2015.03.012 1558-7878/Ó 2015 Elsevier Inc. All rights reserved.
Animals and management The study was carried out at the Experimental Farm of the University of Debrecen (47 330 N/21420 E), between February and
366
D. Gavojdian et al. / Journal of Veterinary Behavior 10 (2015) 365e368
July 2014. Purebred Dorper sheep were managed semi-intensively under an accelerated mating system (3 lambings/2 years). The Debrecen region has a typical Central European humid continental climate. At the research station, which is located at an elevation of 121 m above sea level. The total annual precipitation is 566 mm, with a mean annual temperature of 9.85 C. Temperatures show seasonal patterns with summer daily means of 20.3 C in July and winter daily means of 2.6 C in January. Data from 161 animals (72 ewes, 86 lambs, and their sires) and more than 720 records were analyzed for estimation of the genetic parameters for temperament and correlations of behavioral reactivity with production traits. Ewes were between 1.5 and 8 years old, with balanced age and parity within the flock and representing a diverse sampling of genetic lines (imported from Austria, Canada, Germany, and Romania). Individual lamb record data included birth type, sex, ear tag number, birth date, dam and sire, temperament (lamb, dam, and sire temperament scores), and lamb weight at birth and at 80, 120, 140, and 150 days of age (International Committee for Animal Recording [ICAR] “B” method). For adult ewes, body weight before the next reproduction season (1.5 months after litter weaning), litter size, and temperament were recorded. Lambs were weaned at 80 days and fed ad libitum with medium-quality lolium hay (8 megajoules [MJ] metabolizable energy [ME]/kg dry matter [DM]) and commercially available pellets (16% protein, 10.6 MJ/kg DM). During lactation and after weaning, the lamb’s ewes received a high-quality alfalfa hay (9.5 MJ ME/kg DM) ad libitum, and while suckling, they received concentrated supplements (200 g/d). The concentrate was comprised of corn (50%), wheat (20%), soybean meal (18%), sunflower meal (10%), calcium (1%), and a vitamine mineral supplement (1%). In addition, all animals had free access to potable water and mineral blocks. Both ewes and their lambs were kept confined on deep straw bedding, with a space allowance of 1.2 and 1 m2, respectively. All data were recorded in a single reproductive cycle to limit to the extent possible the effects of farm, year, and season. The Dorper breed was introduced in Hungary in 2008, with a current census of roughly 100 breeding ewes being registered in the breed’s herd book. The Hungarian Sheep and Goats Breeders Association manages the performance and recording scheme for the breeds. The production system focuses exclusively on meat production, with Dorper rams being used as terminal sires for the improvement of growth rates and carcass qualities in crossbreeding schemes with native breeds (Tsigai and Zackel). All research activities were performed in accordance with the European Union’s Directive for animal experimentation (Directive 2010/63/EU). Temperament assessment Temperament was assessed according to the scale test method described by Pajor et al. (2010) and Dodd et al. (2012), a subjective restraint method used to evaluate behavioral reactivity and fear response to handling. Temperament was scored at an age of 5 months for the lambs and right before admission to reproduction for the ewes. Behavior of all animals was recorded using a 5-point score system at weighing, where all animals spent 30 seconds on the scale: 1dcalm, no movement; 2dcalm with occasional movements; 3dmoderately movements; 4dabrupt episodic movements; and 5dcontinuous episodic movements. Scoring was done by 2 independent observers and videorecorded for re-evaluation, in case of divergent scoring. Based on temperament scores given, lambs and ewes were classified as either calm (scores 1 and 2) or nervous (scores 3, 4, and 5).
Statistical analysis Heritability was estimated using the threshold model described by Schaeffer (2014):
. h2temperament ¼ h2liability *z2 ðpð1 pÞÞ where h2liability is the heritability under normal distribution scale, z is the height of the normal curve at the threshold point (on the observed scale), and p is the proportion of observations in 1 category. The model included as fixed effects the lambs and birth type (singleton, twins, or triplets) and as random factors the dam and sire temperament scores. Phenotypic and genetic correlations of temperament scores of ewes and lambs with production traits were estimated using the analysis of variance described by Grosu and Oltenacu (2005). Comparisons between temperament scores for ewe weight at mating, litter size, and lamb growth rates were carried out using an analysis of variance main effects model. Chi-squared tests were performed to determine if ewe temperament influenced the litter size. All the statistical tests were done using Statistica software (StatSoft Inc.) (Hill and Lewicki, 2007). All decisions about the acceptance or rejection of statistical hypothesis were made at the 0.05 level of significance.
Results and discussions The heritability (standard error of the mean) of temperament in Dorper breed was low (h2 ¼ 0.10 0.031) and consistent with previous estimates in sheep (Plush et al., 2011; Dodd et al., 2014), which found low to moderate heritabilities for flight speed and agitation score. Conversely, Martin et al. (2004) estimated the heritability of temperament in sheep to be around 0.23 for the Allandale flock, which has been intensively selected for calm temperament over a period of 10 years. Notable breed disparities for behavior of sheep have been reported in a series of studies (Vierin and Bouissou, 2003; Pickup, 2004; Boissy et al., 2005; Konig von Borstel et al., 2011) and highlight the differences in propensity for behavioral reactions. This behavioral variation might contribute to differences for the heritability among sheep breeds. Despite that temperament was found to have a low heritability in the Dorper, given the feasibility of the scale test that can be easily applied at farm level, with both lambs and ewes being scaled on a regular basis (e.g., for drenching, performance recording), sheep breeders alone could assess the temperament of their sheep. Moreover, the scale test was found to have one of the highest repeatability (up to 0.71) when compared with other tests used to evaluate ovine behavioral reactivity (Dodd et al., 2012). Dorper lambs showed a higher behavioral reactivity (2.78 0.20) compared with their dams (2.40 0.16). Temperament scores of lambs are similar to those reported by Pajor et al. (2013) in Tsigai fattening lambs, evaluated by the same method. Habituation to handling might have contributed to the lower behavioral reactivity of ewes, as previously outlined by Erhard et al. (2006). Temperament of ewes had no significant effect (c2 ¼ 0.276, degrees of freedom ¼ 5, P ¼ 0.99) on the birth type, distribution of litter size was 53% singletons, 35% twins, and 12% triplets in ewes ranked as calm and 60% singletons, 27% twins, and 13% triplets in nervous ewes. Despite calmer ewes outperforming those ranked as nervous, and that less reactive lambs achieving higher growth rates (Table 1), differences between the 2 counterparts were not significant (P > 0.05). Results for ewes’ body weight are consistent with those previously reported (Amdi et al., 2010; Wolf et al., 2008), in which
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Table 1 Means (SEM) for productive performances of ewes and lambs based on their temperament Trait Ewes performance Ewes weight (kg) Ewes litter size (%) Lambs ADG 0-80 d (g)b Lambs performance ADG 0-80 d (g) ADG 80-120 d (g) ADG 5 mo (g)
Cohort
Calm
Nervous
Differencesa
58.66 1.50 156.30 0.12 383.43 11.08
60.29 2.23 158.80 0.17 393.19 16.08
56.81 1.94 153.30 0.19 372.38 15.13
3.48NS 5.5NS 20.81NS
380.17 10.60 286.09 13.45 345.95 18.90
394.72 13.76 298.32 23.05 349.21 24.20
366.39 15.71 274.52 14.62 342.86 29.43
28.34NS 23.80NS 6.35NS
ADG, average daily gain; NS, not significant. a Calm versus nervous animals. b Regarded as dam effect.
no relationship was found between behavior and live weight, even if calmer ewes were heavier (þ3.48 kg, P > 0.05) than their nervous counterparts. Litter size of ewes was higher compared with data reported for the breed by Zishiri et al. (2013a), with calm ewes being more prolific (þ5%) compared with nervous animals. Growth rate of lambs from birth to weaning was attributed to maternal effects on growth rate until weaning, as previously demonstrated in the Dorper breed (Zishiri et al., 2013b). Lambs reared by calmer dams exhibited higher growth rates (þ20.8 g, P > 0.05) compared with those born by more reactive ewes. Lambe et al. (2001) found a positive genetic correlation (0.4) between ewe maternal score and lambs weight gain, demonstrating the importance of the temperament of ewes. Growth performances of lambs were higher compared with those reported by Cloete et al. (2000) and consistent with those of Snowder and Duckett (2003). Lowest growth rates were achieved by lambs during the 80-120 day interval, showing that postweaning stress affects the trait to a great extent. Less reactive lambs had higher growth rates compared with nervous lambs, in agreement with reports of Pajor et al. (2010) and of Horton and Miller (2011). Correlations, both genetic and phenotypic, between ewe behavioral reactivity and litter size and growth rates of unweaned lambs were negative in sign and not significant (P > 0.05) (Table 2). Significant negative phenotypic (rp ¼ 0.40, P 0.05) and genetic (rg ¼ 0.44, P 0.01) correlations were found between ewe temperament and body weight, thus, the more reactive the ewe the lower its body weight. In general, ewes in good body condition are desired because they tend to have higher reproductive performances (estrus onset, ovulation and conception rates, etc.) as reported by Sejian et al. (2010) and Yilmaz et al. (2011). The low heritability of temperament in the Dorper breed linked to its negligible negative genetic correlation with litter size suggests that selection for temperament traits will result in negligible genetic gain for prolificacy. Phenotypic correlations between temperament and average daily gains in lambs were nonsignificant (P > 0.05). These results
Table 2 Phenotypic (rp) and genetic (rg) correlations between temperament and production traitsa Trait
Ewe temperament rp
rg
Lamb temperament rp
rg
Ewe weight L0.40 ± 0.167 L0.44 ± 0.092 Ewe litter size 0.06 0.182 0.08 0.090 ADG 0-80 d 0.15 0.180 0.32 0.081 0.19 0.159 L0.44 0.078 ADG 80-120 d 0.27 0.156 L0.52 ± 0.085 ADG 5 mo 0.02 0.169 0.09 0.153 ADG, average daily gain. a Significant correlations are presented in bold.
are consistent with reports of Dodd et al. (2014) on relationships between behavior and carcass traits in lambs. The lack of significant phenotypic correlations between temperament and growth rates could be assigned to major environmental factors, such as the nutrition level. According to Dodd et al. (2014), the effect of nutrition might be greater than that of behavioral reactivity, thus masking the relationships between temperament and growth rate. Genetic correlations between temperament and growth rates during suckling (0-80 days) and the postweaning period (80120 days) were found to be significant (0.44 0.078, P 0.05 and 0.52 0.085, P 0.05, respectively). Thus, selection for calmer animals will have a positive impact on lambs’ growth rates during first 3 months of life and vice versa. Genetic parameter estimates for growth traits in South African Dorper breed are described by Zishiri et al. (2013b). Genetic correlations between behavioral reactivity and growth rates during the fattening period (at the age of 5 months) were found to be negative and nonsignificant (0.09 0.153, P > 0.05). Conversely, Pajor et al. (2013) reported the temperament in fattening lambs to be in close relationship with growth rate. Regrettably, because of the low number of Dorper purebreds found in Hungary, the available sample size included in the research trial was lower than desired, with some important production traits being left aside (e.g., lambs’ survival rate, ewe’s fertility). Furthermore, we consider that the current results need to be confirmed under different production systems, especially under adverse rearing conditions or extensive production systems, where the effects of temperament are expected to be more prominent. Conclusion Correlations between temperament and production traits suggested that selection against animals that are highly reactive to improve welfare and ease of handling would not have detrimental impacts on productivity. Furthermore, significant genetic correlations were found between lamb temperament and growth rates during their first 3 months of age. As a result, selection for calm temperaments should translate to increased growth rates of lambs. Acknowledgments This research was supported by the European Union and the State of Hungary, cofinanced by the European Social Fund in the framework of Hungarian National Development Agency (TÁMOP) 4.2.4.A/2-11-1-2012-0001 National Excellence Program. Conflict of interest The authors declare no conflict of interest.
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