Genetic and Phenotypic Variation in Prelaying Behavior of Leghorn Hens Kept in Single Cages

BREEDING AND GENETICS Genetic and Phenotypic Variation in Prelaying Behavior of Leghorn Hens Kept in Single Cages G. HEIL Institut flir Kleintierzucht, DSrnbergstrasse 25127, D-3100 Celle, Federal Republic of Germany H. SIMIANER Institut flir Tierhaltung und Tierziichtung der UniversitUt Hohenheim, Garbenstrasse 17, D-7000 Stuttgart, Federal Republic of Germany

Lehrstukl fur Tierzucht der TV MUnchen-Wiehenstephan D-8050 Freising, Federal Republic of Germany (Received for publication September 29, 1989) ABSTRACT Prelaying activity of hens in single cages was observed on time-lapsed video. The partially pedigreed hens came from five different Leghorn strains. In four of these strains, hens from three successive generations were observed. The following traits were investigated: duration of restlessness before oviposition; escaping frequency with which the hens put their head through the front of the cage from 10 to 5 min before oviposition; and stance during oviposition (standing or sitting). Differences among strains were significant for all traits. Heritability estimates and standard errors for traits based on one oviposition were .06 ± .07, .04 ± .06, and .33 ± .08 for duration, escaping, and stance, respectively. Heritability estimates increased to .12, .09, and .53, respectively, if the traits were observed in five oppositions per hen. Results indicated that population means can be changed by selection if progeny testing is used. The cost of such selection would be justified only when the connection between these traits and animal welfare is better understood. (Key words: prelaying behavior, repeatability, strain differences, age, heritability) 1990 Poultry Science 69:1231-1235 nSTTRODUCnON

The activity of caged hens before oviposition is important because of poultry welfare and economic implications. Mills (1987) reviewed problems that can arise with undesirable prelaying behavior from both the poultry welfare and economic implications and concluded that selection for certain behavioral traits offers at least a partial solution to problems in these areas. Before successful breeding strategies can be developed, one has to know if the traits under consideration show genetic variability. In the present study, the genetic and phenotypic variation of three traits of prelaying activity for hens kept in single cages was investigated using observations from time-lapse video film. MATERIALS AND METHODS

The investigation involved 491 hens from five White Leghorn strains, with four studied

in tiiree successive generations (Table 1). Strains B, H, and V had their origin in one of three different commercial Leghorn crossbreds. Over two generations each were randomly mated using 30 sires and ISO dams. Since then, the strains were part of an investigation in which the suitability of different traits for improving the egg shell quality by selection was being examined (Hartmann et al., 1984). The strains have been selected for three generations for high egg shell strength (Strain B), low egg shell deformation (Strain H), or high specific egg weight (Strain V). Strains K and L originated from cross-breeding of eight Leghorn populations, which were selected for 10 generations for low (Strain K) or high (Strain L) initial egg weight (Hilfiker and Lortscher, 1972). Since 1973, these strains have also been kept in the Institute of Poultry and Small Animals in Celle where they have been reproduced by random mating with 10 sires and 100 dams per strain.

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L. DEMPFLE

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HEIL£XJ4L.

TABLE 1. Number of hens observed Strain Generation

B

H

V

L

K

1 2 3

56 38 47

20 38 48

48 42 46

14 26 45

23

Y ij]dm = p. + LGAjjt + haiji + hpyi + (a x ha)ijki + (a x h p ) ^ where Yipdm is the average of two observations of different persons of the nr* oviposition of the 1th hen in the k"1 age class that descended from the j " 1 generation of the i"1 strain; \L is the overall mean; LGAjjk is the fixed effect of the i"1 strain in the j * generation in the k m age class; ha^i is the random additive gene effect of the 1th hen from the j " 1 generation of the i * strain; h p ^ is the random permanent effect (excluding additive gene effects) of the 1th hen from the j * generation of the i"1 strain; (a x ha)iju are the random interaction effects between the age class k and the additive gene effects of the 1™ hen from the jto generation of the 1th strain; (a x hp)jju are the random interaction effects between the age class k and permanent effects of the 1th hen from the J* generation of the r31 strain; and eijklm is the random error. Variance components of the random effects were estimated using iterative Minimum Variance Quadratic Unbiased Estimation (MTVQUE; Rao, 1971) leading to Restricted Maximum Likelihood (REML; Patterson and Thompson, 1971) estimates. Using these values, best linear unbiased estimators of the fixed effects were obtained. In the matrix of relationships, all covariances between the

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For strains B, H, V, and L, an average of 40 dams and their daughters were observed. Average number of daughters per dam was 2.1. Because hens were kept in single cages, reproduction was by artificial insemination with pooled semen from an average of 15 cocks. As a rule, these cocks did not descend from hens whose prelaying activity was observed. An average of 2.4 ovipositions per hen were observed for the following three traits: 1. Duration of restlessness before oviposition (minutes). 2. Escape behavior as measured by counting how often each hen put her head through the cage front from 10 to 5 min before oviposition (number per 5 min). This trait is expected to describe the intensity of the restlessness before laying. 3. Stance (standing or sitting) of the hen when laying as measured on the binomial scale. The activity was recorded at the beginning of the daily light period of 16 h at 0400 h. To avoid large influences of the time of day, prelaying behavior of only those ovipositions taking place between 0700 and 1200 h were included. Each hen of the first generation was filmed on 3 different days during one of the following observation periods: 8th to 11th (Strain B), 16th to 20th (Strains V and K), or 25th to 26th mo of age (Strains B, H, V, and L). The hens were force-molted before the third observation period. Hens of the second and third generations were filmed three times from the 8th to 11th and three times from the 16th to 20th mo of age. For 63% of the hens of the second and third generation at least one oviposition in both periods was observed. To investigate the precision of measurements and the predictability of future behavior of a hen, three different correlation coefficients were estimated. The correlations estimated were: 1. Correlations between the scores of two independent observers of a trait measured

during one oviposition. These are a measure of the precision of a single . observation. 2. Correlations between the average scores from two observers of two random ovipositions of the same hen within 3 mo. These are a measure of the predictability of future behavior taking place within a short time. 3. Correlations between the average scores from two observers of two random ovipositions of the same hen within 5 to 12 mo. These are a measure of the predictability of future behavior taking place after a longer time. The above correlation coefficients are related to repeatabilities. The estimates of the different correlations were calculated within each line, generation, and, for correlations 1 and 2, period combination, and subsequently pooled. For the genetic analysis the following statistical model was used.

GENETICS OF PRELAY1NG BEHAVIOR TABLE 2. Correlation coefficients estimated between scores of the same trait of different observations of the same hen

Comparisons Between observers within oviposition Between ovipositions within 3 mo Between ovipositions within 5 or more mo

TABLE 3. Average differences and their standard errors between traits of hens aged 8 to 11 mo and 16 to 20 mo

Relaying behavior trait Duration Escaping Stance Strain .92

.88

.72

.46

.38

.60

.28

.21

.24

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B H V L _ Pooled X

Prelaying behavior trait1 Duration Escaping Stance Difference2 Difference Difference (percentage (min) (n per 5 min) sitting) 31 ± 7.8 1.9 ± .85 10 ± 9.5 35 ± 7.3 -2 ± .77 1 ± 9.1 25 ± 7.3 .3 1 .77 1 ± 9.1 22 ± 9.8 .3 ± 1.05 2 ± 11.5 28 ± 4.0 .6 ± .43 3 ± 4.9

breeding values of the hens were considered. It has been assumed that all cocks from which semen had been obtained and mixed contributed with the same probability to the following generation. When variance components were negative, they were set to 0 in the model. Heritabilities were calculated based on the following formula.

within 3 mo. Further increase in time between two observations decreased further the correlation coefficient estimates. These results are consistent with correlation estimates for other traits of prelaying behavior (Heil, 1987) calculated from original data of different sources (Wood-Gush and Gilbert, 1969; Martin, 1975; Mills, 1983). However, the traits investigated in the present ^ha + ^ p + ^axha) + ^axhp) + ^ study had much lower correlations between The variances of the heritability estimates were ovipositions than the traits "number of steps per calculated by the Taylor series approximation minutes in the 10 min before laying" and "the proportion of time the hen spent sitting in the (Kendall and Stuart, 1969). same period", for which traits, Mills et al. (1985) estimated the intraclass correlations RESULTS AND DISCUSSION between ovipositions as .8 on average. They Means and standard deviations of the calculated their estimates within two strains duration of restlessness (minutes), escape each on the basis of five birds scored five times. behavior (number per 5 min), and stance when The five observations were made at random laying (percentage sitting) were 66 ± 45, 4.3 ± intervals when the animals were between 26 and 4.7, and 18 ± 35, respectively. All three traits 52 wk of age. The strains they used were very show a large variability between individual different in regard to origin and behavior. oviposition. The distribution of duration and Whether this distinction can be explained by escaping was skewed. In both traits, few different observation methods or whether strain observations have extremely high values. In differences in variability of behavior exist 82% of the cases, the stance was standing cannot be answered on the basis of these data. during oviposition. Age Influences Correlation Coefficients In Table 3, the average differences between The data in Table 2 shows that the observa- age of 8 to 11 mo and 16 to 20 mo are given. The tion of a single oviposition provided sufficient duration of restlessness was more or less precision. An intermediate precision was esti- reduced by .5 h in all strains, on average, from 81 mated for the prediction of future behavior to 53 min. This change corresponds to a

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Duration = duration of restlessness before oviposition (minutes); Escaping = behavior measured by counting how often each hen put her head through the cage front from lOto 'Duration = duration of restlessness before oviposition; 5 min before oviposition (number per 5 min); Stance = Escaping = behavior measured by counting how often each stance (standing or sitting) when laying (percentage sitting). hen put her head through the cage front from 10 to 5 min before oviposition; Stance = stance (standing or sitting) when laying. 2 Difference ( X ^ n „„, - X16_2o W -

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tfESLET AL.

TABLE 4. Strain means and their standard errors of the observations in Generations 1 (after molting), 2, and 3

Strain

Relaying behavior trait1 Duration Escaping Stance

reduction of the starting value by a third. However, the hens showed large variability in the changes observed with advancing age. From 210 hens laying at least one egg in both periods, 51 hens showed an increase in duration with an increase in age. The changes observed with advancing age were relatively small for the traits of escaping and stance. They were not statistically significant either on average or in any of the strains. The largest differences were shown by the hens in Strain B. With these, the escaping behavior reduced from 6.2 to 4.3 units of measure and the proportion of hens that laid their eggs while sitting had decreased from 23 to 13%. Genetic Differences Between Strains To investigate the possibility of strain differences, the data of Strains B, H, V, and L of Generations 1 (observation after molting), 2, and 3 were used. The strain means of all generations are shown in Table 4. Significant differences between strains can be explained by genetic differences and could be influenced by the individual history of the strains. However, the phenotypic variances make clear that differences between hens within a strain were distinctly larger than the strain differences. On the basis of their behavioral traits, hens cannot be clearly distinguished as being from a particular strain.

Relaying behavior trait1

&&

fi2

SE

Duration (min) Escaping (n per 5 min) Stance (% sitting)

9.4 .96 .21

.06 .04 .33

.07 .06 .08

1

Duration = duration of restlessness before oviposition; Escaping = behavior measured by counting how often each hen put her head through the cage front from 10 to 5 min before oviposition; Stance = stance (standing or sitting) when laying.

five strains. Although a method of calculating was used that made use of all relative relationships to estimate the additive genetical variance, the values of the individual strains were too inaccurate to test if differences in heritability exist between the strains. The values for the different strains are therefore not shown. All traits exhibited considerable genetic variation. Estimates in Table 5 show the heritability for traits of hens with only one oviposition recorded from two independent observers. Heritability estimates increased when the precision of the data was improved by observing more ovipositions per hen. When 5 oppositions were observed for each hen, the heritability estimate values increase to .12 for duration and to .09 for escaping. For both traits, the heritability estimates are then about as high as for egg production. For the "stance" behavior, the estimate increased to .53 where based on five ovipositions. This value corresponds to the heritability of egg weight. If more ovipositions are observed for each hen, the heritabilities increase only slowly to the limits of .16, .11, and .65, respectively, which are nearly reached after about 20 to 25 observed ovipositions. Relationships Between Traits Correlations between the traits, which were calculated on the basis of each individual oviposition, were low and not statistically significantly different from 0. Based on strain averages, the correlation coefficients were: duration and escaping, .07; duration and stance, -.05; escaping and stance, .004. The correlation coefficients indicate that the prolonging behavior traits were independent

Genetic Differences Within Strains Expected Effects of Selection The data in Table 5 show estimated values for the additive genetic variance and the heritabiliThe traits of prelaying activity observed ties. These estimates were pooled values for the with the help of video recordings have large

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(min) (n per 5 min)(% sitting) 55 ± 3.6 5.1 ± .40 20 ± 4.6 72 ± 3.4 3.5 ± .36 17 ± 4.4 63 ± 3.4 2.3 ± .36 19 ± 4.4 62 ± 4.5 7.7 ± .48 6 ± 5.4 1 Duration = duration of restlessness before oviposition; Escaping = behavior measured by counting how often each hen put her head through the cage front from 10 to 5 min before oviposition; Stance = stance (standing or sitting) when laying. B H V L

TABLE 5. Estimated values of additive genetic standard deviations and heritabilities

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GENETICS OF PRELAYING BEHAVIOR

The question remains as to how the large environmental variance observed in these three traits is valued in respect to the adaptation of animals to cages. Differences of this order between and within hens have been described in several studies. They were published first by Schjelderup-Ebbe (1923) for the trait duration of restlessness before oviposition of hens kept in ranges. Similar variation is found in physiological changes that can be observed in connection with the oviposition; for example, the rise in the corticosterone level of the blood (Beuving and Wonder, 1981), the rise in body

temperature (Bobr and Sheldon, 1977), and the increase of energy expenditure (Van Kampen, 1976). ACKNOWLEDGMENTS

The authors would like to thank Yutta Emmerich-Seidlitz and Kerstin Krosmann for their excellent technical assistance and Michelle Fountain for her help in English translation. REFERENCES Bobr, L. W., and B. L. Sheldon, 1977. Analysis of ovulationoviposition patterns in the domestic fowl by telemetry measurement of deep body temperature. Aust. J. Biol. Sci. 30:243-257. Beuving, G., and G.MA Vonder, 1981. The influence of ovulation and oviposition on corticosterone levels in the plasma of laying hens. Gen. Comp. Endocrinol. 44: 382-388. Hartmann, W., G. HeiL and H. W. Rauch, 1984. Effect of differences in certain egg shell traits on the frequency of broken eggs in laying hens. Pages 153-157 in Proc. XVH World's Poult. Congr., Helsinki, Finland. HeiL G., 1987. Die UnruhevordemLegen-einMerkmalmit groffer Vielfalt Dtsch. Geflugelwirtschaft Schweineproduktion 39:562-567. Hilfiker, J., and H. Ldrtscher, 1972. Untersuchungen fiber die Erblichkeit des Eigewichts bei Legebeginn (Selektionsversuch bei Geflugel). Arch. Geflugelkd. 36: 81-88. Kampen, Van, M., 1976. Activity and energy expenditure in laying hens. 1. The energy cost of nesting activity and oviposition. J. Agric. Sci. Camb. 86:471-473. Kendall, M. G., and A. Stuart, 1969. Page 232 in The Advanced Theory of Statistics. Vol. 1. Griffin, London, England. Martin, G., 1975. Uber VerhaltensstOrungen von Legehennen im KSfig. Angew. Ornithol. 4:165-176. Mills, A. D., 1983. Pages 153-156 in: Genetic analysis of strain differences in pre-laying behavior in the fowl. PhD. Diss., University of Edinburgh, Scotland. Mills, A. V., 1987. Select for desirable pre-laying behaviour. Poultry 3:8-13. Mills, A. D., D.G.M. Wood-Gush, and B. O. Hughes, 1985. Genetic analysis of strain differences in pre-laying behaviour in battery cages. Br. Poult. Sci. 26:187-197. Patterson, H. D., and R. Thompson, 1971. Recovery of interblock information when block sizes are unequal. Biometrika 32:545-554. Rao, C. R., 1971. Minimum variance quadratic unbiased estimation of variance components. J. Multivar. Anal. 1:445-456. Schjelderup-Ebbe, T., 1923. Weiteie Beitrage zur Sozial und individualpsychologie des Haushuhnes. Z. Psychol. 92:60-87. Wood-Gush, D.G.M., and A. B. Gilbert. 1969. Observations of the laying behaviour of hens in battery cages. Br. Poult Sci. 10:29-36.

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phenotypic variation. But the relatively low heritability estimates point at a small amount of additive genetic effects. The differences between Leghorn strains and the absolute value of the additive gnetic variance nevertheless show that the behavior of populations can be changed by selection. If negative correlations exist between behavioral traits and the fitness of animals in a particular environment or between selection traits of the breeder, the populations will adapt to the given conditions through natural selection. However, based on the genetic parameters, only small changes between one generation and the following are to be expected by natural selection. Larger differences are obtainable through artificial selection, although this requires large expenses. As the heritability estimates for duration and escaping correspond with those of the egg production, similar response to selection in the behavior traits as for the production traits are to be expected if one uses accurate selection methods. This means that breeding values should be estimated by testing offspring by recording the prelaying behavior of several ovipositions per hen. Changing the behavior of populations is financially expensive and it should be clear whether such procedures result in better adaption of the population to the environment and an improvement in animal welfare. For this evaluation, the genetic relationships among behavioral traits and traits of welfare have to be known. To evaluate the welfare, the following traits should be considered: fear, the reaction to frustration; rise in heart rate, body temperature, and in the corticosterone values of the blood before oviposition; disease resistance; and health.